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THE JOURNAL

OF

COMPARATIVE NEUROLOGY

EDITORIAL BOARD

Henry H. DonaLpson ApoLF MEYER

The Wistar Institute Johns Hopkins University
J. B. JoHNSTON Ouiver S. STRONG

University of Minnesota Columbia University

C. JupDSON HERRICK, University of Chicago
Managing Editor

VOLUME 29

FEBRUARY—-OCTOBER, 1918

PHILADELPHIA, PA.

THE WISTAR INSTITUTE OF ANATOMY AND BIOLOGY

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lala ea

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CONTENTS

1918

No.1. FEBRUARY

Naoki Suaira. Comparative studies on the growth of the cerebral cortex. III. On
the size and shape of the cerebrum in the Norway rat (Mus norvegicus) and a com-
parison of these with the corresponding characters in the albino rat. Two charts
DIT MFA KOW Stab Rg ctst SAR Ee ea ee oC ee ER AST AR AL Ea Co eyed ne tat Lc

Naoxr Sucira. Comparative studies on the growth of the cerebral cortex. IV. On
the thickness of the cerebral cortex of the Norway rat (Mus norvegicus) and a com-
parison of the same with the cortical thickness in the albino rat. Ten charts.......

Suinxisur Harar. Metabolic activity of the nervous system. II. The partition of
non-protein nitrogen in the brain of the gray snapper (Neomaenis griseus) and also
the brain weight in relation to the body length of this fish. One chart.............

No. 2. * APRIL

Naoxi Sueira. Comparative studies on the growth of the cerebral cortex. V. Part I.
On the area of the cortex and on the number of cells in a unit volume, measured on
the frontal and sagittal sections of the albino rat brain, together with the changes in
these characters according to the growth of the brain. V. Part II. On the area of
the cortex and on the number of cells ina unit. volume, measured on the frontal and
sagittal sections of the brain of the Norway rat (Mus norvegicus), compared with
the er responding data for the albino rat. Three figures and four charts...........

NAOKI £ TA. Comparative studies on the growth of the cerebral cortex. VI. Part
I. On tie increase in size and on the developmental changes of some nerve cells in
the cerebral cortex of the albino rat during the growth of the brain. VI. Pari IT.
On the increase in size of some nerve cells in the cerebral cortex of the Norway rat
(Mus norvegicus), compared with the corresponding changes in the albino rat. Six
LIP RICCSeAT Ohi OME IEA eR Nee ee se ee ee i eee ese eae, Pte ain ari hans

W. J. Crozier. On tactile responses of the de-eyed hamlet (Epinephelus striatus)......

No. 3. JUNE

Naoxr Sucira. Comparative studies on the growth of the cerebral cortex. VII. On
the influence of starvation at an early age upon the development of the cerebral
Carrexe Alioth Oran wONehantsr. eens ital ne Ned. J clan a gekuiele + Aatiere = S40

Naoxi Sucira. Comparative studies on the growth of the cerebral cortex. VIII.
General review of data for the thickness of the cerebral cortex and the size of the
cortical cells in several mammals, together with some postnatal growth changes in
phese structures.“ Lhreeipures and twolcharts.... 60 .cc 00s ques vue Oe he eee

Sypney E. Jonnson. The peripheral terminations of the nervus lateralis in Squalus
SLe kebid Wepe TT OIRO Ses va ere far lees le PES he Sa fh foo oth aos Gaaldoade wt so eo eae ee Fe

Toxvuyasu Kupo. On the development of the nerve endorgans in the ear of Trigono-
cephatusiaponicus:, One plate (ive fizures) 40). 20 2. oie Sa niga cee ih ea eee ole

ill

1}

4}

61

279

1V CONTENTS

No.4. AUGUST

S. W. Ranson. An introduction to a series of studies on the sympathetic nervous sys-

tem: 4One were po Aes ree a eee «+>. Gee. Sale. ne eh pene 305
S.-W. Ranson AND P. R. Brutinestey. The superior cervical ganglion and the cer-
vical portion of the sympathetic trunk. Fifteen figures.........................0. 313

P. R. Brutrnastey anv S. W. Ranson. On the number of nerve cells in the ganglion
cervicale superius and of nerve fibers in the cephalic end of the truncus sympathi-
cus in the cat and on the numerical relations of preganglionic and postganglionic

TE UTOTES eee en sci kets Sie aisles SoU MENSOM baie vprstdcaie. Je oot RD sag RIE ae els eee Ne EA 359
P. R. Bruyincsitey asp 8S. W. Ranson. Branches of the ganglion cervicale superius.
inept 1 5) Ay accent Hera ale pe RI hein She sche Sy aah eg 367
Sypnry E. Jonnson. On the question of commissural neurones in the sympathetic
panmlin, .Wiiteen Heures... 06 2 joes ee 2a an anne: oo Sed ere 385
S. W. Ranson Aanp P. R. Binuinastey. The thoracic truncus sympathicus, rami com-
municantes and splanchnic nerves in the cat. Nine figures.....................-.-. 405
S. W. Ranson anv P. R. Biturncsuey. An experimental analysis of the sympathetic
trunk and greater splanchnic nerve in the cat. Ten figures......................-.. 441

No. 5. OCTOBER

N. E. McInpoo. The olfactory organs of Diptera. Fifty-five figures.................. 457

F. H. Prxe. Remarks on von Monakow’s “‘Die Lokalisation im Grosshirn’’ Sandee nase

C. A. Stewart. Weights of various parts of the brain in normal and pnertad nite
rats at different ages. One figure and three tables..............5..00.00. 00 hoses dee 511

Henry H. Donatpson AND G. NaGcasaka. On the increase in the diameters of nerve-
cell bodies and of the fibers arising from them—during the latter phases of growth
(albino rat). ‘Three charts*and ‘one figure: . 2222/52 08 22705. SO Se ey ee eee 529

F. W. Carpenter. Nerve endings of sensory type in the muscular coat of the stomach
and small intestine. Preliminary note. Four figures.................. 00:00 .+0++00% 553

AUTHOR’S ABSTRACT OF THIS PAPER ISSUED BY
THE BIBLIOGRAPHIC SERVICE DECEMBER 15

COMPARATIVE STUDIES ON THE GROWTH OF THE
CEREBRAL CORTEX

II. ON THE SIZE AND SHAPE OF THE CEREBRUM IN THE NORWAY
RAT (MUS NORVEGICUS) AND A COMPARISON OF THESE WITH
THE CORRESPONDING CHARACTERS IN THE ALBINO RAT

NAOKI SUGITA
The Wistar Institute of Anatomy and Biology

TWO FIGURES AND TWO CHARTS

In connection with an earlier study on the size and shape of
the cerebrum in the albino rat (Sugita, ’17), I took up a study of
the changes in the size and shape of the cerebrum in the Norway
rat during its growth. The method of investigation which was
adopted by me for the albino rat, was followed in this case also,
so that for these methods it is only necessary to refer to the
paper just cited.

Table 1 shows the body and the brain measurements of the
Norway rats which were used. The individuals have been
grouped according to their brain weights and the average meas-
urements for each group are given in the table. To distinguish
these from the like groups for the albino rat, which will often be
referred to for comparison, a capital letter N was attached to
every Norway rat group number. A large part of this material
has been used for further studies on cortical development or for
other purposes. Inasubsequent paper the individual data will
be presented, so that the average values alone are here printed.

The material, consisting of 62 Norway rats (43 males and 19
females) whose brain weights fall between 1.1 grams and 2.4
grams, was collected from time to time in the city and vicinity of
Philadelphia from April to November, 1916.

Figures 1 and 2 show the dorsal and laterai views of the Nor-
way rat brain, on which the positions of the five diameters to be

1

THE JOURNAL OF COMPARATIVE NEUROLOGY, VOL. 29, No. 1,
FEBRUARY. 1918.

2 NAOKI SUGITA

TABLE 1

Giving average values of the physical measurements for a series of Norway rats
arranged according to brain weight groups. Sexes combined

Mer Gar oe Brees °F | sopy weIGcHT | BoDy LENGTH | TAIL LENGTH | BRAIN WEIGHT
grams mm. mm. grams

N XI 9 1) 7 86 47 1.161
N XII 0

N XIII 2 35.5 109 87 1.356
N XIV 2 37.0 113 90 1.436
N XV 5 52.6 126 104 1.536
N XVI 8 65.8 136 118 1.644
N XVII 8 93.8 157 129 1.743
N XVIII + 131.9 166 148 1.836
N XIX 3 193.1 187 164 1.965
N XX 5 250.9 212 179 2.033
N XXI 4 296.1 223 189 2.164
N XXII 1 336.8 223 182 2.266
N XXIII 1 394.0 256 202 2.345

measured are designated. The dimensions of the figures are in
accordance with the data given in table 2 and the figures are
comparable with figures 1 and 2 given in the study on the albino
rat brain (Sugita, 717).

Table 2 shows the average values of the five diameters of the
Norway cerebrum, measured at the same locations as in the case

Fig. 1. Dorsal view of the Norway rat brain weighing 1.64 grams—enlarged
1.8 diameters. To show the positions at which the two measurements for the
width and the two measurements for the length were taken.

Fig. 2. Lateral view of the Norway rat brain weighing 1.64 grams—enlarged
1.8 diameters. To show the position at which the height was measured.

GROWTH OF CEREBRAL CORTEX 3

TABLE 2
Giving the brain weight for each brain weight group, the cube root of the brain weight
and the linear measurements for width, length and height of the cerebrum. Nor-
way rat. W. B = Width AB; W. D = Width CD, L. G = Length EG, L. F=
- Length EF (see figure 1). Ht. = Height HK (see figure 2)

BRAIN CUBE ROOT

WEIGHT Sarees ee, pea W.B W.D AG: Bs 0 Ht.

CAROWIE WEIGHT

grams mm. mm. mm. mm. mm.

N XI 9 1.161 1.051 13.86 12.69 12.63 L218 8.83
N XII 0
N XIII 2 1.356 IP LO7 14.20 12.98 13.60 13.05 9.45
N XIV 2 1.4386 1.128 14.45 11336741 1) 7A 13.24 9.31
N XV 5 1.536 1.154 14.7 seo 14.18 13.48 9.28
N XVI 8 1.644 1.180 14.91 13.65 14.24 13.62 9.61
N XVII 8 1.743 1.204 15.10 13.92 14.54 13.88 9.97
N XVIII 4 1.836 1225 15.17 14.20 15.00 14.32 9.98
N XIX 3. 1.965 22 15.68 14.28 15223 14.68 10.08
N XX 5 2.033 1267 oO 14.34 1 5e52 14.74 10.02
N XXI 4 2.164 1.293 16.25.) 14.94 15.92 155112 10.18
N XXII 1 2.266 1.314 16.60 14.90 16.15 15.70 10.35
N XXIII 1 2.345 1.329 16.55 15.65 16.30 15.50 10.25

of the albino rat and denoted by the same abbreviations (figs.
1 and 2). The data are arranged in groups according to the
increasing values of the brain weight at intervals of 0.1 gram.

Chart 1 gives a graphic view of the average measurements of
the Norway cerebrum in each brain weight group, plotted on the
basis of the data in table 2.

A study of the individual records used for table 2 shows that
within any group the individual variability does not amount to
more than +1.2 per cent, as compared with the average values
for the group and each diameter shows a relatively steady in-
crease, generally in close relation with brain weight.

On examining Chart 1, the curves for W. B and W. D are
found to run almost parallel and the same is true for the curves
L. Gand L. F, as seen already in the case of the Albino cerebrum.
By a comparison of the graphs for the width with the graphs for
the length, it is evident that the rapidity of growth along the
sagittal diameter is greater than that along the frontal diameter,
a relation that was also seen in the Albino cerebrum. AH. in-
creases slowly as compared with the other diameters.

4 NAOKI SUGITA

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“05 COM LOTS 08009) ONT Se eS Re IT BIS IS arco th N22 2s ges

Chart 1 Giving the average values of the five diameters of the Norway rat
cerebrum for each brain weight group.

—- WB. oo LF
pase W.D. x—-—x Ht.
— ],G.

The approximate value of each diameter can be caleulated by
the following formulas:

W. B (mm.) = Cy X V Brain weight (grams) (1)
where Cy will be 12.8 for a brain weighing 1.3-1.6 grams.
12.5 for a brain weighing 1.6-2.4 grams.

W. D (mm.) = W. B mm.) — 1.25 mm. (2)

L.G(mm.) = C, X ¥ Brain weight (grams) (3)
where C, will be 12.2 for any brain weighing 1.3-2.4 grams. ,

ji PCat) Si C2(Gime ye 0 (4)

Ht. (mm.) = Cy X ¥ Brain weight (grams) (5)

where Cy will be 8.5 for a brain weighing 1.1-1.4 grams.
8.2 for a brain weighing 1.4-1.9 grams.
7.9 for a brain weighing 1.9-2.4 grams.

At the first entry in this study, Group N XI (table 2), the
relative volume of the cerebrum (W. B xX L. GX Ht.) is

13.86 x 12.63 x 8.83 = 1546.92 (see also table 3 A)

GROWTH OF CEREBRAL CORTEX 5

corresponding to a brain weighing 1.161 grams (body weight
19.7 grams, body length 86 mm., tail length 47 mm. and age
estimated at about 10 days), while the relative volume of a
cerebrum in the last entry, Group N XXIII (table 2), is

16.55 < 16,30 x 10.25 = 2765.09 (see also table 3 A)
corresponding to a brain weighing 2.345 grams (body weight 394

TABLE 3

Giving the relative cerebral volumes, obtained by the formula: W.B X L.G X Ht.,
for each brain weight group of the Norway (A) and of the Albino (B). The albino
rat brain weight corresponding to the given Norway brain of the same age, obtained
by reducing the Norway brain weight by 18 per cent, is also given in (A)

(A) NORWAY RAT | (B) ALBINO RAT
235, EES
. = 5 ol Si ‘3 5
28 ee Observed 3 g2 zo
Brain weight paleulsted 2kSos | Brain weight brain weight eee ae
weigh Soe 4 ache : Soeal a
w SIP paola ®welshe| the Albino | 33238 | # UP | Albino rat | ES ES
N XXIII r'"| brain of the] + 3X3 Sak PS
D same age Bo m2 IX—xx ee
Norway rat = ore
sone based on table 3
oa8 (Sugita, 717)
jan]
grams grams grams
N XI 1.161 0.952 1547 9) LX 0.954 1335
N XIII 1.356 ee, S259 illite 1.047 1356
N XIV 1.436 A ALPE 1844 | XI 1.156 1522
N XV 1.536 1.259 1944 } XII 12253 1606
N XVI 1.644 1.348 2040 || XIII 1.334 1663
N XVII 1.743 1.429 2189 — | XIV 1.449 1788
N XVIII 1.836 1.505 DOTA. | kV 1.558 1956
N XIX 1.965 TOU, 2407 Ie NeVGE 1.662 2014
N XX 2.033 1.667 2442 FDA Ie W330 PMY
N XxI 2.164 1.774 2634 i XeValiah 1.832 2228
N XXII 2.266 1.858 PHT A ee; 2) D8 1.924 2285
N XXIII 2.345 1.923 2765 KX 2.037 | 2568

grams, body length 256 mim. and tail length 202 mm.). <Ac-
cording to these determinations, the volume increases by 79 per
cent while the weight increases by 102 per cent, showing roughly
that the specific gravity of a brain in the fully mature Norway
rat is higher than that of younger one.

By an estimate based on the data given by Donaldson and
Hatai (11), it would appear that, if the Albino and the Norway

6 NAOKI SUGITA

brains of the same age be compared, the Norway brain weight
is 20 to 25 per cent higher than the albino brain weight, when
the albino brain weight is taken as the standard. For the pur-
pose of comparison in their developmental stages, I have as-
sumed that the Norway brain would correspond to an Albino
brain whose weight is 18 per cent less than the Norway brain
weight of like age. Here the Norway brain weight is taken as
the standard. The evidence for this conclusion will be given in
detail in a later paper which discusses the thickness of the cortex
in the brain of the Norway rat.

A comparison of the Norway brain with that of the Albino
may be made in two ways; by a comparison of brains of like
weight or by a comparison of brains of like ages. In Chart 2,
the diameters of the cerebrum in the Norway rat are compared
with those in the albino rat. In part A of this chart, the data for
the Norway and the albino rats were entered according to the
observed brain weights, and in part B of the same chart, the
same linear measurements for the Norway as used in part A are
entered above brain weights which are 18 per cent below the
observed Norway brain weights and which in turn represents the
weights for the albino brains of like age with those of the Norway
rat. The corresponding brain weights of the Norway and of the
albino rats at the same age are given in table 3 A. It is assumed
that the albino brain weight is 82 per cent of that for the Norway.

If, as shown in part A of Chart 2, the comparison is made
between the brains of the two rats using similar brain weight
groups, W. B in the Norway cerebrum surpasses W. B in the
Albino on the average by 0.4mm. L.G is quite equal in both
the rats for brains weighing 1.1 to 1.6 gms, after which stage it
is clearly greater for the Albino. Hf. is on the average slightly
in favor of the Norway.

If, on the other hand, as shown in | part B of the chart, a Nor-
way cerebrum be compared with an Albino cerebrum of the
same age (over 10 days), the Norway cerebrum has a greater
W. B than the Albino, by about 1.00 mm., and also a greater
L.G. The excess of L. G in the early age is on the average 0.7
mm., but this difference decreases as the age advances, owing to
the more rapid growth of the albino cerebrum in this dimension.

GROWTH OF CEREBRAL CORTEX 7

Ht. in the Norway cerebrum is greater on the average than that
of the Albino of the same age by ca. 0.6mm. As was to be ex-
pected the excess in the dimensions of the Norway brain are
greater in part B, Chart 2, where the brains are compared ac-
cording to age, because at like ages the Norway brain is heavier.

The chief point of interest brought out by this comparison is
the similarity in the direction of the corresponding curves for the
two forms and the fact that the age at which L. G crosses W. B
in the Albino is approximately the age at which these diameters
come nearest to crossing in the Norway.

Table 3 A gives the relative volumes of the cerebrum in each
brain weight group of the Norway rat, obtained by the formula:

nn B

; 418 =

| |
—4 ed a —— | —l.

alee. | | |

|

|
5 }-—_+—_+—__+__+
|

| T
| |
j++}. 1 _} + 5 = 4 + = = ———
| | |
| |
| |
|

|
—

4 : | us| 12 = | | | a a es _! x |
“il 12 15 14 15 16 17 18 19 20 21 22 23 m= 09 10 If 12 13 44 45 ie iT #8 19 gr

Chart 2 Giving a comparison of the cerebral measurements (W.B, L. G and
Ht.) of the Norway and the albino rats. Part A was plotted according to the ob-.
served weight of the brain for each brain weight group of the Norway rat. Part
B was plotted according to the corresponding weight of the brain in the Albino
of the same age, the Albino brain weights being obtained by reducing the observed
weight of the Norway brain by 18 per cent. The measurements for the Norway
cerebrum were based on table 2 of this paper and the measurements for the Al-
bino cerebrum were based on table 3 of the first paper of this series (Sugita 717).

—-* o— WB(Norway) —— W.B(Albino)
e----- @ O----0 EEG “) see ss L.d( “ )

8 NAOKI SUGITA

W.B x L.G X Ht., based on the measurements given in table
2. Table 3B gives the similar calculations for the Albino cere-
brum based on the measurements given in table 3 of the first
paper in this series (Sugita, 717).

Table 4 gives for both the rats the cerebral volumes (A) ac-
cording to brain weight, and (B) according to age. In table 4 A,

TABLE 4
Giving the ratios of the cerebral volumes of the Norway to the Albino rats (A) pairing
the brains of the same weight and (B) pairing the brains of thesameage. Calcu-
lated on the basis of the data given in table 3

(a) (B)

Pairs of groups in w hich acom- | Ratio of cerebral || Pairs of groups in which a com-| Ratio of cerebral
parison of cerebral volume was | volume between| parison of cerebral volume was | yolume between
made. Like brain weights two groups of the) made. Like ages two groups of

like weight. the like age.
Norway Albino Albino = 1.000 Norway Albino Albino = 1.000

N XI xa 1.016 N XI IX 1.159

N XIII XIII 1.097 N XIII X! 1.271!

N XIV XIV 1.031 | N XIV XI e212

N XV XV 0.994 li Ni XV) exalall _1.210

N XVI XVI 1 O13 ee yy Nel Ui 1227

N XVII XVII IONS | N XVII XIV 1.224

N XVIII XVIII 1.019 N XVIII XV 1.161
N XIX XIX 1.053 N XIX

N XX xX 0.951 N XX XVI 1.212

N XxXI XVII 122i

N XXII XVIII 1.248

le IN) Sexe sT | Sxaox: 1.210

IAVET AGC. ska cee ae 1.021 ly) Avena erence eo i 1.214

1 As the reduced brain weight of Group N XIII falls between the brain weights
of Groups X and XI, the mean value @ the cerebral volumes of Groups X and XI
was used in comparison.

the brains of like brain weight groups are compared, by pairing
the groups which carry the same number. By this comparison,
it is seen that, on the average, the values for the Norway rat
are somewhat greater, except in Group XV and in the old age
group, Group XX, in which the reverse is true This shows that
the Norway brain has, as a rule, a less specific gravity than the
brain of the albino which has the same weight. One important

GROWTH OF CEREBRAL CORTEX 9g

factor in producing this relation is that the Norway brain is
younger and less advanced in myelination than the albino brain
of the same weight.

In table 4 B the cerebral volume of a Norway rat is compared
with the cerebral volume of an Albino of presumptively the same
age. Each Norway brain weight group is paired with an albino
group which has the average brain weight nearest to the corre-
sponding albino brain weight of the same age with the Norway
group. The data were all taken from table 3. Compared in
this way, the Norway cerebrum has a volume about 21 per cent
above that of the albino cerebrum of the same age, as shown in
table 4 B.

The width-length index of the Norway cerebrum, which is ob-
WwW. Dex 100
iB
Group N XI, and decreases as the brain weight advances, drop-
ping to 97 or less in the last and oldest groups. Compared with
the like group of the Albino, the width-length index of the Norway
cerebrum is on the average always higher by 2 or more points
than that of the albino cerebrum. So, it may be concluded that
the Norway cerebrum is becoming somewhat elongated as the
age advances, but not to so marked a degree as does the albino
cerebrum and that it is always somewhat more rounded in shape
as compared with the albino cerebrum of the same weight or
age. The method of measurement here used reveals only in
part the degree of difference in the shape of the two brains, for
direct inspection shows the surface of the Norway cerebrum to
be distinctly more rounded than that of the Albino, especially at

the frontal poles.

tained according to formula , is 104 in the youngest

LITERATURE CITED

Downaupson, H. H., anp Harar, 8. 1911 A comparison of the Norway rat with
the albino rat in respect to body length, brain weight, spinal cord
weight and the percentage of water in both the brain and the spinal
cord. Jour. Comp. Neur., vol. 21, pp. 417-458.

Suaira, Naoxt 1917 Comparative studies on the growth of the cerebral cortex.
I. On the changes in the size and shape of the cerebrum during the
growth of the brain. Albinorat. Jour. Comp. Neur., vol. 28, pp. 495-
510

as ene i

AUTHOR’S ABSTRACT OF THIS PAPER ISSUED BY
THE BIBLIOGRAPHIC SERVICE DECEMBER, 15,

COMPARATIVE STUDIES ON THE GROWTH OF THE
CEREBRAL CORTEX

IV. ON THE THICKNESS OF THE CEREBRAL CORTEX OF THE NOR-
WAY RAT (MUS NORVEGICUS) AND A COMPARISON OF THE SAME
WITH THE CORTICAL THICKNESS IN THE ALBINO RAT

NAOKI SUGITA

From the Wistar Institute of Anatomy and Biology

TEN CHARTS

I. INTRODUCTION

In my second study in this series (Sugita, 717a), I described
in detail the postnatal growth of the cortex in thickness in the
brain of the albino rat. With the same purpose and by the
same technique, I have examined also the growth of the cere-
bral cortex of the Norway rat, the wild form from which the
albino rat has been derived. Donaldson and Hatai (11) have
been interested in a comparison of the wild Norway with the
albino rats in respect of their body measurements and the size
of the central nervous system. They have concluded that on
account of domestication the albino rat grows less well than
the wild Norway rat, from which it has been derived, and es-
pecially that the relative weight of the brain of the adult albino
rat is about 16 per cent less than that of the Norway rat of like
body weight. It has been assumed as probable that the greater
weight of the brain in the Norway rat is due to an enlargement
of the constituent neurons rather than to an increase in their
number. The percentage of water appears to be nearly the
same in the central nervous system of both forms during the
period of active growth, but after this period it remains slightly
higher in the Norway rat. From these differences between
the two forms as regards the weight and the water content of
their brains, it is also inferred that there will be some structural

1

12 NAOKI SUGITA

differences in the cerebral cortex. Consequently, it became
desirable for me to compare in these two forms, one wild and
aggressive and .the other gentle and domesticated, the course
of the growth of the cerebral cortex.

Using my previous studies on the Albino (Sugita, ’17a) and
on the form of the Norway brain (Sugita, 718) as a paint of de-_
parture, I will present in this paper the data on the cortical thick-
ness of the Norway rat and will compare these with the data
for the Albino. In this comparison of the brains of the two
forms, the data, other than those on cortical thickness, are all
quoted from Donaldson and Hatai (’11, 715).

Il. MATERIAL

The Norway rats used in this study, were all supplied through
the courtesy of The Wistar Institute and were trapped alive in
Philadelphia and its vicinity, between April and November,
1916. There were 36 males and 18 females, representing every
stage of growth between 17 and 394 grams in body weight.
In the preparation of the material and the arrangement of the
data, the same methods as those described in my former study
on the Albino (Sugita, ’17a) were followed. For the discrimi-
nation of a Norway group from an albino group of the same
tabular number, the Norway records carry the capital letter N
before their group number.

The following tables, tables 1 and 2, give the sex, body and
tail lengths, and body and brain weights of the Norway rats
used in this study, grouped according to their brain weights and
averaged for each group. Table 1 contains the material used
for the sagittal and frontal sections and table 2 that for the
horizontal sections.

Comparing the body measurements of this series with those
given in table 85 in “The Rat’? (Donaldson, ’15), it is found
that the average values for my material by groups correspond
fairly well with the table values.

The increase in the body measurements of the Norway rat
according to age is imperfectly known, so that we can not in-
fer the age from the body measurements with any exactness.

GROWTH OF THE CEREBRAL CORTEX r3

TABLE 1

Showing the sex, body weight and length, tail length and brain weight of the Norway
rats used in this study (sagittal and frontal sections) accompanied by the averages
for each brain weight group

eo

NO. na SEX BODY WEIGHT BODY LENGTH TAIL LENGTH BRAIN WEIGHT
grams mm, mm, grams
NeXT b | Gd) | m 19.8 84 41 1.155
a | (1) | m 20.8 86 44 1.160
i (2) | m LAS 85 65 1.175
19.5 85 50 1.164
N XII
NXIIIa | ()| m 35.3 110 66 1.369
35.3 110 86 1.369
NeXEV |G). | m 33.1 104 84 1.407
g | @) | m 37.5 112 88 1.429
(4) aa 33.8 113 94 1.431
i (3) | m 36.3 107 86 1.431
e | (5)| m 43.6 124 108 1.437
els) ln 36.1 112 87 1.445
36.7 112 91 1.430
NXVe m 42.6 122 102 1.517
e m 66.7 135 114 1.557
54.7 129 108 1.537
N XVI a m 74.8 137 1.619
g m 54.8 130 107 1.632
e m 56.3 128 105 1.636
62.0 132 106 1.629
N XVII e f 81.0 152 120 1.710
g m 57.0 137 113 1,721
a f 118.5 172 136 1.738
¢ f 104.0 164 132 1.788
90.1 156 125 1.739
N XVIII ¢ f 136.9 157 147 1.825
a m 128.1 177 142 1.833
132.5 167 145 1.829
N XIX b m 160.7 177 158 1.962
a f 251.0 210 174 1.981
205.9 194 166 1.972

14

NAOKI

SUGITA

TABLE I—Continued

NO. | eer | SEX BODY WEIGHT | BODY LENGTH | TAIL LENGTH | BRAIN WEIGHT
7 | Brains mm. mm. grams
NAc f 254.0 215 180 2.015
a (1) f 253.1 213 2.089
253 .6 214 180 2.052
N XXI g m 331.0 215 195 2.156
d m 231.8 215 174 2.187
281.4 216 _ 185 2.172
N XXII
N XXIII a m 394.0 256 202 2.345
394.0 256 202 2.345
TABLE 2

Showing the sex, body weight and length, tail length and brain weight of the Norway
rats used in this study (horizontal sections) accompanied by the averages for each
brain weight group

NO.

N XII

NXE b

IN=XVb
d

|

eee ae SEX | BODY WEIGHT | BODY LENGTH

grams mm.
(1) m 20.0 85
(2) | m 17.0 83
(0) am 20.7 87
19.2 85
(3) m B30). 71 108
85.7 108
(4) m 31.7 103
(3) m 36.7 111
(3) | m 38.4 115
(Gy ht 43.8 126
(4) | m 34.7 108
Be Al 113

m 48.5

m 54.1

51.3

TAIL LENGTH

BRAIN WEIGHT

mm.
42
64
41
49

101
101

grams

1.133
1.160
1.199
1.164

1.348
1.343

407
.428
443
475
481
447

er oy

1.511
1.529
1 520

NO.

N XVI f

N XVII f
b
d
h

N XVIII b
d

N XIX ¢

N XX e
b

N XXI f
j

N XXII

N XXIII a

GROWTH OF THE CEREBRAL CORTEX

TABLE 2—Continued

LITTER
NO.

BODY WEIGHT

BODY LENGTH

TAIL LENGTH

Rh eh

(4) f

Lon)

grams
56.7
73.9
66.7
98.3
73.9

71.8
95.4
125.0
97.7
I .8

128.5
134.0
131.3

167 °6
167.6

394.0
394.0

mm.
129
148
138
156
143

140
155
180
152
157

256

mm,
109
132
112
141
124

112
130
150
139
133

153
148
151

160
160

188
178
183
190

195
193

202
202

BRAIN WEIGHT

grams

1.613
1.666
1.674
1.699
1.663

Leal
als
1.773
ere)
LeWAr

1.815
1.870
1.843

—

953
1.953

008
028
018

%® bo bo

150
.162
156

® bo bo

2.345
2.345

But, according to the authors cited above, the marked difference
between the two forms in body size does not appear during the
period of rapid growth, but later, so that at maturity the Nor-
way rat has a body weight 25 to 40 per cent above that of the
For the same age however, the percent-
ages of water in the central nervous system is just a trifle higher
in the case of the Norway. Relative to the body weight, the
Norway rat at maturity has a heavier brain than the albino rat,
the difference being about 16 per cent in favor of the Norway.

Albino rat of like age.

16 NAOKI SUGITA

On the basis of these rough data, the approximate age of the
individuals in tables 1 and 2 can be inferred.

To my regret, I did not obtain material under 17 grams in
body weight. I could, therefore, not make a complete study of
the postnatal growth of the cerebral cortex of the Norway rat
from birth on and must in consequence be content to present in
this paper the data beginning with material probably from 10 to
12 days old. It may, however, be noted here, that, among the
rats trapped, the following were evidently members of the same
litter and still following the mother.

(1) NXIa, NXIb, N XIc, N XId, with their mother
N XX a, and three other young which were used for another
purpose.

(2) N XIi, N XI h, and four others.

(3) ON XIN a. AN’ XI oy? IN) GI aN) OGY She N XIV a
N XIV j, N XIV k.

(4) N XIVe, N XIV f, and two others.

(5) N X1IVa, N XIVb, N XIVc, N XIVd and two others,
with their mother N XX b.

This suggests that the Norway rats whose brain weighs less
than 1.5 grams or whose body weighs less than about 40 grams
are not yet independent of their mothers.

III. TECHNIQUE

For the technique of fixation and imbedding and the making
and staining of the sections, the same procedures which have
been already described (Sugita, ’17 a) were followed. ‘Thirteen
different localities were measured on sections in three planes cor-
responding to those used in the former study of the Albino cor-
tex (cf. figs. 2, 4 and 6 in the paper cited).

As to the cortical cell-lamination of the Norway rat, two sets
of figures with explanations were given in the former paper (Su-
gita, 717 a) reproduced from Lewis (1881) and Fortuyn (14) and
to those I would like to call attention on this occasion. There
does not appear to be any important difference between the
Norway and the albino rats in the cell-lamination of the cerebral
cortex.

GROWTH OF THE CEREBRAL CORTEX ny.

IV. OBSERVED DATA GIVEN IN TABLE AND CHART

As in the ease of the albino rat, the measurement of the corti-
cal thickness of the Norway brain was made at the localities
I-XIII by the direct measurement of the sections as prepared
and was then recorded without correction. The results thus ob-
tained are condensed in table 3.

Table 3 shows for each brain weight group the average
thickness of the cerebral cortex of the Norway rat as directly
observed in each of the three sections and the general average
obtained by averaging the thicknesses of the sagittal, frontal and
horizontal sections. The average brain weight corresponding to
the average thickness of the cortex is obtained by doubling the
weight of the brain, from which the sagittal and frontal sections
were taken, adding the weight of the brain from which the hori-
zontal sections were taken, and dividing the sum by three.

Chart 1 is based on table 3 and shows the increase in the gen-
eral average thickness of the cerebral cortex of the Norway rat,

TABLE 3

Showing the general average thickness of the cerebral cortex of the Norway rat ac-
cording to brain weight groups, also the average thickness in the sagittal, frontal
and horizontal sections. Observations on slide, without correction

ates SAGITTAL SECTION ania. HORIZONTAL SECTION Renee
WEIGHT
GrOuE Number| Brain Thick- | Thick- | Number} Brain Thick- Brain Thick-
of cases | weight ness ness of cases | weight ness weight ness
grams mm. mm. grams mm. grams mm.
N XI 3 1.164 | 1.34 1.48 3 1.164 1.44 | 1.164 1.40
N XII 0 0
N XIII 1 1.369 1.35 1.50 1 1.343 1.50 | 1.360 1.45
N XIV 6 1.4380 1.43 1.48 5 1.447 1.54 | 1.486 1.48
N XV 2 1.537 1.40 1.50 2 1-520 1.58 | 1 o32 1.49
N XVI 8} 1.629 1.41 1.54 4- | 1.663 1.63 | 1.640 1.538
N XVII 4 1.739 1.51 1.56 4 1.747 1.59 | 1.742 1.55
N XVIII 2 1.829 1.51 1.64 2 1.843 1.63 | 1.834 1.59
N XIX 2 1.972 1256 1.58 1 1.953 1.68 | 1.965 1.61
N XX 2 2.052 1.49 1.48 2 2.018 1.58 | 2.041 1.52
N XXI 2 242 1.53 1 533 2 2.156 75) | 2E1166 1.60
N XXII 0 0
N XXIII 1 2.345 1.60 1 2.345 Ste) || Bees USE

THE JOURNAL OF COMPARATIVE NEUROLOGY, VOL. 29, No. 1

18 NAOKI SUGITA

as directly observed, and without correction and also the average
values for the sagittal, frontal and horizontal sections, according
to the increase of the brain weight.

V. CORRECTED DATA PRESENTED IN TABLES AND CHARTS

Using the detailed observed values which were all carefully
tabulated, although they have not been published, a series of

mm.

24; ———-

il |

= al
|
|

dle hel
|_| i |
| eee

|
|
19 20 21 22 23 gs

ore

|
|
|
|
|

|
fo i 12 43 14 15 16 IT 18

Chart 1 Giving the average thickness of the cortex on slide (not corrected)’

’ . in the sagittal, frontal and horizontal sections and the general average thickness

on brain weight group in the Norway rat. Based on table 3. -—--—S Average
thickness of the cortex in sagittal section. Measuredon slide. —-——-F Average
thickness of the cortex in frontal section. Measured onslide. - - - - - H Average
thickness of the cortex in horizontal section. Measured onslide. *———*A Gen-

eral average thickness of the cortex of three kinds of sections. Measured on slide.

correction-coefficients, obtained in exactly the same manner as
for the albino rat, were found and applied to the observations
on the Norway cortex. The corrected values are those entered
in tables 4,5 and 6. The tables also contain in each case the
measurements from which the correction-coefficient was obtained
and for each brain weight group the average value of the cor-
rection-coefficient for that group.

Table 7 shows the corrected values for the average thickness of
the cortex, obtained in the same way as were the uncorrected

GROWTH OF THE CEREBRAL CORTEX 19

TABLE 4

Showing the corrected values of the cortical thickness in the sagittal section for each
individual and for each brain weight group. ‘The data for the correction-coefficients
are indicated separately for each brain and the coefficient is given with the average
for each group

CORRECTION- THICKNESS OF THE CORTEX
COEFFICIENT (SAGITTAL SECTION)
BRAIN WEIGHT | BRAIN

GROUP weIGcHT | Diam. Dinu!

oigen | LF | Loc. | Loe. If | Loe. HI} Loe. IV | Loe. V sea
ben on slide =
grams mm. mm. mm. mm. mm. mm. mm, mm.
ING XCM on eel Som ale om aL Oe40 2.18 1033 1.44 TLsPAL |) aL OSS |), Dheey
a | 1.160 | 12.10 | 10.15 2.40 1.83 1.63 1.32 | 1.07 | 1.65
rl} a alicday: |) 4 ays 9.80 2.61 1.83 AGH 1.26 | 1.04 | 1.67
1.164 1.20 2.40 1.80 1.56 26a Oo leo
N XII

N XIII a | 1.369 | 12.95 | 10.10 2.47 1.87 1 42 IES 3a anole
1.369 1.28 2.47 1.87 Towle: Heetoy WIL |i Ces
N XIV b | 1.407 | 13.45 | 10.50 2.76 | 2.04 1.73 1.59 | 1.36 | 1.90
g | 1.429 | 13.05 | 10.10 2.56 1.82 1.72 UL 40) | ey] a 8
a | 1.481 | 18.15 | 10.40 2.64} 2.01 1.82 12567 dan ele si
leon eiseOoy | O25 mle Zo6 1.90 ileal (PASS ie Seal elen®
e | 1.487 | 12.80 | 10.05 2.47 1.87 1.73 Tt) | Pee Ih alee
k | 1.445 | 13.35 | 10.30 | 2.88 | 2.03 1.78 1.64 | 1.38 | 1.93
1.430 1.28 2.64 1.95 1.76 i a | GSS || cer

—_
oo
1o<)
_
i)
oO
—_
~I
for)

Neve) 1.517 112. 70° |, 10.10 Ww t2256)) 2.92) 1.72
eel.557| 13275) | 1025.0 92.83 | +1293.) 1.

~I
bo
rs
No)
=
is
—_
(0)
co

| 1.537 1.30 DION tOG:| 127B.)|) TAs Pel sBeia 1282

N XVivail! #619" |) 13,50) | 10.25 | 2.68 | 2:04) 1:77 | 1.46) 134) 1.86
g | 1.632 | 13.45 | 10.00] 2.86 | 2.17} 1.84] 1.53 | 1.21 | 1.92
enimleaGsar ple opalel0. 10 aeeze et 98 | 177) L490 SE |p 2286

1.629 1.83 DEG NCO VL tetO NW 1 AO Ne gon | Sa

N XVIle .710 | 13.70 | 10.50 | 2.84 | 2.09 95 .55 | 1.42 no7
g | 1.721 | 13.40 | 10.35 | 2.78 | 2.138 .98 63 .38 | 1.98

.788 | 14.20 | 11.20 | 2.93} 2.15

1 1 1 1 1

1 i 1 i! 1

a lh e738eelS.608) 10:70. \eaee2 | 2:00 | 1276, L.405so2t ts

1 1 1 1 2
1.739 1.29 Moe. | Od | od 1 1 i

N XVIII ¢ |} 1.825 | 14.80 '| 10.85 | 2.91 | 2.07] 1.88} 1.49 | 1.28 | 1.93
aie te Sagas 20) lt 5O:| 62589) |) 22061) 1.690 Peale) i 48) | E93
1.829 1.27 QNOG | 2:07 | 1.79 | PROO L.38 | 15235

20 NAOKI SUGITA

TABLE 4—Continued

CORRECTION- THICKNESS OF THE CORTEX
COEFFICIENT (SAGITTAL SECTION)
BRAIN WEIGHT | BRAIN
GROUP WEIGHT | Diam. Di
Dak 1am. Aver-
oni ireshile ee: Loc. I | Loc. II |fLoc. III | Loc. IV | Loc. V
brain on slide a
grams mm. mm. mm. mm, mm. mm. mm, mm,
N XIX b | 1.962 | 14.70 | 11.50 2.98 2.12 1.97 1.54 | 1.46 | 2.01
a | 1.981 | 14.40 | 11.50 2.83 2.08 7s 1.54 | 1.44 | 1.93

1.972 1.26 2.91 2.10 1.86 igh |) IAS |) Oi
N XX c | 2.015 | 14.55 | 11.50 | 2.86 | 2.00 | 1.81 | 1.55 | 1.43 | 1.93
a | 2.089 | 14.95 | 12.00! 2.75] 1.93] 1.671 1.341 1.30 | 1.80
2.052 1.25: 2.81 1 97 A ELON dL Kova els ia
N XXI g | 2.156 | 15.15 | 11.90 | 3.01 | 2.15 | 1.82) 1.58] 1.40") 199
d| 2.187 | 15.30 | 11.50 | 2.94] 2.09] 1.85! 1.60 | 1.41 | 1.98
mie, 1230 2.98 CPA 1.84 ANS) || lel |) 2

N XXII ]
N XXII a | 2.345 | 14.50 | 12.50 | 2.74| 2.07 | 1.75| 1.38 | 1.93 | 1.86
2.3845 LUG: 2.74 2.07 US ih isxey || Il SoS) || JL SIH

values shown in table 3. This table (table 7) serves as a stand-
ard for discussing the actual thickness of the fresh cortex of the
Norway rat. The average thickness in the adult Norway rat is
2.06 mm., as obtained by averaging the thicknesses of the cortex
in Groups N XV—-N XXIII, in which stages the cortex may be
considered to have reached its full thickness.

Charts 2 to 7 show graphically the data given in tables 4 to 6
respectively, and chart 8, which is based on table 7 giving the
average values, presents a general picture of the growth changes
in the cortex according to brain weight.

Charts 2, 4 and 6 show the individual determinations for the
thickness of the cortex in the sagittal, frontal and horizontal sec-
tions, respectively, plotted according to the brain weight.
Chart 2 gives the individual records for locality I and locality V
with the average for all localities from I to V in the sagittal
sections. In a like manner, chart 4 gives the values for localities
VJT and VIII with the DSS of localities VI to VIII for the

GROWTH OF THE CEREBRAL CORTEX Baal

TABLE 5

Showing the corrected values of the cortical thickness in the frontal section for each
individual and for each brain weight group. The data for the correction-coeffi-
cients are indicated separately for each brain and the coefficient is given with the
average for each group

commrtemt SUE a are
BRAIN WEIGHT BRAIN
GROUP WEIGHT Di .W.D c
ont Diam-W;?| Loc. VI | Loc. VII | Loc. VIII | Average
Hig A |v ga her My | op es | rm | Wi erage gcc
N XI b 1.155 13.00 9.90 2.05 lel 1.68 1.95
a 1.160 12.70 10.00 1.94 1.92 1.62 ses
i 7s 12.50 9.20 1.96 1.99 1.62 1.86
1.164 Meow 1.98 2.01 1.64 1.88
N XII
N XIII a 1.369 13.00 10.00 PAVE 7} PAI 1.59 1.96
1.369 1.30 2.07 eo 1.59 1.96
N XIV b 1.407 13.05 9.90 Dh PAL, Qes Lez 2.04
g 1.429 13.20 9.50 2.18 2.29 il e7/l 2.06
a 1.431 12.85 10.70 2.04 2.00 83 1.92
1 1.431 13.40 10.30 1.90 2.06 Row 1.84
e 1.437 Be25 9.80 1.89 DF Als} 1.56 1.86
k 1.445 seo 0 9.90 pal, Deals 1.65 1.97
1.480 HX? BO” SDs iS} 1.66 1.96
N XVe 1 Sul? 13.20 10.00 1.98 PPAl 1.62 1.94
e eS od 13.50 9.60 2.28 2.39 1.76 2.14
~ HY 1786 Oo1d: 2.30 1.69 2.04
N XVi a 1.619 13.80 10.80 2.01 7} 1s Lag 1.95
CRlAGS2 13.70 9.90 2.24 Ph SIN 1.83 PHA
e 1.636 13.80 10.00 2.14 2.36 il 7%) 2.08
1.629 1.30) Calo: 2200! ety 2.08
N XVIile alo) 13.80 10.00 Ph NS ell 1.68 2.05
g Leal 13.60 10.40 2.20 2.30 1h) 2.10
a 1.738 14.10 10.60 2.01 Pe 1.66 1.95
c 1.788 13.95 10.60 DP} Bt) 2.40 1.82 2.19
1.739 OO 218 2201 HVS 2207,
N XVIII e 1.825 14.45 10.70 2.20 DBAs; 1.73 2.09
a 1.833 13.95 11.70 2.18 D) pay? 1.80 2.07
1.829 a Do!) 2.29 Hey 2.08

22 NAOKI SUGITA

TABLE 5—Concluded

THICKNESS OF THE CORTEX

COEFFICIENT
c (FRONTAL SECTION)

BRAIN WEIGHT BRAIN
J WEIG : ;
GROUP EIGHT | Diam.W.D eee
on | Gavelida Loc Wii Loc. VII | Loc. VIII | Average
fresh brain
grams mm. mm. mm. mm. mm. mm.

N XIX b} 1.962 14.60 11.60 2.08 2.28 1.68 2.01
Bele 981 13.95 10.80 2.04 2.21 AZ, 1.99

1.972 1.26 2.06 2.95 1.70 | 2.00
NXXe]/ 2.015 14.30 10.50 2.14 2.32 173 2.06
a| 2.089 14.50 11.20 1.80 2.08 1.66 1.85
2.052 WSS 129% 2.20 1.70 1.96
NXXIg| 2.156 14.75 11.10 2.03 2 94 1.69 1.99
ail) 2187 15.05 10.80 2.19 2.54 1377) Ae oatz
2.172 1.36 2.11 2.39 1.73 | 2.08
N XXII
N XXIII

frontal sections. Chart 6 does the same for localities IX and XIII
with the average of localities [X to XIII in the horizontal sec-
tions. Charts 3, 5 and 7 show the average values of the cortical
thickness in the sagittal, frontal and horizontal sections, for each
brain weight group. Further, on each chart is shown the change
in thickness at each one of the localities measured in that
section.

Chart 8 is based on table 7 and shows the general average (cor-
rected) thickness of the cerebral cortex of the Norway rat accord-
ing to the brain weight and also the average thickness in each of
the sections.

VI. DISCUSSION

The relations existing between each of the several localities
measured in this study of the Norway are quite similar to the
relations found in the cerebral cortex of the albino rat. Individual
variations appear, but these are no higher than +6 per cent,
compared with the average values of the group. No sex differ-

GROWTH OF THE CEREBRAL CORTEX

TABLE 6

Showing the corrected values of the cortical thickness in the horizontal section for

each individual and for each brain weight group.

The data for the correction-

coefficients are indicated separately for each brain and the coefficient is given with
the average for each group

BRAIN WEIGHT
GROUP

N XI d

N XII

Np XE b

N XIVe

fe esto

INXS VISE
h
d
b

INEXV IT £
b
d
h

N XVIII b
d

THICKNESS OF THE CORTEX

COM RETC TENE (HORIZONTAL SECTION)
BRAIN r
eee ae Diam. Loe Loe. Loc Loe Loe

fresh | W-B EN é Sey ee xaer ) ) | xray! |Averaze

Brain on slide |
grams NLM. mum. mene mm. mm, mm. mm. mm.
1.133" | 13.80) || 11.00 2.52 1.91 ie 1256.) d3t |) 1.80
1.160 | 18.80 | 10.10 2.85 1.99 1.92 1.69 | 1.50 | 1.99
1.199 | 13.90 | 10.80 2.52 1.84 1.75 L627) tessi el ssl
1.164 1.30 2.63 OD 1.80 JURE A lefts) | Leif
1.343 | 14.20 | 10.30 2.91 2.02 2203 1.85 | 1.57 | 2.08
OLS 1.38 2.91 2.02 2.03 1.85 | 1.57 | 2.08
1.407 | 14.20 | 10.60 2.57 2.06 1.93 1.72 | 1.48 | 1.95
1.428 | 14.35 | 10.70 3.19 2.14 2.08 I S2pealixoe | 2eG
1.443 | 14.35 | 10.50 2.96 PLP 2.24 1.95 | 1.69 ;} 2.21
1.475 | 14.55 | 10.90 2.92 2.08 2.03 IE Sis lh Tonal 2208
1.481 | 14.60 | 10.25 2.91 222, 1.88 1.74 | 1.56 | 2.06
1.447 1236) 2.91 2.14 2.03 1.81 | 1.57 | 2.09
1.511 | 14.65 | 10.10 3.19 Deon 2.15 1.97 | 1.78 | 2.28
1.529 | 14:50 | 10.50 3.11 PyePA | PAM P4 LAOR | A625) 2519
1.520 1.41 8.15 2.27 2.14 1.94 | 1.70 | 2.24
1.613 | 14.90 | 11.00 | 3.25} 2.84] 2.10 1. 965 PIS6G 2526:
1.666 | 15.00 | 10.95 2.95 2.23 2.22 OA leiGalpeese
NGA 5ton | 1130 2.93 2.14 712 185m eo 2hie2 ab
1.699 |) 14.75 | 11.05 | 3.338 2.36 192) iL OLAS || eZ el7,
1.663 1.35 8.12 Dal 2.09 LISS) I UGL NW irl 9,
Gli NS. A S| nea 2.89 2.18 2.16 1-93) 1262") 2.06
1.718 | 14.60 | 11.30 Qld MG 2.04 1.80 | 1.41 | 2.03
ionelon OO sce Dietil Pyare 23 M84 AS |) 2.410
NED) |) MO ZO | oles B27 I Peail Jess |) 22020 | gley2 0230
1.747 1.35 roe | eee | 21S | 1.90 \ 1 ore 2 aro
Le SlS a PLSLOON 1200) ) S065) 2521 2.08 1.84 | 1.57 | 2.15
1.870 | 15.40 | 10.85 3.60 2.38 2.14 1-96 ' 176 |2-3%
1.848 1.39 3.00 2.80 2.11 LGON| L267. \ e286:

|

24 NAOKI SUGITA

TABLE 6—Concluded

THICKNESS OF THE CORTEX
COE ESE: (HORIZONTAL SECTION)
BRAIN WEIGHT | BRAIN =
GROUP WEIGHT iam. :
W.Bon a Loc. Loc. Loe. Loc. Loe. z
fresh a IX X XI Ki jek oe
Bran Ones ide
gra ms mm. mm. mm. mm. mm, mm. mm. mm.
INPXCEXG C1953) 155655| 11S 70s oa 2a 2S 20 de Sieiezeos
1.958 1.34 SLs Old) emilee 2.01 | 1.81 | 2.26
N XX e | 2.008 |} 15.55 | 11.90 | 3.10

2228 | 2209 | ASST 3) A cb2 5 2.7
b | 2.028 |. 15.85 | 12-00). 2:78 | 2:05.) L907 ebs715) ae 09
2.018 1.31 2.94) 2.17 | 2.038 | °1.79 | 1.48 | 2.08

NXT £ | 22150) 16.55 | 12:10.) 3.30 | 266.) 2.22.) 1:94) box | e2eee
J |) 2.162). 16.25.) 12-40 | 3-60) 2es87|- 2° 1.98 | 1.57 | 2.34
2.156 1.34 8.45 | 2.52) 2.19 | 1.96 | 1.67 | 2.34

N XXII
N XX a} 2.345 | 16.55 | 12:90 | 3.14) 2:58°| 2g) 2695 s4 | 2-22
2.345 1.28 3.14] 2.58 | 2.17 | 1.69 | 1.54 | 2.22

ence in cortical thickness is recognizable when the brain weights
are similar.

In the sagittal sections, the cortex attains nearly its full thick-
ness when the brain weighs 1.63 grams (Group N X V1), while in
the frontal and horizontal sections, this is attained somewhat
earlier, that is, in the brains weighing 1.53 grams (Group N XV)
(cf. charts 3, 5, 7, 8). In the general average thickness of the
cortex of the Norway rat, the full thickness is attained in the
brains weighing about 1.53 grams, at which phase the body weight
observed is about 55 grams (tables 1 and 2) (chart 8). In the
full grown Norway rat at brain weights between 1.6 and 2.4
grams, the average cortical thickness ranges between 1.97 and
2.14 mm., with a mean value for Groups N XVI-N XXIII (table
7) of 2.06 mm. The average thickness for each locality is given
in table 8 for the Norway rat, together with the corresponding
values for the Albino, thus making it possible to compare the
cortical thickness in the two forms.

GROWTH OF THE CEREBRAL CORTEX 25

TABLE 7

Showing the average corrected thickness of the cerebral cortex in the Norway rat for
each brain weight group.

FRONTAL

SAGITTAL SECTION = HORIZONTAL SECTION GENERAL AVERAGE
BRAIN WEIGHT eres
GROUP 7S ee Ss
bea Thickness | Thickness esa Thickness bias Thickness
grams mm. mm. grams mm. grams mm.
N XI 1.164 1.61 1.88 1.164 a teVe 1.164 1.79
N XII
N XIII 1.369 13 1.96 1.343 2.08 1.360 1.92
N XIV 1.480 1.84 1.95 1.447 2.09 1.436 1.96
N XV 1.537 1-82 2.04 1.520 2.24 1.532 2.03
N XVI 1.629 1.88 2.08 1.663 2.19 1.640 2.05
N XVII 1.739 1.94 2.07 1.747 2.19 1.742 2.05
N XVIII 1.829 1.93 2.08 1.843 2.26 1.834 2.09
N XIX 1.972 1.97 2.00 1.953 2.25 1.965 2.07
N XX 2.052 1.87 1.96 2.018 2.08 2.041 1.97
N XXxI 2.172 1.99 2.08 2.156 2.34 2.166 2.14
N XXII
N XXIII 2.345 1.86 2.345 2.22 2.345 2.04

Within the limits of our material, the course of development
of the cortical thickness in every locality seems, in general, simi-
lar to that in the corresponding locality of the albino rat, the
descriptions of which were given in the former paper (Sugita,
17 a, pp. 574-577).

VII. A COMPARISON OF THE NORWAY RAT WITH THE ALBINO RAT
IN RESPECT OF CORTICAL THICKNESS

The main object of the present paper is to compare the data
from the Norway with those from the albino rat, in respect of
the cortical thickness, a comparison of much interest, since the
two forms are so closely related genetically and at the same time
show differences in body size and in absolute brain weight which
have been already noted.

Comparing the mature brains, which weigh alike, of the both
forms (table 8), the Norway cortex, whose thickness on the av-
erage in Groups N XVI to N XX (brain weight average 1.844
grams) is 2.05 mm., surpasses by 0.15 mm. or 8 per cent the albino
cortex, whose thickness on the average in Groups XVI to XX

26 NAOKI SUGITA

(brain weight average 1.815 grams) is 1.90 mm. Here the al-
bino cortex is taken as the standard for the determination of
the percentage difference. For the comparison of each locality
and the averages of each section, table 8 is to be consulted. It is
remarkable that both in the sagittal and horizontal sections the

34 = + — :
| | | | |
32 +—— 4+ — = a } 1 |
} |
| | |
30! —+—_- 1 all i i | —;-—5—+ | ; |
| | lo || | |
28 =e + £. ns —
| °
PO a SS ES eS ee eee 4
| | J | |
| ° } | |
24; eh ee ech, EE --h -+ a
| | | |
| | | |
|e = ——— wo al thea:
| i | |
20 a a L + top
| . le
48|- t T Te | i 7
| |
‘ae + . id 4 4 4 =e a all = zoe
: eg ae |
44} —_1 SaaS ete + ts ti 4
| | | Vahezdlie | situs
12/ {| oe (Peseel D ee > ee L eae
10) — ails Soll ie ea weak os
(see a | AP |
pepeee) Sekaee | + — + — 4 =
| |
a6| | i = | = a th = 4
| | |
| | |
ial oA ee ee on | ;
| ‘i
a2 —— -+—}_}__ {+
r) | | =i pe Jt | Ail | |
LOPS A AS Gy di 18) ASN AOy 21 22 Seams

Chart 2 Giving the corrected thickness of the cerebral cortex of the Norway
rat in the sagittal section. Individual entries for the cortical thickness at lo-
calities I and V, and the average thickness of thé sagittal section (localities I, II,
III, IV and V) are given. Based on table 4. ° Cortical thickness at locality I.
Corrected. Cortical thickness at locality V. Corrected. * Average thick-
ness of the sagittal section. Corrected.

percentage differences follow in the same order from the frontal
to the occipital pole, rising towards the occipital pole.» The oc-
cipital parts, represented by the pair of localities V and XIII, are
the most developed in the Norway, surpassing the corresponding
parts of the Albino by 15 and 28 per cent respectively. The
pair of localities IV and XII, whose positions are adjoining, show
also a marked excess in thickness, that is, 10 and 11 per cent

GROWTH OF THE CEREBRAL CORTEX 2

respectively. The only other large difference is 15 per cent at
locality VI.

Accordingly, in the mature rats, the average thicknesses in the
sagittal, frontal and horizontal sections are respectively 6.7, 9.1

o4|__+

| |
|
Q2;/—_+ —_ + —_J—_+_ —_+}_ __+ = = call = ++
| | |
°

(EA ba ea SE La elle i
{DEA OSE Sd GMa TAO ETOMECOM dM een tai eas gee

oa |}

Chart 3 Giving the average thickness of the cortex for each brain weight
group at localities I, II, III, IV and V in the sagittal section and the average
thickness at five localities in each brain weight group in sagittal section. Based

on table 4. -— -—-— (above the heavy line) Cortical thickness at locality I.
Corrected. ------- (above the heavy line) Cortical thickness at locality IT.
Corrected. -— -— -— (near the heavy line) Cortical thickness at locality III.
Corrected. --------- (below the heavy line) Cortical thickness at locality IV.
Corrected. -—-—- — (below the heavy line) Cortical thickness at locality V.

Corrected. °
weight group.

°S Average thickness of the sagittal section by each brain

and 8.0 per cent greater and the general average thickness is,
consequently, 8 per cent greater in the Norway than in the al-
bino rat, while the brain weights are almost the same (about 1.8
grams).

As regards the differences in cortical thickness here found a
few comments may be made. Possibly all of the larger differ-

28 NAOKI SUGITA

28 T | T ] ] 1
26 | | | | |

T Saf t + =

| | | | | |
24 — + +

aa elie ecck aes
22} | It 4 2 ee ae ee ee +

| | i | [*. |-. | 4 ;
20 foas aes a aan alien iliaaa ‘i

| | les | | | |
18 = t ol : “ Jo] aS |

| Mi) A site ‘i
i | ieaSeateatic wt al 4
14 | aes]

| 4 Toot i
a i a

| | | |
1.0 iP + t t eaten
0.8|—— | Lael

resins! | Ie |
26 | 4 | eel ae

el |
04+ — mee —+ sea ltnat} = ae }

here Selhoee se || | |

| | | | | |
02 ral = = SS }
° 1 | | S| [lf | | | 1

1 Sal ad Si SEIS SHE SIS IK) 20) Pe Prerrs

Chart 4 Giving the corrected thickness of the cerebral cortex of the Norway
rat in the frontal section. Individual entries for the cortical thickness at locali-
ties VII and VIII, and the average thickness of the frontal section (localities VI,
VII and VIII) are given. Basedon table 5. ° Cortical thickness at locality VII.
Corrected -*< Cortical thickness at locality VIII. Corrected. * Average thick-
ness of the frontal section. Corrected.

mm.
28) T ssa T —————$—_—_—_—_
|

26 +

24

40 1 1 —t —t

08 |

06 |
of a

02 4 : +

“G9 i213 4 15 16 17 1819 20 2f a2 gm
Chart 5 Giving the average thickness of the cortex for each brain weight group
at localities VI, VII and VIII in the frontal section and the average thickness at
three localities for each brain weight group in frontal section. Based on table 5.

-------- Cortical thickness at locality VI. Corrected. -— -— -— Cortical
thickness at locality VII. Corrected. ——— Cortical thickness at locality VIII.
Corrected. *——*F Average thickness of the frontal section by each brain

weight group.

GROWTH OF THE CEREBRAL CORTEX 29

ences noted may be correlated with differences in function, but
at present we shall consider only those which appear in the oc-
cipital cortex, that is, at localities IV, V, XII, and XIII. There
is reason to think that the eye and the visual apparatus in gen-
eral are less well developed in the Albino than in the Norway rat.

|
|
nals
&
:
Je
:
[ies

cy
i

i | |
o4} et + ro at a eo

ae ——— ee { a — —— |
|

|

| if

| i jerome | L |

Ty GY G2 Sey GRU KS Sip SER SIS) GXe) 5 aN Oey 7a arcs

Chart 6 Giving the corrected thickness of the cortex of the Norway rat in
the horizontal section. Individual entries for the cortical thickness at localities
IX and XIII] and the average thickness of the horizontal section (localities IX, X,
XI, XIf and XIII) are given. Based ontable 6. ° Cortical thickness at locality
IX. Corrected. *Cortical thickness at locality XIII. Corrected. * Average
thickness of the horizontal section. Corrected.

The visual cortex of the rat is at the occipital.end of the brain
(Ferrier, 86) and would probably be underdeveloped in the Al-
bino in which vision was less perfect. The relatively less thick-
ness of the cortex in the localities IV, V, XII and XIII in the
Albino brain would therefore fit with the diminished visual func-
tion in this form.

30 NAOKI SUGITA

If, during the growing period, a comparison of cortical thick-
ness in brains of like weight is made, the result is somewhat puz-
zling, as seen in chart 9, which gives the thickness of the cortices
of the Norway and the albino rats in brains of the same weight.

‘

38 T = = = = ]
x6 | a = t— |
| | | | |
34 t - = VN |
ees hy Ne TY
at | |
ae SESS EERE
| | | Seine | Al
a! | | /
30 si ai i ial {
| mel | |
28 + - - + t se 1S
| |
26) AE — ed ——
| ee | |
24 - + 7 |
22 | i
|
2.0} ;
al
48 t
16 1 +
44 } ; —
12|- | d:
| |
40} }
i
| | | |
oe T ails flea
| | | | |
4 7 | 4 | a | |
04} =! | | ! Hel =! ———t
i esata La L
|
ala aa Lea
PLC ne Yee i De fy a T- S 2

Chart 7 Giving the average thickness of the cortex for each brain weight
group at localities IX, X, XI, XII and XIII in the horizontal section and the
average thickness at five localities in each brain weight group in horizontal sec-
tion. Basedon table 6. (above the heavy line) Cortical thickness at locality
IX. Corrected. — -— :— (above the heavy line) Cortical thickness at locality
X. Corrected. ---------- Cortical thickness at locality XI. Corrected.
-—-—- (below the heavy line) Cortical thickness at locality XII. Corrected.
(below the heavy line) Cortical thickness at locality XIII. Corrected.
*H Average thickness of the horizontal section for each brain weight group.

Generally the cortical thickness of the Norway rat, whose brain
weighs more than 1.3 grams, is clearly higher than that of the
albino rat of like brain weight, while in brains weighing less than
1.2 grams the relation is reversed. This seems surprising, but

GROWTH OF THE CEREBRAL CORTEX 3l

has its reason. If the data are treated as follows, which seems
to me quite a rational treatment, the reason will be disclosed.°
The brain of the Norway rat at birth weighs usually somewhat
more than that of the newborn albino rat, and the final brain
weight in the full grown Norway is ca. 2.5 grams or 25 per cent
higher than that in the mature albino rat of like age, which
weighs about 2.0 grams. As already shown by Donaldson and

ho SSeS + ——— +
| | | | | | | | | | 5]
24 }— — 4p +—+ = =!
} | | | |. | a | | Nix *4
22 r+ + | tL {___.+ t =:
ie sire = ele wae
| | | jee |e | i = r
| | aie } Aaa ene ~™ = 4 —S at S
a ee eae aS ee es | ee
| | ae |
46+ - = t
| | 4 4
a4) T | +—
|
42 + a_i IL = jt
| |
40 |
| | | |
| | | |
0.8 | | t
06 + ——t 2 See
| | | |
} | | | | |
04 |— mt + ee a
| |
a2) Ss ——= Saale bt rs 1 fact =

40 if 12 13 14 45 16 17 18 49 20 21 22 23 gre

Chart 8 Giving the corrected thickness of the cortex in the sagittal, frontal
and horizontal sections and the general average thickness for each brain weight

group. Based on table 7. Norwayrat. -—-°-—-—S Average thickness of the
cortex in sagittal section. Corrected. ———-F Average thickness of the cortex in
frontal section. Corrected. --------- H Average thickness of the cortex in

horizontal section. Corrected ° eA General average thickness of the cortex
of three kinds of sections. Corrected.

Hatai (’11), the span of life is probably the same in both the
forms, extending to about three years. So, if throughout this
span of life the developmental course of the brains was quite
similar for both forms, the brains which have like weights would
not represent the same stage of the development, but on the con-
trary, a brain of the Norway rat would be under these conditions,
in a younger stage.

Table 9 gives the percentage of water in the brains of the Nor-
way and of the albino rats. The comparison of the data of the

32

NAOKI SUGITA ~

TABLE 8

A comparison of the cortical thicknesses at each locality and on the average, in the

adult Norway and the albino brains of the same absolute weight.

The measure-

ments used here are average values of Groups N XVI-N XX and Groups X VVI-XX
respectively, taken from tables 4 to 6 of this paper and tables 6 to 8 (Sugita, ’17a).
The corresponding brain weights are 1.844 grams in the Norway and 1.815 grams
The thickness of the Albino cortex is always taken as the stand-

in the Albino.
ard for computing the percentage differences

SECTIONS

LOCALITIES

THICKNESS OF THE CORTEX

CORTEX OF THE
NORWAY RAT EX-

Norway rat Albino rat CEE DSSS
mm. mm. per cent
Locality I 2.84 2.80 1.4
IL 2.06 1.92 Tos
Sagittal III 1.82 1.74 4.6
IV 1.51 1.36 10.0
V 1.37 1.19 155,11
Average........ 192, 1.80 6.7
Locality VI Aral 1.84 14.8
Frontal VII 2.28 2.18 4.6
Vill 1.73 1.59 8.9
Average.:...... 2.04 1.87 9.1
Locality IX 3.09 3.08 0.3
x E23 2.06 8.2
Horizontal XI 2.10 2.04 3.0
XII 1.90 Ia ileal
XIII 1.63 2% 28.3
Average...... Y 2.19 2.03 8.0
General average ...........-.- 2.05 1.90 8.0

two forms is made so as to bring those of approximately the

same age on the same line of the table.

It will be seen by these

comparisons that the Norway rat brain, if paired with the albino
rat brain of like age, shows almost the same value of the percent-
age of water, while the brain weight differs by 16 to 20 per cent
in favor of the Norway rat brain, the weight of the Norway brain

being taken as the standard.

So, from the point of view of age, a Norway rat brain should
be in the same phase of development with an albino brain,

GROWTH OF THE CEREBRAL CORTEX a3

TABLE 9

Giving the percentage of water in the brain of the Norway and of the albino rats of the
same age. The comparison of the data of the two forms is made so as to bring those
of approximately the same age on the same line of the table. Based principally on
tables 10 and 12, given by Donaldson and’ Hatai (711) on pp. 439-443, Jour. of
Comp. Neur., vol. 21

NORWAY RAT (MALES) ALBINO’ RAT (MALES) OF LIKE AGE
PERCENTAGE OF WATER : LESS THAN
AGE Wana Setar ee sae arcane oe
OBSERVED eer eae Sateanese CALCULATED|CALCULATED] aap
days grams grams per cent per cent grams grams per cent
i 5.1 0.2361 88 .2 88.00 4.7 0.217 8
10 12.2 0.859 86.9 87.05 TRS 0.840 2
13 18.1 1.245 85.3 85.39 14.9 1.011 19
15 - tate 1.195 84.5 84.58 16.1 1-057 12
16 26.1 1.368 82.8 84.19 16.7 TOC 21
19 25.5 1.423 81.5 83.12 18.7 1.131 21
25 32.6 1.498 80.9 81.39 23.9 1.237 17
40 35.88 1.525 79.2 4 79.39 42.5 1.434 6
47 38.5% | 1.522 79.3 79.24 54.1 1.507 1
106 68 .68 1.878 78.4 78.50 174.0 1.830 3
200.0 2.152 78.7 78.59 160.0: 1.807 16
215.0 PARC 78.8 78 .53 170.0 1.824 16
231.0 2.20 78.6 78.45 180.0 1.8388 16
248 .0 2.23 78.7 78.38 190.0 1.854 17
267 .0 2.25 78.2 78.32 200.0 1.866 ilf/
287.0 2.28 78.2 78.24 210.0 1.879 18
308 .0 2.31 78.9 78.18 220.0 1.890 18
331.0 2.33 78.2 78.12 230.0 1.903 18
355.0 2.35 78.3 78.11 240.0 1.913 19
380.0 2.38 78.2 78.10 250.0 1.923 19
406.0 2.41 78.0 78.06 260.0 1.933 19
434.0 2.43 78.2 77.96 270.0 1.944 20
463.0 77.9 77.50 280.0 1.954
494.0 78.0 290.0
525.0 78.0 300.0

1 The data given in this column below this entry are based on unpublished ob-
servations of Donaldson and Hatai, the records of which are kept in the Wistar
Institute.

* The data given in this column below this entry were obtained by calculation
according to body weight.

3 As the result of confinement, the body growth in the Norway is remarkably
retarded.

THE JOURNAL OF COMPARATIVE NEUROLOGY, VOL. 29, No. 1

34 NAOKI SUGITA

which weighs 16 to 20 per cent less. With this relation in view,
I reduced by 18 per cent—which is the mean value of 16 to 20
per cent (see table 9)—the weight of the Norway rat brains in
table 7, and assumed that I thus obtained brain weights which
represent the corresponding brain weights of the albino rat in
respect to the cortical development. I have plotted the values
for the actual cortical thickness on the reduced brain weights by

mm

26 aa ins, al call wl mele = T =

24 /——_+___+_+_ — f= ea — | + + wh

22 = re } q -- =
a - |

20 { | | a ae lei

ee | fe 01 Fe acne (eee ea eee a |AL

4s | [a aie
| aa es |

46 | ]

44 + | a 5 (Ces el ase | 4

1 T jt | +—+ | ——t | T
es | | | | | |

40 | : t + + t } = T 1 7 L T

ieee UI Ce ae 1 By 2s | | SS ea)

ae | | 4 | r} | | | 1

06 cid es oe ee r ae | | oon 71 ] Hol | |
| | |

eH

| | | |
gif ik eg : ) =i — | } > =
Keddie 1 Ia ea | Hae) alata
205 QLPLOL TOS TOA OOMOCMNO TAOS TUCO LO 2am SCAT a Site ONAN e2 ee eO I fet

Chart 9 Giving a comparison of the thickness of the Norway cortex with that
of| the albino cortex, on brain weight. °¢ °N General average thickness of the |
Norway cortex according to the actual brain weight group. - - - - - AL General
average thickness of the Albino cortex according to the brain weight group.
Smoothed. Taken from chart 9 of the second paper of this series. *—*—®
N’ General average thickness of the Norway cortex entered according to the re-
duced brain weight representing the albino brain weight of the corresponding age.

the dot and dash line in chart 9, in which the smoothed graph for
the cortical thickness of the albino rat is represented by a dotted
line. Glancing at the chart, my assumption appears to be jus-
tified as both the graphs for the reduced Norway and the Albino
are found to run a similar course. This relation is acceptable,
since, as shown in the tables given by Donaldson and Hatai (11),
and also by Miller (11), the relative weight of the brain in the
mature albino rat is 12 to 16 per cent less than in the Norway rat
of like body weight, and, furthermore, the relative weight of the

GROWTH OF THE CEREBRAL CORTEX 30

body in the Albino is about 20 to 40 per cent less than in the
Norway rat of like age (table 9). Accordingly, the albino brain
should be about 18 per cent or more, less than the Norway brain
of like age, and the data for the thickness of the cortex in the
two forms show a fairly constant relation, when plotted as in
chart 9 in accordance with this assumption (see also table 3,
Sugita, 717 a).

As stated, Norway rats under about 10 days of age have not
been studied, but a comparison of the graph for the thickness of
the cortex in the normal albino rat with the graph forthe Norway
cortex displaced for age makes it reasonable to assume that a
Norway brain which weighs 1.16 grams (Group N XI) corre-
sponds to an albino brain which weighs about 0.95 grams (Group
IX), at which stage the cerebral cortices of the both forms have
nearly completed their active growth in thickness and are going
over to the second phase, during which the cortical area keeps
pace with the increase in brain volume. It may be assumed
also (see later) that, in the Norway rat, with a brain weight of
about 1.4 grams the cortical myelination is beginning to take
place.

Thus in the postnatal life of the Norway rat, the first phase of
the development of the cerebral cortex covers the period during
which the brain weight increases to 1.16 grams from birth, when
the brain weight is about 0.25 grams, and the second phase of
the cortical development covers the period, during which the
brain weight increases from 1.16 grams to about 1.44 (Group
N XIV) when the cortex attains within 4 per cent the full thick-
ness. By the middle of the second phase the process of myelina-
tion is active, and before the end of this phase the cortex has
already attained nearly its full thickness.

This assumption, that the completion of the cortical develop-
ment in thickness coincides with the period of active myelination,
is supported ‘by another set of facts. Table 10 gives the abso-
lute weights of the dry substance in the brain of the Norway rat,
arranged according to brain weight. These values were calcu-
lated by me from tables originally given by Donaldson and
Hatai (11). The data are plotted in chart 10, which also gives
the corresponding data for the albino rat, in a dotted curve.

36 NAOKI SUGITA

TABLE 10

Giving the weight of the dry substances in the brain of the Norway rat according to
brain weight. Based on the observed data given by Donaldson and Hatai (’11),
in p. 448, Jour. Comp. Neur., vol. 21. Both sexes averaged. *Males only.

WEIGHT OF THE WEIGHT OF THE
TOTAL BRAIN WEIGHT DRY SUBSTANCES IN TOTAL BRAIN WEIGHT DRY SUBSTANCES IN

THE BRAIN THE BRAIN
grams grams grams grams
0.25 0.041 1.55 0.309
0.35 1.65 0.339
0.45 165 0.377
0.55 1.85 0.400
0.65 0.067* 1.95 0.407
0.75 0.100 2.05 0.445
0.85 0.100 2.15 0.460
0.95 2.25 0.498
1.05 2.35 0.500
1.15 0.155 2.45 0.540
1.25 0.210 2.55 0.534
1.35 0.229 2.65 0.575
1.45 0.291 2.75 0.600*

03

a2

a4 1

T ; ++ +

0 a2 04 a6 08 10 12 4 16 18 20 22 24 26 28 gms

Chart 10 Giving the absolute weights of the dry substance in the! N orway
brain, arranged according to brain weight, based on the observations of Donald-
son. and Hatai (’11), accompanied by the corresponding data for the albino rat,
in a dotted line. ™* and * show the turning points of the curves.

GROWTH OF THE CEREBRAL CORTEX 37

This chart shows clearly that the solids in the Norway brain
increase rapidly after the brain weight has reached something
more than 1.2 grams (see x). This turning point of the graph
corresponds to 0.95 grams of brain weight in the Albino (see *).
It was found in the albino rat that, when the brain weight has
surpassed 1.15 grams, namely 0.95 plus 0.20 grams, myelination
of the cortical fibers is active. Hence, in the Norway brain, the
myelination in the cortex should be active when the brain weight
has reached 1.44 grams, namely somewhat more than 1.2 plus
0.2 grams. Furthermore, as we have seen that in the albino rat
the beginning of myelination in the cortex coincides with the
phase when the cortex has nearly attained its full thickness, so
we see the same relations in the Norway rat also.

From these facts we conclude that the brains of the both forms
pass through the same course of cortical development according to
age, as the span of life is the same in the two. The weights of
the brains which are in the same stage of development, are how-
ever not the same in the both forms, being in the Norway rat
about 18 per cent—the Norway brain weight being taken as
the standard—heavier than in the albino rat. The statement of
Donaldson which was expressed in the paper cited, to wit: “‘If
in the animals compared the brain weights are the same, then
the Norway rat has a smaller body weight and a higher percent-
age of water in the central nervous system,” might be rewritten
as follows: When ages are the same, the Norway rat has a greater
body weight, a heavier brain (18 per cent more in weight), a
thicker cortex and nearly the same percentage of water in the
central nervous system.

A comparison of the cortical development in the two forms
can be made adequately only by first reducing by 18 per cent
the actual brain weight of the Norway rat and then comparing
the cortex in both forms according to the corrected brain weight.
Since mature Norway brains have only a slightly greater volume
than the Albino brains of like weight (see table 4 A, Sugita, ’18),
but at the same time have a cerebral cortex on the average 8 per
cent thicker, it follows that in the Norway brain the proportion
of gray substance is greater. This difference apparently accounts
for the higher percentage of water found in the Norway brain.

38 NAOKI SUGITA
VIII. SUMMARY

1. The thickness of the cerebral cortex of the Norway rat has
been systematically investigated, employing as material 36 males
and 18 females, all over 17 grams in body weight, and using uni-
formly the methods which were adopted by me for the investi-
gation of the cerebral cortex of the albino rat.

2. The observed data are first given and later are corrected to
the values for the fresh condition of the material. The corrected
data are given fully in tables and in charts. ;

3. The relations of the cortical thicknesses at the several lo-
calities measured are quite similar among themselves to those
found in the albino rat. The average thickness of the cortex in
the adult Norway rat is always higher (1 to 28 per cent) than
that of the corresponding locality in the adult albino rat. The
occipital cortex is better developed (thicker) in the Norway rat.
This is to be associated with the more perfect visual apparatus
in the Norway rat.

4. As to the phases of development of the cortical thickness, a
Norway brain of a given age corresponds to an albino brain,
which weighs about 16 to 20 per cent less. The Norway brain
weighing 0.25 to 1.16 grams (Groups N II to N XI) is inits
first phase of active development which corresponds to an Al-
bino brain weighing 0.25 to 0.95 grams. The Norway brain
weighing 1.16 to 1.44 grams (Groups N XI to N XIV) is in its
second phase of development of the cortex corresponding to the
albino brain weighing 0.95 to 1.15 grams. "

5. The cortex of the Norway rat attains nearly its full thick-
ness at the time when the brain weighs somewhat more than 1.44
grams, corresponding to the age of twenty days and to a body
weight of something more, than 36 grams. At this phase probably
the rapid myelination of the fibers in the cerebral cortex is taking
place.

6. The general average thickness of the cortex in the mature
Norway rat is 2.06 mm., exceeding by about 8 per cent that of
the albino rat brain of the same weight.

GROWTH OF THE CEREBRAL CORTEX 39

7. Owing to the greater thickness of the cerebral cortex the
mature Norway brain contains more gray matter than does the
albino brain of like weight and this excess of gray matter ex-
plains the somewhat higher percentage of water found in the
Norway brain.

LITERATURE CITED

Donaupson, H. H. anp Harar, S. 1911 A comparison of the Norway rat with
the albino rat in respect to body length, brain weight, spinal cord
weight and the percentage of water in both the brain and spinal cord.
Jour. Comp. Neur., vol. 21, pp. 417-458.

Donatpson, H. H. 1915 The Rat. Memoirs of The Wistar Institute of Anat-
omy and Biology. No. 6.

Ferrier, Davin 1886 The funetions of the brain. 2nd ed. Smith, Elder &
Co., London, pp. 261-262.

Fortuyn, A. B. D. 1914 Cortical cell-lamination of the hemispheres of some
rodents. Arch. Neurol., Path. Lab. London County Asyl., vol. 6,
pp. 221-354. Mus decumanus (Pall), p. 260.

Lewis, Bevan 1881 On the comparative structure of the brain in rodents.
Phil. Trans., 1882, pp. 699-749.

Mitter, Newton 1911 Reproduction in the brown rat (Mus norvegicus).
Am. Naturalist, vol. 45, pp. 625-635.

Suarra, Naox1 1917 a Comparative studies on the growth of the cerebral cor-
tex. II. On the increases in the thickness of the cerebral cortex dur-
ing the growth of the brain. Albino rat. Jour. Comp. Neur., vol. 28,
pp. 495-510.

Suerra, Naoki 1918 Comparative studies on the growth of the cerebral cortex.
III. On the size and shape of the cerebrum in the Norway rat (Mus
norvegicus) and a comparison of these with the corresponding charac-
terS in the albino rat. Jour. Comp. Neur., vol. 29.

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METABOLIC ACTIVITY OF THE NERVOUS SYSTEM

II. THE PARTITION OF NON-PROTEIN NITROGEN IN THE BRAIN OF
THE GRAY SNAPPER (NEOMAENIS GRISEUS) AND ALSO THE
BRAIN WEIGHT IN RELATION TO THE BODY
LENGTH OF THIS FISH

SHINKISHI HATAI

The Wistar Institute of Anatomy and Biology, and Department of Marine Biology,
Carnegie Institution of Washington

ONE CHART

The prime object of the present investigation was to extend
some observations made recently concerning the metabolic ac-
tivity of the central nervous system of the albino rat (Hata,
17) to the nervous system of lower vertebrates. It was my
hope that such a comparative study might yield valuable data
for an understanding of the complex phenomena of metabolism
in this important organ.

In the course of the present investigation I was able to ac-
cumulate a considerable amount of data on the weight of the
brain together with its water content, a study which has re-
vealed several interesting facts which have not been yet fully
appreciated, so that I have decided to present these data also
in the following pages. In connection with this work, it is a
pleasure to acknowledge my indebtedness to Dr. A. G. Mayer,
Director of the Department of Marine Biology of the Carnegie
Institution of Washington. Dr. Mayer not only granted me
the privileges of the laboratory at the Dry Tortugas, but gave
me encouragement and many helpful suggestions throughout
the course of this work.

41

42 SHINKISHI HATAI

MATERIAL USED

The gray snapper, Neomaenis griseus, was chosen for this
investigation not only because these fish are abundant in sub-
tropical seas, but also because they possess numerous virtues
for experimental purposes. The snapper may be kept in the
laboratory for a long period, and in captivity as well as when
free, takes almost any kind of food, cooked or raw, animal or
vegetable. The fish is well known for sagacity and boldness
and is suited for various kinds of experimentation. Indeed the
snapper has already been carefully studied by Reighard (08)
as to its behavior. Thus, with the hope that the gray snapper
may in future prove to be a suitable form for certain lines of ex-
perimental work, I have utilized all the brains which have been
used for chemiéal investigation, together with some others, for
studying the growth of the brain in weight with respect to body
length. Most of the fish were secured by netting them, but on
account of the difficulty of getting the larger fish by this method,
I have also used dynamite as well as the hook and line. I
have noted in table 1 the method adopted for catching each
individual.

TECHINQUE EMPLOYED

The fish were examined as soon as they were brought into
the laboratory. However, as in the case, of netting them, when
too many were caught at once some were kept in a live box for
not more than two days, except in a few cases in which they
were kept for special purposes for several days. When the fish
were kept in a live box for more than two days it is so stated
in table 1.

In every instance the length of body was recorded in the fol-
lowing way. The fish was laid on its side and the length was
determined by means of calipers from the tip of the snout to the
middle of the caudal edge of the tail. The body weights of the
fish were also taken in a few instances. Although I realized
the desirability of recording the body weight in all cases, yet it
was not always possible to make this measurement.

METABOLIC ACTIVITY OF NERVOUS SYSTEM 43

TABLE 1

Showing the brain weights according to various body lengths, together with the per-
centage of water in the brain, of the gray snapper. Arranged according to in-

creasing body length

BODY

WATER IN

BRAIN WEIGHT BRAIN REMARKS
Length Weight
mm, grams grams per cent
88 2) 0.122 78.85 Net
137 43 0.234 78.63 Net
155 59 0.284 79.33 Net
PAG) 0.622 79.52 Net
216 140 0.628 81.12 Dynamited
217 0.483 78.34 Net
225 0.670 79.05 Net
227 173 0.627 80.43 Dynamited
237 0.575 78.19 Net
| PBS 197 0.660 79.91 Hook
240 0.711 79.92 Net
245 220 0.732 81.48 Dynamited
249 218 0.723 80.69 Dynamited
252 0.748 79.55 Net
252 0.762 78.64 Net
253 229 0.897 80.65 Dynamited
256 0.748 77.01 Net
258 0.828 79.47 Net
259 0.844 78.32 Net
262 0.833 78.75 Net
262 0.882 77.85 Net
263 0.864 77.29 2 | Net
*263 269 0.803 80.08 Hook
263 261 0.816 79.68 Hook
268 0.859 79.74 Net
269 0.781° 77.49 Net
271 0.921 78.78 o | Net
Qa 0.816 78.57 Net
278 0.848 78.32 Net
278 311 0.871 82.91 Hook
285 0.985 79.17 9 | Net
293 1.006 77.28 o | Net
294 0.861 78.86 o& | Net
295 0.925 77.56 o& | Dynamited
296 0.900 78.07 Net
298 0.982 78.49 o’ | Kept in live box 4 days
300 0.907 79.21 & | Dynamited
300 0.971 78.17 2 | Net
301 0.952 77.10 & | Net

44 SHINKISHI HATAI

TABLE 1—Continued

Leas BRAIN WEIGHT WATER VIN REMARKS
BRAIN
Length Weight
mm. grams grams per cent
302 1.042 77.87 2 | Net
302 1.042 77.06 3 | Net
303 0.776 75.40 9 | Dynamited
306 1.079 79.17 2 | Kept in live box
317 0.974 78.03 « | Net
318 1.072 79.57 Q | Net
330 1.124 76.51 | Net
335 681 1.164 80.07 9 | Kept several days in box
336 1.124 77.67 9 | Kept several days in box
340 908 1.126 76.16 9 | Net
34505 1.061 79.15 9 | Net
348 14 lbs. 1.141 77.46 2 | Net
353 2° Ibs: ilsalalys 76.63 9 | Net
353 2lbs: 1.169 77.81 9 | Net
360 1.178 7.88 o | Net
362 1257 78.65 o | Net
367 781 1.262 76.67 o& | Hook
369 | 1.286 77.08 9 | Net
374 2 lbs: 1.249 76.24 o | Net
380 3 lbs. 1.281 75.33 o | Net
385 1.418 o | Net
390 1.336 77.59 o | Net
392 1.353 79.67 o& | Net
392 1.644 @ | Dynamited
401 1.584 @ | Dynamited
408 1.618 @ | Dynamited °
416 1.6382 oa | Dynamited
424 1.369 78.54 9 | Dynamited
430 1.400 _ * @ | Dynamited
432 1.424 79.97 3 | Dynamited
438 1.530 os | Dynamited
439 1.400 Q | Dynamited
439 1.499 80.00 9 | Dynamited
441 1.601 @ | Dynamited
448 1.591 Q | Dynamited

As soon as the brain was exposed by means of a small bone
forceps, it was separated from the spinal cord between the first:
vertebra and the base of the skull. It was not practicable to
find the first spinal nerve or to determine the caudal end of the
fourth ventricle, methods which are usually adopted in separat-

METABOLIC ACTIVITY OF NERVOUS SYSTEM 45

ing the brain from the spinal cord in the mammalian nervous
system. Anteriorly the olfactory nerves were cut close to the
olfactory bulbs. The saccus vasculosus was not included with
the brain. The brain which was thus removed was placed in
a small bottle which had been previously weighed, and this was
weighed again to a milligram. After the fresh weight of the
brain was determined, the bottle with its contents was placed
in a steam oven at a temperature of 80°-90°C. for several days
(Tortugas laboratory) and then later dried at the Wistar In-
stitute under better laboratory conditions at 96°C. The various
other methods used for the analysis of the brain will be de-
scribed later.

THE BRAIN WEIGHT IN RELATION TO BODY LENGTH

Altogether observations on 74 brains of the gray snapper have
been made.

From table 1 the average brain weight of the sanpper for
several values of the body length has been calculated and the
results are given in table 2. :

In order to show the general distribution of the brain weights
in relation to the body length, I have prepared a chart based
on the data given in tables 1 and 2.

In the chart males and females are not distinguished. As will
be seen from chart 1, the distribution of brain weight in respect

TABLE 2
Showing the average brain weight of the gray snapper for the several values of the body
length
BRAIN WEIGHT

BODY LENGTH BODY LENGTH NUMBER OF

RANGE OBSERVED @beeea Capaned by SNAPPERS
mm. mm.

200-250 231 0.643 0.667 10
250-300 271 0.860 0.840 23
300-350 319 1.037 1.048 15
350-400 373 1.296 : 1.282 12
400-450 428 1.513 1.520 a

LSE AE A OS. Od Ot oad OF 1.070 1.071

46 SHINKISHI HATAI

to the increasing body length from 150 mm. upward is_ practi-
cally linear. This linear relation between these two characters
is better shown by the positions of the averaged values, which
are also plotted. It is well known that in the adult stage the
relation between brain weight and body length or body weight
is practically linear, even in the case of some mammals (see for
instance growth of brain in weight in the albino rat in respect
to body length or body weight, Donaldson, ’09) but it is re-
markable to find the linear relation in fish when they are so
small. This linearity during the period of early growth prob-
ably means that in the gray snapper the brain reaches its struc-

20
BEES RE DOE E RES eShooSheaee GBS
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foe af | | of ta ff a rs |e
IB EERE EERE REECE EEE tt Hts
EECCA TEEPE CEE CEP
Ha BEE Eee EEE EEE
io EEEEEE EEE EEC beatae EEE
ECE ESR PERE EEEEEEEEEE
Ho Hate oo a | eat i i
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PEEEEEEEEEEE Ee
A SHEDS See PR OSB SeomeGe se Sas le 0
0) 50 * 100 150 200 250 300 350 400 450

Chart 1 Showing the weight of the brain of the gray snapper according to
body length. The observed weights are represented by 74 fish. e = observed
weight — 0 — 0— = average observed weight (table 2).

tural maturity early, and that the subsequent increase in weight
indicates merely a uniform swelling of the nervous system as
a whole. The maturity of the brain at a relatively early stage
of growth may be inferred also from practical constancy of the
percentage of water in the brain from the very small to the very
large fish in this series (page 48).

It is to be regretted that it was not possible to obtain data on
smaller specimens, though every effort was made to obtain such
specimens while I was at the Tortugas Laboratory. We were
even unable to find any of the gray snapper fry, though the fry
of the school master (Neomaenis apodus) which is most closely

METABOLIC ACTIVITY OF NERVOUS SYSTEM 47

related to the gray snapper, was abundant everywhere. Pos-
sibly the months of June and July were not a proper season to
find them, or the fry of the gray snapper may not live in the
open seas or along the beach, but may be in hiding under the
intricate roots of mangroves, a tree not found on the Tortugas
Islands.

On account of the scantiness of the data on the gray snapper
less than 200 mm. in body length, I am unable to present a com-
plete record of the growth of the brain. However it appears
from the general trend of the growth curve that, with the possible
exception of the very early period, the relation between the
brain weight and body length does not deviate much from
linearity.

Kellicott (08) who studied the growth of the brain in the
smooth dogfish (Mustelus canis, Mitchill) in respect to the body
weight, found the graph to resemble that for the mammalian
brain; that is the graph shows a rapid rise at the early period
which is followed by a slower rate of growth. The form of the
curve suggests a logarithmic formula such as was used to repre-
sent the growth of the brain in the albino rat (Hatai, 09). In
other words the form of the graph for the gray snapper is strik-
ingly different from that for the dogfish. This difference may be
due to the fact that in the dogfish the brain possesses a voluminous
cerebellum, as well as olfactory bulbs, and the combined weights
of these two structures may be greater than that of the rest of
the brain, while these two structures in the gray snapper are
very small and the latter was not included. It appears that
these two parts, olfactory bulbs and cerebellum, of the dogfish
brain grow very rapidly during the earlier period, thus giving
the form of the graph similar to that for the mammal.

Since the brain weight of the gray snapper shows a linear
relation to the body length through a wide range, and since the
fish which are usually caught fall within this range, I have de-
vised the following formula for brain weight on body length,
in hopes that it may prove useful for some future investigation.

Brain weight (gms.) = 0.00433 Body length (mm.) — 0.333.

The results of the calculation are given in table 2 and there

48 SHINKISHI HATAI

contrasted with the observed values. The agreement is highly
satisfactory, and thus the formula may be employed when the
probable brain weight of the gray snapper in which body length
is known, is desired. I may point out that the absolute amount
of increment of the weight of the brain following every milli-
meter increase of the body length is slightly over four milligrams
(4.33 milligrams).

PERCENTAGE OF WATER IN THE BRAIN

Altogether 64 snappers were examined to determine the water
content in the brain, and the results have been already given
n table 1. An examination of the table reveals several strik-
ing relations in regard to the percentage of water. The per-
centage of water given by the smallest fish is 78.85 per cent while
that of the larger fish, having a body length of 424 mm. and
ranking in length third from the largest in which the water de-
termination was made, gives 78.54 per cent. The frequency
distribution of the percentage of water gives the following
results.

TABLE 3

Showiny the frequency distribution of the percentage of water in the brain of the
gray snapper

PER CENT OF WATER NUMBER OF CASES
75-76 2
76-77 5
77-78 : 15
78-79 : 17
79-80 16
80-81 6
81-82 2
82-83 1
Totalsnumibersa eee eee One eee 64

Despite the fact of a wide range in the percentage o° water,
the distribution of the frequencies is practically normal, and fur-
thermore the high and low values are well mingled, when these

METABOLIC ACTIVITY OF NERVOUS SYSTEM 49

values are arranged according to the body length of the snapper
(table 1) and there is no noticeable tendency for the lower values
of the percentage of water to occur more frequently among larger
fish, or vice versA. From this we infer that so far as the present
data are concerned, the percentage of water in the small and
large fish is nearly identical within a wide range of body length,
and therefore the percentage of water does not vary regularly
with the length or size of the fish. The average of 64 deter-
minations gives the percentage of water as 78.61 per cent.

This wide variation in the percentage of water I am unable
to explain at the present moment. It was thought at first that
the method of capture, particularly the use of dynamite, might
be responsible for it. Careful examination however (see re-
marks in table 1) of the table shows at once that such is not
the case, and these wide variations are not correlated with the
method of capture. It is true that the cranial cavity of the fish
contains liquid as well as a jellylike substance, and the adhesion
of particles of this substance may alter to some extent the per-
centage of water, but this factor is too insignificant to cause the
wide variations shown in the table.

One other factor, though it appears to be important, cannot
be readily tested, namely, masked age; that is a failure of the
size and weight of the fish to indicate the age. We have no way
to determine the age of the gray snapper. It may be that the
size of the fish shows a wide range of variation for any given age.
If size was positively correlated with age, then the low percentage
of water would be given by the older fish, and vice versa. There-
fore should we be able to arrange the data according to the ages
of the fish, not the size of the fish as has been done, the values
for the water should arrange themselves in a regular descending
order with increasing age. ‘This is, however, a mere speculation
and must wait the test of future investigation.

Still another possible factor is the low grade of organization
of the fish brain compared with that of the higher vertebrates.
It is conceivable that owing to this low grade of organization,
the structural maturity, or especially the processof myelination,
may not progress regularly, and that within the same size or at

THE JOURNAL OF COMPARATIVE NEUROLOGY, VOL. 29, No. 1

50 SHINKISHI HATAI

the same age, a wide range of variation might exist in respect
to the degree of myelination, according to the environment of
the fish or to the general nutritional conditions. Whether or
not this suggestion has a value, only further investigation can
determine.

Scott (12) found that the percentage of water in the brain of
the smooth dogfish differs very little between small and large
specimens, and gives on the average 78.5 per cent. Donaldson
(05) who examined the brains of the summer flounder (Para-
lichthys dentatus) noted also but slight variation in the percent-
age of water in the brains of large and small individuals. The
average from sixteen flounders in which the body weight ranges
from 539 grams to 1290 grams, is 78.45 per cent. Thus the
average percentages of water obtained by Donaldson, Scott and
by myself are 78.45 per cent (flounder), 78.5 per cent (dogfish)
and 78.61 per cent (gray snapper) respectively. For the purpose
of comparison I gave the percentages of water in the brain of
several fish, as determined by various investigators.

As will be seen from table 4 despite the widely different sizes
and probably wide differences in the age of fish, the percentages
of water in the brains are very close to one another, and further
interest lies in the fact that the values given by the fish brains
are not much different from the percentage of water in the adult
mammalian brain.

Since the reduction in the water in the brain is induced by the
deposition of the so called ‘myelin substance’ (Donaldson, ’16)
we may infer that the process of myelination in the fish brain
attains its mature form at a very early period’ thus permitting
but very slight variation from small to large individuals. Scott
(12) also concludes from his observations on the water content

1 In a private communication Dr. G. W. Bartelmez informs me that in Ameiu-
rus melas, larvae 10 to 12 mm. long show already well advanced myelination of
the roots of all the cranial nerves, as well as of the fasciculus longitudinalis medialis.
The age of the larvae, according to Dr. Bartelmez’s estimate, is about ten to
twelve days after fertilization. The largest adults measure as much as 120 mm.
or nearly ten times the length of the larvae in which the myelination is already
well advanced. From the above we may safely assume that myelination takes
place in the fish at an early stage of development.

METABOLIC ACTIVITY OF NERVOUS SYSTEM ol

of the dogfish that the differences in the reduction of water in the
two cases is that ‘‘the nervous (and body) changes which occur
in the mammal are post-embryonic and extra-utero. In the

TABLE 4

Showing the percentage of water in thebrain sof several fish. Data compiled from
various sources

c “iy || Sans
SPECIES Pet ene 8 : Rhee Sere eer SEX OBSERVER
a TRACT
Cyprinus carpio....... 77.50] 8.33 Von Bibra (1854)
Cyprinus barbus....... 78.00} 9.37 Von Bibra (1854)
SalmowarcOnans.,.4e5 - 78.92) 8.42 Von Bibra (1854)
' ~80.00
JUGS Cxfornagoadeeoue 81.93} 7.25 Von Bibra (1854)
FEES In ae ees, SN 8. 9.10 Schlossberger
. (1856)

Cyprinus auratus...... 77.80 Bezold (1857)
Summer flounder...... 539 | 393) 0.253) 78.05 Donaldson (1905)
Summer flounder...... 540 | 397| 0.305] 79.06 o'| Donaldson (1905)
Summer flounder...... 540 | 386) 0.351] 78.00 o'| Donaldson (1905)
Summer flounder...... 560 | 411] 0.338] 78.70 Donaldson (1905)
Summer flounder...... 630 | 409) 0.279) 78.06 o'| Donaldson (1905)
Summer flounder...... 640 | 404) 0.293) 78.43 @| Donaldson (1905)
Summer flounder...... 682 | 405) 0.288) 79.56 Donaldson (1905)
Summer flounder...... 834 | 440] 0.311] 78.60 @| Donaldson (1905)
Summer flounder...... 840 | 462} 0.358} 78.98 @| Donaldson (1905)
Summer flounder...... 860 | 453] 0.406) 78.37 @| Donaldson (1905)
Summer flounder...... 880 | 459) 0.381} 77.11 | Donaldson (1905)
Summer flounder...... 890 | 459) 0.417| 77.98 2} Donaldson (1905)
Summer flounder...... 1010 | 460) 0.355) 78.22 2} Donaldson (1905)
Summer flounder...... 1010 | 447| 0.369) 78.72 o’| Donaldson (1905)
Summer flounder...... 1080 | 478) 0.412) 79.06 2} Donaldson (1905)
Summer flounder...... 1290 | 505) 0.391] 78.27 2| Donaldson (1905)

AOU ee aera S66 Balog DOO CReeel bio crore 78.45
Mustelus canis!........ 78.5 Scott (1912)
Barracuda eer 12 lbs. |1047| 1.554) 79.39 o'| Hatai (1917)
Neomaenis griseus? .... 78.61 Hatai (1917)
Cherna americana:

Red Grouper......:. 142 lbs. | 807) 1.230} 78.80 Hatai (1917)
Shanks Spec cn sees 160 lbs. 32.593} 80.07 o'| Hatai (1917)

1 Average of 97 determinations from very small to very large.
Percentage of water shows very slight variation.
2 Average of 51 gray snappers. Range of variation is shown in table (1).

52 SHINKISHI HATAI

dogfish they take place in utero.’”’ He, however, has not de-
termined the water content in the brain of the dogfish in utero.

From the foregoing it is clearly important to determine the
water content in the brain of the fish at very early stages in
order to discover the period of rapid reduction which must take
place in consequence of the appearance of myelin in the brain.
It is the hope of the writer to do this in the near future.

CHEMICAL ANALYSIS OF THE BRAIN (GRAY SNAPPER)

Utilizing the materials which were employed for the deter-
mination of the percentage of water, I have determined the
nitrogen in the total solids, as well as the amount in the ether-
alcohol soluble fraction extracted from the total solids. The
results of these determinations are shown in table 5.

TABLE 5

Showing the amount of the ether-alcohol soluble and insoluble fractions in the brain
of the gray snapper; also the amount of nitrogen in the total solids, as well as the
nitrogen in the ether alcohol fraction

BRAINS WEIGHT OF NITROGEN IN
TOTAL 5;
SERIES = 8 SOLIDS | WATER | NITRO- Alcohols Alcohols
¢ 2 aE Residue ether Residue ether
D = Extract Extract
a &
weight per cent | mgms. gms. gms. mgms. mgms.
1 28 |27.303) 5.665) 79.14 | 462 2107 2.958 364 98
8.15%| 47.79% | 52.21% | 78.79% | 21.21%
2 19 |20.013) 4.588) 77.07 | 334 1.938 2.650 269 65
7.28%| 42.24% | 57.75% | 80.54% | 19.46%
IAWVCTAZO hte ceRe assess 78.11 | 7.72%| 45.02% | 54.98% | 79.67% | 20.38%

To carry out the determinations presented in table 5, I have
divided the entire materials into two groups in which group 1
gives for the brain a percentage of water which ranges between
78 per cent and 80 per cent, while in group 2 the percentage of
water ranges between 76 per cent and 77 per cent. All the other
brains which gave percentages of water beyond these limits were
excluded. Since all these data for the fish may be discussed
conveniently by comparing them with similar data obtained

METABOLIC ACTIVITY OF NERVOUS SYSTEM 53:

from the rat brain, I may state simply that the values for the
alecohol-ether soluble fraction obtained in this series of fish are
similar to those obtained by Von Bibra (’54) and by Schloss-
berger (’56) in other forms of fish (table 3).

CONTENT OF ‘NON-PROTEIN NITROGEN’ IN THE BRAIN

Altogether 44 snappers of medium size were used for the
purpose of determining the various extractive nitrogenous sub-
stances in the brain. These brains were divided into three sam-
ples, each giving nearly the same amount of moist brain weight.
One additional sample was obtained from the brains of the school-
master (Neomaenis apodus) which is a species most closely related
to the gray snapper.

The fresh brains of each sample were ground finely and then
preserved in 150 cc. of 2.5 per cent solution of trichloracetic
acid in water.- The ground brains were transferred to a bottle
by means of 50 cc. water, thus making altogether 200 ce. of
solution. The filtrates from this mixture were brought back
to the Wistar Institute for analysis. The methods used for the
determination of various nitrogen fractions were as follows:

1. Total non-protein nitrogen. Micro method of Folin and
Farmer as modified by Benedict and Bock.

2. Amino-acid nitrogen. Van Slyke’s nitrous acid seine
Also the same author’s micro apparatus. i

3. Urea nitrogen. Urease method.

4. Ammonia nitrogen. By the usual aerat on method.

In all cases, except the case of the amino acid, the nitrogen
content was determined by means of the DuBoseq colorimeter.
The results obtained from these determinations are given in
table 6.

Since it is my intention to discuss this einen later in com-
parison with the similar data recently obtained from the brain
of the albino rat, I shall merely direct attention to the fact: that
these three samples give results very close to each other... Fur-
thermore the results obtained from the sample of the school-
master also agree with those found in the case of the gray snapper.

54. SHINKISHI HATAI

TABLE 6

Showing nitrogen content in terms of the non-proteins, the amino acids, the urea
and the ammonia, in the brains of the gray snapper and of the ‘schoolmaster.’

BRAINS MILLIGRAMS NITROGEN PER 100 GRAMS OF FRESH BRAIN
SERIES ; Undeter-
Number Weight a genet Urea Ammonia panel
nitrogen
Neomaenis griseus
gms.
1 16 13.166 204 101.8 13e2 geez Te3
2 13 10.713 224 125.0 17.8 18.9 62.3
3 15 12.048 203 L212 ozs 7/2! 48.6
AVERAGE? Eo. ries 11.976 210 116.0 15.6 18.0 60.7
Neomaenis apodus
i | 10 | 11.195 | 295 | 126.0 | 17.3 | 17.2 | 64.5

This agreement in the various substances might also be taken
to support the belief of the systematists that these two species
are closely related.

COMPARISON BETWEEN THE GRAY SNAPPER AND THE ALBINO RAT
IN REGARD TO THE CHEMICAL COMPOSITION OF THE BRAIN

In order to compare the data on the chemical composition of
the brain in the gray snapper with those for the brain of the
albino rat, table 7 was prepared. The entries for the fish are
based on tables 5 and 6, while the data on the albino rat were
obtained from. an earlier paper (Hatai, 717).

When comparison is made between the fish brain and the en-
tire brain of the albino rat, we find a distinct difference in regard
to the content of the total nitrogen and of the nitrogen in the
lipoids, as well as in the total amount of the ether-alcohol ex-
tractive materials. These differences must undoubtedly be
correlated with anatomical differences in the two forms of the
brains. In the rat we find a well developed cerebrum and cere-
bellum in which the myelinated nerve fibers are relatively less
than in the stem, while the cell bodies are more abundant. On
the other hand in these fish brains we find a mere trace of the

METABOLIC ACTIVITY OF NERVOUS SYSTEM DO

TABLE 7

Showing the comparison of the gray snapper with the albino rat in regard to the chemi-
cal composition of their brains

a hee
ENTIRE | ENcEPHA- | ENTIRE
BRAIN LON SN
Water Insbrain percents... o arcceta ec sae 78.11 75.16 77.96
Total nitrogen in fresh tissue, per cent............ 1.69 1.89 1.95
Totalini¢rozenm:solids, per cent! 3645 sesenie - Gate leat 8.98
Alcohol-ether extract in solids, per cent........... 54.98 55.03 47-14
Nitrogen in alcohol-ether soluble fraction, per cent| 20.60 19.90 18.20
Percentage of water in lipoid-free tissue, per cent. 88.80 87.06 87 .00
Milligrams of non- protein nitrogen per 100 grams
of fresh tissue, milligrams See RR TI re dice pes RN 225 150 159
Partition of nitrogen in milligrams of nitrogen per
gram of solids
INON=PROLEIN=IN Nath sees tale cee was nse xe ees 9.6 6.0 7.6
AMIN O-aclds=Nieraasscrce cas sa edo Oo ee eee 5.3 2.9 3.5
Wire tae nme Nereis cere, ates oclemes WU AT SS Go's ORG 0.7 Ond
FAMITMLON IAIN Geant ances cite om eine he tere wrtaeh i ormieate. 5 0.8 0.6 ORG
Partition of non-protein nitrogen in percent of pro-
tein nitrogen
INU OMS JOT OG EMTS tray seeps r rte R rn) meats ear ima eats sep ty oar 13.04 9.72 10.37
PATVIM OP ACLU Steere NEA Ore TES RE (220 4.68 4.60
(ORR SERS cons OG tact acts PAST ORES Si tr cicieae one ea 0.97 1.05 0.95
AITO NE. obo permcoe Op elo eee De a obo polbo Gee 510i] 1.04 1.01

cerebrum and cerebellum compared with the size of the stem
in which the myelinated nerve fibers are abundant. Conse-
quently we should expect a higher value of the total nitrogen
in the rat brain than in the fish brain, since the former possesses
relatively a much greater number of cell bodies in those two
well developed parts, the cerebrum and cerebellum. At the
same time the rat brain ought to give relatively a less amount |
of lipoids, owing to the greater abundance of the gray matter
in the predominant parts. In the fish brain the insignificant
growth of the cerebrum and cerebellum makes the stem of the
brain relatively predominant in the quantitative relations, and
since the stem is the portion of the brain in which the myelinated
fibers are mostly found, we should expect the percentage value
of the lipoid fraction in the fish brain to be relatively higher
than in the rat.

56 SHINKISHI HATAI

If we compare now the entire brain of the snapper with the
stem of the albino rat brain (table 7) we notice a surprisingly
close similarity. This we should expect since as was already
stated the fish brain is practically represented by the stem, since
the cerebral and cerebellar portions are relatively insignificant.
Thus we notice the practical identity in the percentage values
of the total nitrogen, lipoid nitrogen, and the amount of the
lipoids. The percentage of water in the stem of the rat is how-
ever far less than in the entire brain of the fish which may be
accounted for by the fact that in the brain of the fish the cere-
brum and the cerebellum, though small in, relative quantity;
nevertheless are composed of structures rich in water, and thus
bring the value of the water higher in the fish than in the stem
alone of the albino rat brain.

The nitrogen content of the lipoid is slightly higher in the fish
brain than in the albino rat brain, though almost identical with
that in the stem. This difference may be due to the quantita-
tive difference in the proportion of various lipoids in which the
nitrogen content is not the same.

I now wish to consider the partition of the non-protein nitro-
gen in the fish brain compared with the brain of the albino rat. As
will be seen from table 7 the content of the non-protein nitrogen is
considerably greater in the fish than in the rat brain. We also
notice that the greater part of the non-protein nitrogen is repre-
sented by the nitrogen of the amino acids. The nitrogen values
given by both the urea and ammonia are small and are practi-
cally identical both in the fish and rat. The greater amount of
non-protein nitrogen found in the fish brain in comparison to the
rat is interesting, though I am unable to explain this difference
satisfactorily. I wish however to call attention to two factors
which may have some bearing on the difference just noted.

1. It seems probable that on account of the low grade of or-
ganization of the fish brain the physical consistence of the nervous
system may not be as stable as that of the more highly organized
mammalian nervous system, and thus the wear and tear process
may be greater and produce a correspondingly greater amount
of waste products in the fish brain. |

METABOLIC ACTIVITY OF NERVOUS SYSTEM 57

2. According to Folin and Denis (’14) the normal human blood
contains, on the average of four cases, 32 milligrams of non-
protein nitrogen per 100 ce. of blood, while Wilson and Adolph
(17) found in the blood of various fresh water fish much higher
values for the non-protein nitrogen (42 mgms. per 100 ec.) than
in the human blood, and furthermore these investigators found
a greater fraction of the non-protein nitrogen was represented
by the nitrogen of amino acids (23 mgms. per 100 ce. or about
55 per cent of the total non-protein nitrogen). Thus my own
observations on the fish brain closely agree with those of Wilson
and Adolph on the fish blood, so far as the relative abundance
of the non-protein nitrogen is concerned, as well as in the relation
of the amino acid nitrogen to the total non-protein nitrogen.

Denis (?13—14) found also a considerably greater amount of
non-protein nitrogen in the blood of marine fishes when con-
trasted with human blood. Denis found 62 mgms. of non-pro-
tein nitrogen per 100 ce. of blood (average of 10 species of teleosts)
and as high as 1087 mgms. in the case of the elasmobranchs
(average of three species). Thus the greater abundance of the
non-protein nitrogen in the fish blood, accompanied by a slow
circulation, might be largely responsible for a greater accumu-

lation of the non-protein nitrogenous extractive substances in
the fish brain.

SUMMARY

The gray snapper, Neomaenis griseus, was mainly used for
the present investigation. The following are the more impor-
tant facts brought out.

1. The relation between brain weight and body length is prac-
tically linear. This linear relation appears in the fish as small
as 150 mm. in length. The fish smaller than 150 mm. were not
studied because they could not be obtained.

2. The percentage of water in the brain varies very little from
small to large (body length : 88 mm. to 448 mm.). <A similar
relation was observed by Donaldson (’05) in the brain of the
summer flounder and by Scott (712) in the brain of the smooth
dogfish. The probable explanation is that the process of mye-

58 SHINKISHI HATAI

lination is completed in the fish brain relatively earlier than in
the mammalian brain.

3. With respect to the total nitrogen, nitrogen in ether-alco-
hol extract, and the lipoid content, the fish brain closely resembles
the stem of the rat brain, but significantly differs from the entire
rat brain. This is explained by the fact that the mature fish
brain resembles essentially the stem of the mammalian brain
owing to the small growth of cerebrum and cerebellum.

4. The non-protein nitrogen is considerably greater (42 per
cent) in amount in the fish brain than in the rat brain. The
suggestions were made that probably on account of unstable
physical consistence of the fish nervous system, the wear and tear
of the neurons may be greater than in the more highly organized
mammalian nervous system, thus producing a larger quantity
of the waste products, and also that on account of higher non-
protein nitrogen content of the fish blood, accompanied by a
slow circulation, the deposition of the waste products might
become greater, and at the same time a less vigorous removal
further tends to increase the accumulation. .

5. The greater fraction of the non-protein nitrogen is repre-
sented by the amino acid nitrogen in both the fish and the-rat.

6. The amounts of urea nitrogen and of ammonia nitrogen
are closely similar to those found in the rat brain,

METABOLIC ACTIVITY OF NERVOUS SYSTEM 59

LITERATURE CITED

Brzouip, A. von 1857 Untersuchungen iiber die Vertheilung von Wasser, or-
ganischer Materie und anorganischen Verbindungen im Thierreiche.
Zeitschr. f. wiss. Zool., vol. 8.

Brpra, Ernest von 1854 Vergleichende Untersuchungen iiber das Gehirn
des Menschen und der Wirbelthiere. Verlag von Basserman u. Mathy.
Mannheim.

Denis, W. 1913-1914 Metabolism studies on cold-blooded animals. 2, The
blood and urine of fish. J. Biol. Chem., vol. 16, pp. 389-393.

~ Donaupson, H.H. 1905 On the percentage of water in the brain of the summer
flounder, according to body weight. Not published—in manuscript.
1909 On the relation of the body length to the body weight and to
the weight of the brain and of the spinal cord in the albino rat (Mus
norvegicus var. albus). Jour. Comp. Neur., vol. 19, pp. 155-167.
1915 The Rat. Reference tables and data for the albino rat (Mus
norvegicus albinus) and the Norway rat (Mus norvegicus). Memoirs
of the Wistar Institute of Anatomy and Biology, no. 6.

1916 A preliminary determination of the part played by myelin in
reducing the water content of the mammalian nervous system (albino
rat). Jour. Comp. Neur., vol. 26, pp. 443-451.

Fourn, Orro anp Denis, W. 1914 On the creatinine and creatine content of
blood. Jour. Biol. Chem., vol. 17, pp. 487-491.

Harar, 8S. 1909 Note on the formulas used for calculating the weight of the
brain in the albino rats. Jour. Comp. Neur., vol. 19, pp. 169-173.
1917 Metabolic activity of the nervous system. I. Amount of non-
protein nitrogen in the central nervous system of the normal albino
rat. Jour. Comp..Neur., vol. 28, pp. 361-378.

~ Keuuicort, W. E. 1908 The growth of the brain and viscera in the smooth
dogfish (Mustelus canis, Mitchill). Am. Jour. Anat., vol. 8, pp.
319-353.

REIGHARD, J. 1908 An experimental field study of warning coloration in coral
reef fishes. Papers from the Tortugas Laboratory, Carnegie Inst.
Washington, vol. 2.

ScHLossBERGER, J. E. 1856 Allegemeinen und vergleichenden Thierchemie.
Leipzig u. Heidelberg.

Scorr, G.G. 1912 The percentage of water in the brain of the dogfish. Proc.
Soc. Exp. Biol. and Med., vol. 9, no. 3.

Witson, D. W. anp Avotpnu, E. F. 1917 The partition of non-protein nitrogen
in the blood of fresh water fish. Jour. Biol. Chem., vol. 29, pp. 405-
411.

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AUTHOR'S ABSTRACT OF THIS PAPER ISSUED
BY THE BIBLIOGRAPHIC SERVICE, FEBRUARY 2

COMPARATIVE STUDIES ON THE GROWTH OF THE
CEREBRAL CORTEX

V. PART I. ON THE AREA OF THE CORTEX AND ON THE NUMBER
OF CELLS IN A UNIT VOLUME, MEASURED ON THE FRONTAL
AND SAGITTAL SECTIONS OF THE ALBINO RAT BRAIN, TOGETHER
WITH THE CHANGES IN THESE CHARACTERS ACCORDING TO THE
GROWTH OF THE BRAIN

V. PART II. ON THE AREA OF THE CORTEX AND ON THE NUMBER
OF CELLS IN A UNIT VOLUME, MEASURED ON THE FRONTAL
AND SAGITTAL SECTIONS OF THE BRAIN OF THE NORWAY RAT
(MUS NORVEGICUS), COMPARED WITH THE CORRESPONDING DATA
FOR THE ALBINO RAT

NAOKI SUGITA
From the Wistar Institute of Anatomy and Biology

THREE FIGURES AND FOUR CHARTS

PART I
I. INTRODUCTION

The present study is an extension of an earlier one on the
thickness of the cerebral cortex in the albino rat (Sugita, ’17 a)
and aims to present the extent of the actual area occupied by
the cortical cells, as seen in sections which were taken from
the fixed levels of the albino brain, and also to follow the
changes in this area during the postnatal growth of the brain.
In the course of this investigation, the number of nerve cells
contained in a unit volume of a fixed locality in the frontal)
section was counted and the changes in this number with ad-
vancing age were ascertained. Furthermore the relation be-
tween the cell number and the cortical area was critically
examined.

For this study, the sections, which had been previously used
for the investigation of the thickness of the cortex of the albino
rat brain, were again utilized. The material, amounting to 78

61

THE JOURNAL OF COMPARATIVE NEUROLOGY, VOL. 29, NO. 2
APRIL, 1918

62 NAOKI SUGITA

albino rats, sexes combined, which was used in the present study,
is identical with that listed in table 1 of the former paper (Sugita,
"17 a), to which the reference should be made for this study
also.
These studies were made during the winter semester of 1916-
1917.
II. MEASUREMENTS AND ENUMERATIONS

A. Area of the cortex in the sagittal section

As previously described (Sugita, ’17 a), the sagittal section
(fig. 1) was taken in a plane passing through the frontal pole
and parallel to the mesial surface of the hemisphere. This
section from each individual brain was projected on a sheet of
paper by the Leitz-Edinger Projection apparatus, at a magnifi-
cation of exactly twenty diameters, and the outline of the image
then accurately traced on the sheet. At the transitional part
of the cortex at the frontal pole to the olfactory bulb and at the
subiculum, where the cortex goes over into the structure of the
cornu Ammonis, the borderlines were drawn along the radiation
of the cells in those parts (fig. 1). The anterior borderline
(a-a’) is formed by a prolongation of the line bounding the dorsal
surface of the olfactory bulb. The posterior borderline (p—p’)
is ¢learly located, because this was drawn at the point where
the thickness of the ganglionic layer abruptly diminishes at the
beginning of the ganglion cell band characteristic for the cornu
Ammonis. The area of the cortex, including the lamina zonalis,
which contains no proper nerve cells, was then repeatedly
measured to a square millimeter on the drawing, using the Ott
Compensating Planimeter. The values obtained were then
averaged, and 1/400 of the value, which corresponds to the
cortical area on the slide, was recorded. This value was then
converted into that for the fresh condition of the material, by
the following procedure.

On the outline, which was taken from the section on the slide,
the diameter from frontal pole to the occipital pole (LZ. F) was
measured and reduced, and, according to the formula given in
the former paper (Sugita, 717 a), which reads

GROWTH OF THE CEREBRAL CORTEX 63

The diameter L. F in fresh cerebrum

The diameter L. F' on the slide
the correction-coefficient was determined. The value for the
area obtained by the (first) direct measurement from the slide
was then corrected to the corresponding value for the fresh
condition of the material, by multiplying by the square of the
correction-coefficient. The corrected values thus obtained are
given in the last column of table 1.

The values for the cortical areas in the respective sagittal
sections of each individual were then grouped according to the

Correction-coefficient =

Fig. 1 Showing, by shading, the cortical area measured on the sagittal sec-
tion of the albino rat brain. The anterior borderline ((a—a’) is formed by a pro-
longation of the line bounding the dorsal surface of the olfactory bulb. The
posterior borderline (p—p’) is drawn at the point where the ganglionic layer goes
over abruptly to the ganglion cell band in the cornu Ammonis.

brain weight, into twenty groups, as in the other studies of this
series, and the average value for each group wasfound. The aver-
age areas of the cortex in the sagittal section for each group
(table 1) were plotted in chart 1 (graph s), which shows the in-
crease in area according to the increase in brain weight.

B. Area of the cortex in the frontal section

The frontal section (fig. 2) was cut in the plane passing through
approximately the middle point of the mesial surface of the

64 NAOKI SUGITA

TABLE 1

Showing the observed and corrected values of the area of the cerebral cortex in the
sagittal section of the albino rat brain, accompanied by the data for the correction-
coefficient in the individual cases and the correction-coefficient for the group.
L. F is the longitudinal diameter of the cerebrum

ae CORRECTION-COEFFICIENT Oa atan
GROUP BRAIN WEIGHT AREA SS See Ee AREA
OF CORTEX L. F in fresh The same on OF CORTEX
: brain slide
grams mm .2 mm. mm. mm .2
Ea 0.1538 3.2 5.50 4.97 4.1
c 0.154 Bn 0) 5.60 4.80 4.1
b 0.177 4.0 5.70 5.138 4.9
0.161 Bodh iho dkee 4.4
Ila 0.213 4.0 5.80 5.13 oll
b 0.221 3.9 6.00 5.43 4.8
c 0.261 4.8 6.60 5.60 Gad
d 0.271 4.8 6.75 5.80 6.5
e 0.288 4.5 6.70 5.79 6.1
- (Birth) 0.251 4.4 TERUG 5.8
III a 0.311 6.1 7.39 6.45 7.9
b 0.322 6.3 7.20 6.40 8.0
g 0.374 8.1 7.40 7.40 8.1
Cc 0.390 Bt 7.50 6.70 8.4
i 0.395 7.4 7.95 7.20 9.0
0.358 (58) ple Oz 8.3
IV b 0.400 (57h Het) 6.65 9.0
a 0.402 8.4 eto 7.30 9.4
c 0.420 Sez 7.95 7.20 10.0
i 0.443 - 10.6 8.30 8.10 Ibe
d 0.459 8.8 8.05 7.60 9.9
e 0.466 9.6 8.40 7.80 ial
0.432 8.6 1.08? 10.1
Vi 0.501 10.2 8.35 7.90 11.4
a 0.525 WAC 8.55 8.45 12.9
b 0.528 ied 8.50 8.05 12.4
Cc 0.534 9.0 8.65 7.60 11.6
d 0.537 10.1 8.30 7.70 Le
e 0.555 12.3 9.25 8.65 14.0
f 0.558 11.0 9.20 8.50 12.9
g 0.564 11.4 8.85 8.40 AEG
h 0.579 ES 9.10 8.35 13.6
0.542 11.0 1 072 12.6

GROWTH OF THE CEREBRAL CORTEX

TABLE 1—Continued

CORRECTION-COEFFICIENT

OBSERVED CORRECTED
GROUP BRAIN WEIGHT AREA AREA
OF CORTEX L. F in fresh The sameon OF CORTEX
brain slide

grams mm .* mm. iJ mm. mm.2

Vive 0.610 12.0 9.35 8.35 14.9

a 0.617 10.7 9.25 7.95 14.4
e 0.690 15.0 9.60 9.00 leans
0.639 12.6 iii 15.5

Vila 0.740 is), 2 10.50 9.80 18.1
b 0.760 IDS 10.65 8.50 Sra
0.750 IUDSAD tee Hii

VIII a 0.800 14.4 10.50 9.25 18.5
h 0.805 13.8 10.90 9.20 19.4

b- 0.822 16.2 10.45 9.60 1G=2

Cc 0.849 18.0 10.50 9.70 Alot

k 0.870 15.1 10.95 9.40 20.5

d 0.898 730 11.45 10.15 21.6
0.841 15.8 i Ge 20.1

Ix d 0.959 17.9 11.60 10.50 21.8

e 0.960 16.9 11.40 9.85 2259

a 0.972 15.4 11.30 9.70 20.9

(10 days) 0.964 16.7 Hele ENE
xX a 1.033 13.9 11.90 9.40 DOES

b 1.036 15.9 11.85 9.85 Deval

e 1.051 io 12.05 10.05 25.0
1.040 15.8 1.22 23.8

XI a OM Nise 2.00 10.00 Zea
b 1.189 18.8 50 10.25 28.0

Cc 1.193 19.1 65 10.50 2128

d 1.195 16.0 2.60 10.00 25.4

(20 days) rpg 17a8 1.22 26.6
“XII ¢ 1.234 18.4 12.30 10.35 26.0
a 1.2738 lye 7/ 2.45 9.65 26.2
1.253 HGf il 1.247 26.1

XIII a 1.301 18.7 13.00 11.10 20
g 1.307 15.6 12.95 10.00 26.2

b 1.327 17.2 13.20 10.50 2i.2

c 1.346 17.8 13.00 10.10 29.5

h 1.392 21.9 13.45 11.60 29.5

il YD) 18.2 1.23? Ry Ao

66 NAOKI SUGITA

TABLE 1—Concluded

SuakewES CORRECTION-COEFFICIENT GonnEcrEn
GROUP BRAIN WEIGHT AREA es En AC AREA
CORTEX L. F in fresh The same on OF CORTEX
brain slide
grams, mm.2 mm. mm. mm.2
XIV a 1.412 UP 13.40 10.40 29.1
e 1.441 15.2 13.25 10.10 26.2
b 1.483 21.1 13.30 11.30 29.3
1.445 17.9 1.26 28.2
XV a 1.530 17.4 13.70 10.80 28.1
b 1.542 19.6 13.50 11.40 27.5
c 1.552 1572 13.70 10.65 28.6
d 1.5738 20.0 13.70 11.15 30.1
e 1.574 18.9 13.75 11.05 29.3
1.554 18.6 1.242 28.7
XVI a 1.642 18.9 14.10 11.30 29.4
g 1.643 18.7 14.65 11.60 29.7
c 1.647 18.7 13.75 11.05 29.0
e 1.690 eo 13.65 10.70 28.6
1.656 18.4 1.26? 29.2
XVII f 1.720 18.3 14.90 11.60 30.2
a 12721 18.4 13.90 10.90 29.8
b 1.730 23.5 13.85 70 32.8
c 1.731 20.8 14.30 11.60 SHES Z/
1.726 20.2 1.22 31.1
XVIII ec 1.817 18.5 15.20 11.50 32.4
a 1.844 24.7 14.00 12.10 33.0
e 1.855 21.6 15.05 12.15 33.1
1.839 21.6 1.22 32.8
XIX a 1.924 20.6 15.40 12.30 32.3
1.924 20.6 1.25 82.3
xX a 2.039 22.6 15.10 12.60 32.5
b 2.069 745). 1L 15.55 13.20 34.8
2.054 23.9 92 33.7

hemisphere and cutting the corpus callosum, the commissura
anterior and the chiasma opticum (Sugita, ’17 a). On the draw-
ing of the outline of the frontal section (fig. 2), which was traced

GROWTH OF THE CEREBRAL CORTEX 67

in the same manner as that for the sagittal section, the dorsal
and the ventral borderlines of the cortical areg were drawn.
The dorsal border (d) was determined by the ectal borderline
of the corpus callosum, which lies under the tip of the cortex
at the bottom of the fissura sagittalis, and the ventral border
(v-v’) was drawn perpendicular to the surface at the basal end
of the cell group which is found under the cortex proper just
below the region of the fissura rhinalis, latero-basal to the cap-

Fig. 2 Showing, by shading, the cortical area measured on the frontal sec-
tion of the albino rat brain. The dorsal border (d) is chosen at the borderline
of the corpus callosum. The ventral border (v-v’) was drawn perpendicular
to the surface at the basal end of the cell group found near the fissura rhinalis,
latero-basal to the capsula externa. The double shaded part, locality VII,
indicates the area where the cell number and cell size were determined.

sula externa. This latter border is not so sharply defined, but
we could not find any better marking point than this cell group.
The area of the cortex, thus bounded, was then measured and
recorded. In making the measurement, the area of the cortex
was at first measured and then the total area of the frontal sec-
tion,—of one hemicerebrum—excluding the cavity of the lateral
ventricle and the tractus opticus, was measured. The ratio
of the cortical area to the total area of the section was then
computed. Correction of the observed values to those for the

68 . NAOKI SUGITA

fresh condition of the material was made in the same manner
as for the sagittal cortex, by multiplying by the square of the
value of the correction-coefficient. This latter was obtained
by the formula given in a former paper (Sugita, ’17 a), as follows:
The diameter W. D in fresh cerebrum

The diameter W.D on the slide

Correction-¢oeffiicient =

mm.2
75 == 1 | ]
| sae
65+ | a J | sues |
: yas
a lee nea
55 1 = lee | |
50 Won iSes eras
LAE wi |
45) =, 4 Baie |
poe ] |
| aa | |

E
| »| |
| | ions a eae |
| Rieeae in
2 eae ee | : 7 : =
5} ] at Se + lee eee |
| | sae | | ;
A =
“a | me iin Sete = =f
| | Pat } Bee :
| be pee Lae | | | | | | |
Ss | Ls | |
he |_ 7 ) |
; i | | |
an | ba 2a = aa aes) | cae —= a
SE | |
| ¥ = | | |
A Be coal: sol jes | |
/ | | | | | | | | | |
| ; | | | | |

|
| {ese | | | |
0 Of 02 03 04 05 06 O7 08 O9 10 ff, 12 13 4 15 16 47 18 19 20 gns

Chart 1 Showing the corrected areas of the cerebral cortex in the sagittal
and the frontal sections and the area of the whole frontal section, all according
to the brain weight, accompanied by the theoretical value of the last which is
assumed to be proportional to the square of the cube root of the brain weight.
Albino rat. X—.—.—- X, Cortical area in the sagittal section. © oof
Cortical area in the frontal section. ° ef, Area of the whole frontal section.
-------- T, Theoretical area of the frontal section, i.e., the square of the
cube root of the brain weight. All graphs are based on the data in tables 1
and 2.

These data are all entered in table 2, in which the average
measurements for each brain weight group are also given. The
graphs for the total area of the frontal section (graph F) and
for the area of the frontal cortex (graph f) in chart 1 are based
on the corrected data given in table 2.

TABLE 2

Showing the observed and corrected values of the area of the cerebral cortex and of
the total frontal section and the percentage of the cortical area to the total frontal
section of the albino rat brain, accompanied by the data for the correction-coeffi-
cient in the individual cases and the correction-coefficient for the group. W. D
ts the frontal diameter of the cerebrum

GROUP

lo)

Ila

b

c

d

e
(Birth)

Illa
b

g
Cc
1

“IVb

OBSERVED

BRAIN
WEIGHT rentat
ete: Oe
grams mm.? mm.2
0.153 2.8 9.2
0.154] 2.6 8.2
0.177 3.5 9.9
0.161 3.0 Sl,
0.213 4.4 13.0
0.221 3.6 11.9
0.261 4.6 13.0
0.271 4.4,{ 138.1
0.288 4.1 11.8
0.251 4.2 12.6
Orsi 5.1 15.3
0.322 5.1 13.0
0.374 Mees 19.0
0.390 6.5 15.9
0.395 7.5 17.8
0.358 6.3 16.2
0.400 als) 19.4
0.402 6.8 UG 37/
0.420 6.7 17.9
0.448 8.0 19.0
0.459 6.9 17.2
0.466 9.4 21.8
0.432 TG 18.7
0.501 9.0 22.3
0.525 9.8 22.4
0.528 8.7 19.6
0.534 7.6 18.6
0.537 8.8 20.1
0.555 9.9 22.5
0.558 9.2 20.0
0.564 10.2 22.9
0.579 10.1 221
0.542 9.3 421.2

‘CORFFICIENT CORRECTED
W.D Area of
in fresh | "oy side | of cortex | total
mm. mm. mm.2 mm .2
6.45| 5.65| 3.7 | 12.0
6.35| 5.40| 3.6 | 11.4
6.95| 6.26] 43 | 12.2
Bae 3.9 | 11.9
g.40| 7.35| 5.7 | 17.0
7.95| 6.50| 5.4 | 17.8
780) 7.10-|) aes 18.7
7.75| 6.80| 5.7 | 16.9
8.55| 7.05| 6.0 | 17.4
1.162 5.7 | 17.0
8.50| 7.65] 63 | 18.9
8.70| 6.80| 8.3 | 21.2
8.95| 8.40] 8.2 | 21.6
8.85| 7.60| 88 | 21.5
9.10] 8.60} 8.4 | 20.0
1.18% 8.0 | 20.6
9.00| 8.50] 8.5 | 21.7
9.10| 7.90) 9.0 | 22.2
9.00) 815| 82 | 21.8
9.15| 8.40/ 9.4 | 223
9.50 7.95|. 9.8 | 24.5
9.30| 9.25] 9.5 | 221
1.10: 9.1 | 28.4
9.80| 9.20] 10.2 | 25.3
9.65/ 9.10] 11.0 | 25.2
9.90] 8.60) 11.5 | 26.0
10.30] 8.25] 11.4 | 29.0
10.00] 8.80] 11.4 | 26.0
9.90 9.00] 12.0 | 27.2
10.00| 8.55] 12.6 | 27.4
10.10 9.15} 12.4 | 28.0
10.10} 9.05] 12.8 | 27.6
1.182 11.7 | 26.9

69

PERCENT-

AGE OF

CORTICAL
AREA IN

TOTAL

° SECTION

per cent

34
34
30
35

GROUP

BRAIN
WEIGHT

TABLE 2—Continued

Ixd

(10 days)

XGA:

(20 days)

XIle

RO a
—_
ie)
(JC)

grams

0.610
0.617
0.690
0.639

_
bo
(se)
—

~
SS)
qn
cs

ae a
co
bo
N

OBSERVED eee CORRECTED

Area of W.D Area of

Nea fol eek Bak Erde: ofepee a
mm 2 mm.2 mm. mm. mm.2 mm.2
9.9 21 10.15 8.50 14.1 31.0
9.6 216 10.55 8.65 14.3 32.2
11.6 23.0 10.60 9.40 14.8 30.2
10.4 22.3 1.1? 14.4 31.1
itd 22.1 11.00 9.20 15.9 31.6
10.2 20.3 11.20 8.70 16.9 33.6
10.7 21.2 He 16.4 82.6
10.6 21.8 11.15 8.60} 18.8 36.7
11.3 23.6 10.60 8.30 18.5 38.6
13.6 28.5 11.85 10.20 18.4 38.5
13360 28.8 11.40 9.90 18.2 38.3
13.4 Plath 11.45 9.60 19.1 39.5
13.1 31.2 11.75 10.20 17.4 41.5
12:6 26.9 1.20? 18.4 88.9
13.5 28.4 11.80 9.70 | 20.0 42.0
13.8 29.4 12.15 10.10 | 20.0 42.6
14.3 28.4 11.95 9.80 | 21.3 42.4
13.9 28.7 eee 20.4 42.8
14.1 30.3 12.40 10.30 | 20.4 44.0
13.4 30.5 12.40 TOM ay \ee2020 45.5
13.2 25.9 12.10 9.40 | 21.8 43.0
LB6 28.9 1k Yos 20.7 44.2
135.57 28.7 12.90 10R2Z05| Me21e8 45.7
13.3 27.8 13.15 ORSON |e zled, 45.4
14.6 30.8 12.70 102308 e2262 47.0
12.8 27.2 12.50 9.80 | 21.0 44.5
HB) 28.6 1.26 21.7 45.7
15.0 SLA9 12.95 10.70 | 22.0 46.8
1S) 23.6 12.90 9.10 | 24.0 47.5
13.5 27.8 Th oe 23.0 47.2
13.9 28.3 13.20 1OF259) 230 47.1
13.9 29.9 12.70 10.00 | 22.5 48.3
12.2 28.2 13.35 9.70 | 238.2 53.3
13.3 29.0 13.15 9°85 || 23.7 51.8
16.3 34.8 13.10 10.90 | 23.6 50.3
13.9 30.0 1.292 Qane a \ nro ee,

70

PERCENT-
AGE OF
CORTICAL
AREA IN
TOTAL
SECTION

per cent
46
44
49
46

TABLE 2—Concluded

GROUP

XVIII ¢

BRAIN
WEIGHT

OBSERVED

CORRECTI

ON-

COEFFICIENT

CORRECTED

PERCENT-
AGE OF
CORTICAL

Area of W.D.« Nreaiof |p eern

ofeortex | total | imfresh |“crsitde | of cortex | £02! | sncnow

grams mm 2 mm. mm. mm. mm.? mm 2 per cent
1.412 | 13.9 29.4 13.65 | 10.30 | 24.4 51.6 47
1.441 | 12.4 25.7 13.10 9.20 | 25.2 51.0 49
1.483 | 15.2 33.3 13.80 | 10.80 | 24.8 54.4 46
1.445 13.8 29.5 1.387 24.8 62.3 47
1.530 | 14.4 33.6 13.80 | 10.80) 23.5 54.8 43
1.542 | 13.9 30.5 13.70 | 10.40 | 24.2 53.0 46
1.552 |} 14.2 31.7 13.50 | 10.30 | 24.4 54.4 45
1.573 | 14.2 30.8 13.90 | 10.60 | 24.4 53.1 46
1.574 | 14.8 32.2 13.70 | 10.50 | 25.2 54.8 46
1.554 | 14.8 31.8 1.30? 24.8 54.0 46
1.642 | 16.4 37.0 13.80 | 11.20 | 24.9 56.2 44
1.643 | 11.6 27.4 13.40 9.50 | 23.2 54.7 42
1.647 | 14.3 29.8 14.00 | 10.50) 25.5 53.2 48
1.690 | 13.0 30.7 13.45 10.00 | 23.5 55.3 42
G56) 1828 | 181-2 1.332 OE 3 | 54.9 4h
1720) | 1259 28.7 13.50 9.60 | 24.8 56.8 44
1.721 | 14.8 34.5 14.00 | 11.00} 24.0 56.0 43
PefsOn| Lib 40.4 14.70 | 12.385 | 24.8 57.2 43
Wo Gel |) I/o® 39.2 14.40 | 12.10] 24.8 55.6 45
127261) 15.6" |" 85.7 1.262 24.6 | 56.4 4h
ISS lass 31.1 14.00 | 10.10} 25.6 59.8 43
1.844 | 17.4 38.1 15.00 | 12.10 | 26.7 58.5 46
1.855 | 14.2 32.0 14.30 | 10.60] 25.8 58.3 44
1.839 15.0 83.7 1.32? 26.0 58.9 44
1.924 | 14.8 33.9 14.10 | 10.90} 24.8 57.0 44
1.924 | 14.8 83.9 1.292 24.8 67.0 4h
POST 1Gr 8 4207. ARSON 127100) 25.2 63.9 39
ZROGQE Mond 40.3 14.60 | 11.70} 24.5 62.8 39
2.054 | 16.8 41.6 1 oer 24.9 63.4 39

C. Number of nerve cells

On the frontal sections used for the measurement of the cor-
tical area, the number of nerve cells contained in a unit volume
at a fixed locality in the cortex was counted. The locality
selected was at the middle part of the cortical band (fig. 2, VII),
designated as locality VII in figure 4 in a former paper (Sugita,

71

2 NAOKI SUGITA

"17 a). To represent the cortex, the lamina pyramidalis and the
lamina ganglionaris were selected. By the use of the ocular
net-micrometer (with Zeiss Comp. Ocular 6 and Zeiss objec-
tives 2 mm. and 4 mm.), the number of nerve cells in five ad-
joining squares along the cortical band, each square 100 micra
on a side, was counted in a given location. The numbers ob-
tained were added together and then, by multiplying by two,
was converted to the number in a unit area of 0.1 mm.? on the
section. This value, the number of nerve cells in a slice of cor-
tex, 0.1 mm.? in area and 10 micra thick (the thickness of the
section) or 0.001 mm.* in volume, was then reduced to the number
in this volume in the fresh condition of the brain. To make
this reduction, I used as the correction-coefficient the cube of
the reciprocal of the correction-coefficient obtained by the for-

at iameter W.D i S ;
ane ne diameter in fresh cerebrum a a a

The diameter W.D on the slide

previously employed, because the section on the slide was as-
sumed to have shrunken in all three dimensions equally at the
rate of the correction-coefficient and therefore a unit volume
in the fresh condition would correspond to the volume of the
unit on the slide multiplied by the cube of the reciprocal of the
correction-coefficient.

In the lamina pyramidalis, the pyramids are more densely
crowded at the ectal than at the ental part of the layér, which
adjoins the lamina granularis interna. I adjusted the upper
line of the net-micrometer squarely on the border between the
lamina zonalis and the lamina pyramidalis and counted the cell
number included in a square, 100 micra on each side, at the ectal
part of the layer, where the cells are crowded densely. If large
blood vessels appeared in the microscopic field, I gave up such
a field and counted an adjoining one where no large vessels
were present.

In the lamina ganglionaris the large ganglion cells are mixed
with a number of small pyramids, almost equal in size to, or
somewhat smaller than, the pyramids in the lamina pyramidalis.
At first, the number of all the nerve cells, the large and small
combined, was counted. Then the large ganglion cells, which

GROWTH OF THE CEREBRAL CORTEX 73

surely represent a group distinct from the small pyramids, were
counted alone. So, by subtraction, the number of small pyra-
mids only in the lamina ganglionaris was obtained. In counting
the ganglion cells, I adjusted the lower line on the net-microme-
ter accurately on the border between the lamina ganglionaris and
the lamina multiformis, because between the lamina ganglionaris
and the lamina granularis interna there is found a pale band
poor in cells and therefore it was not convenient to adjust the
upper line of the net-micrometer at this border. The number
of cells observed, in a slice of 0.1 mm.? in area and 10 micra
thick on the slide,’ were in the similar manner recorded and
by the use of the same correction-coefficients, as were used
in the case of the pyramidal cells, were reduced to the number
for the fresh condition of the brain.

Out of the total number of cells, which came in view in the
microscopic field, about one-third does not contain the nucleoli
in the cell nuclei. This means that the nucleoli in question lie
outside of the section. Nevertheless I counted the cells having
nuclei without nucleoli together with those in which nucleoli
were to be seen, because my object was to ascertain the cell
density in the locality chosen and not to determine the total
number of nerve cells in a series of sections. In the latter case,
the double counting of one and the same cell must be necessarily
avoided. On the other hand, the cells which were represented
in the section by only fractions of the cell bodies without nuclei
were omitted from the counting. The number of such cells
was small. Neuroglia nuclei, which were to be easily distin-
guished by their smaller size, and the intima cells of the capil-
laries, if they came in view, were not counted.

Table 3 shows the results of these enumerations.

III. DISCUSSION
D, The area of the cortex in the sagittal section

Examining table 1 and chart 1 (graph s), which give the area
of the cortex in the sagittal sections of the albino rat brain, it is
seen that the area increases steadily with increasing brain weight.

TABLE 3

Giving for each individual and for each brain weight group the number of nerve
cells in 0.001 mm.’ in volume of the cortex, in the lamina pyramidalis and in the
lamina ganglionaris, and also the number of the ganglion cells in the lamina
ganglionaris, all counted at the middle part of the cortex in the frontal section, as
shown in figure 2. Albino rat

eee oy NUMBER OF CELLS IN A VOLUME OF CORTEX, 0.001 mm.3
GEour seen W.D ees Lam. pyramid. Lam. ganglion. Serene in
in fresh enalide
brain Ob- Cor- Ob-_ | Cor- Ob- Cor-
served | rected served | rected served rected
grams mm. mm.
la | O2153 6.45 5.65 1150 775
e | 0.154 6.35 5.40 1130 695
lo |} Oa ie/7/ 6.95 6.26 945 690
0.161 (GUAT ANE 1075 720
IIa | 0.218 8.40 Goo 830 556 370 248 91 61
le OE22l 7.95 6.50 930 509 393 215 114 62
e | 0.261 7.80 7.10 735 554 322 242 104 78
ol |) e771 Calo, 6.80 726 490 358 242 114 Wil
e | 0.288 8.55 7.05 715 402 424 238 120 67
(Birth) 0.251 (GUAL MD) 787 502 373 237 109 69
IUO8 |) Ose 8.50 7.65 625 456 330 241 112 82
b | 0.3822 8.70 6.80 730 348 415 198 122 58
g | 0.374 8.95 8.40 504 417 270 223 98 82
e | 0.3890 8.85 7.60 493 312 312 197 104 66
1 | 0.395 9.10 8.60 401 337 262 220 90 76
0.358 (GUL ISI) 561 374 318 216 105 ei
IV b | 0.400 9.00 8.50 410 345 258 217 94 79
a | 0.402 9.10 7.90 473 309 267 175 95 62
e | 0.420 9.00 8.15 451 334 240 178 74 55
1 | 0.443 9.15 8.40 424 327 22 176 ds 56
d | 0.459 9.50 7.95 440 258 250 146 77 45
e | 0.466 9.30 9.25 355 348 186 182 59 58
0.482 (GAL MO)? 426 3820 238 Gy) 79 59
ON a0 5019-80) | 9320) | "371 sr 199 165 69 57
a 08529 9.65 9.10 362 303 183 154 67 56
b | 0.528 9.90 8.60 365 240 205 134 al ol
ec | 0.534 | 10.30 8.25 432 222 228 117 78 40
d | 0.537 | 10.00 8.80 412 281 210 1438 al 48
e | 0.555 9.90 9.00 368 277 164 123 62 47

TABLE 3—Continued

CORRECTION-

(o) x, 3
SOMITE NUMBER OF CELLS IN A VOLUME OF CORTEX, 0.001 mm

BRAIN 4 i i
CIDE WEIGHT] w p Lam. pyramid. Lam. ganglion. Soren in
ie W.D . gang].
seetely nde | ——-————
al Ob- Cor- Ob- Cor- Ob- Cor-

served | rected served | rected | served | rected

grams mm. mm.

Vf | 0.558 | 10.00 | 8.55 357 | 223 182 114 79 49
0.564 | 10.10 | 9.15 326 | 242 178 132 62 46

g

h | 0.579 | 10.10} 9.05| 318] 229 | 194 | 140 64 46
0.542) (1/1.13)8 368 | 258 | 194 | 136 70 49

Vic | 0.610 | 10.15] 8.50] 325] 190 | 182 | 106 65 38
A | OLGt7 1085S. | 8865.) § 322)! A77— |) 200) | 110 60 33

e | 0.690 | 10.60} 9.40] 286} 199 | 191 | 133 58 40
0.639 | (1/1.19)3 Bilal 189) C1976 aettG 61 37

Walley POR 740) | 1100) |) 9.20") 62770) 186) || 149,16 100 48 32
b | 0.760 | 11.20] 8.70| 300} 140 | 188 88 47 22
0.750 | (1/1.24)8 289 | 163 | 169 94 48 a7

Wililiea | OL8008 1115.1) 8.60 |) 3021) 128) |) 170 78 43 20
h | 0.805 | 10.60 | 8.30] 293] 140 | 168 80 48 23

by 0-822)| 1485.) 10.20) 266.) 170° -| 138 88 38 24

ce | 0.849 | 11.40] 9.90} 242] 158 | 140 92 37 24

k | 0.870 | 11.45 | 9.60] 257) 151 | 152 90 45 26

dy 80, 898h0 11575) 10/207 2554) 167) =| 188 90 38 25
0.841 | (1/1.20)3 269 | 154 | 161 86 42 24

IX d | 0.959 | 11.80] 9.70 | 241] 133 | 156 86 40 22
@ (02960, 12.15)| 10.10 | 2240) 130. |147 85 39 23

a 029729) 11.95. | 9.80 || 2208) 122) | 150 83 41 23

(10 days) | 0.964. | (1/1.21)3 228 | 128 | 1651 85 40 23
Xa, 0s3ei2 405 10e30yh 2230) 128) || 9153 88 45 26
bal teOsGa2- 40105.) 22a) 1064 136 75 41 23

e | 1.051|12.10| 9.40] 244] 115 | 149 70 43 20
1.040 | (1/1.93)8 226 | 120 | 142 78 43 23
Nae LOT e290, 10-20 |) 2345 site, | 150 74 44 22
belie 189uleisets 10630 | 2298 110.) 148 “il 49 24
Cue LOS Hem2eZ0 I 1Os305|) 220 etise 144 Wa 42 23

Ge et95) ns | Ge80) | 220%eto7 |. 149" 68 44 21

(20 days) | 1.171 | (1/1.26)8 226 | 113 | 146 73 45 23
NOI Ueda 2095 10.70. = 210 WS | 136 76 48 27
aie 27Ba le oOOme toe 100ly 248ylenes7 |! a7a 60 55 | 19
1.253 | (1/1.31)8 229! 103 | 154 68 52 \ 23

TABLE 3—Concluded

paar ee NUMBER OF CELLS IN A VOLUME OF CORTEX, 0.001 mM.3

Ce OKeRY wheat WD a > Lam. pyramid. Lam. ganglion. ee in
brain’ |) = Wao Cor- Ob- Cor- Ob- Cor-

served | rected served rected served | rected

grams mim, mum.

MIMD a | 1-301 | 13.20 |} 10.25 PAP 99 177 83 56 26
g | 1.307 | 12.70 | 10.00 205 100 163 80 52 PAS
loy |! thee |) 118).8%5) 9.70 243 94 180 69 60 23
Gl 3465) isels 9.85 218 92 174 73 57 24
h | 1.392 | 18.10 |°10.90 190. 110 140 81 50 29
1.335 (/1729)3 214 99 167 7 55 25
UV ae e412 13.655) 102380 212 91 164 71 58 25
e | 1.441 | 13.10 9.20 248 86 176 61 63 De,
b | 1.483 | 13.80 | 10.80 218 105 172 82 60 29
1.445 (1/1.34)8 226 94 171 Ut 60 25
XV a | 1.580 | 13.80 | 10.80 185 88 134 64 47 23
b | 1.542) 18).70 || 10.40 207 90 144 63 49 22
@ || 1a |) TRG) || a)es%0) 183 81 152 67 52 23
d | 1.573 | 13.90 | 10.60 184 82 130 58 53 24
Cll S45 se On LONS0 204 93 134 60 52 23
1.554 GH 3O))3 193 &7 139 62 51 23
XViIa .642 | 13.80 | 11.20 170 91 2% 68 50 Zi

.643 | 13.40 | 9.50 225 81 148 53 56 20
5

lo)
oot

SP)

NS

“I

14.00 | 10.50 186 79 134 57 oo 23
e .690 | 13.45 | 10.00 207 84 148 | 61 63 26
656 (1/1.383)8 197 84 139 60 56 24
XVIL£ | 1.720 | 13.50 | 9.60 208 7o 151 o4 60 22
a -| Lo72t |) 14:00 |} 11/00 178 86 132 64 By) 27
b | 1.730,| 14.70 | 12.35 142 84 118 70 44 2
@ | 1.73l |) 14540) | 12-10 144 85 106 63 42 25
1.726 (1/1.26)8 168 83 127 63 50 25
XVIILe | 1.817 | 14.00 | 10.10 188 71 142 Bs) 54 20
a | 1.844 | 15.00 | 12.10 170 89 126 66 48 25
e | 1.855 | 14.30 | 10.60 192 78 139 57 60 24
1.839 | (1/1.32)8 183 79 136 59 54 a3
XIX a | 1.924 | 14.10 | 10.90 174 81 110 51 52 24
1.924 (1/1.29)8 174 81 110 51 52 24
XX a | 2.039 | 14.80 | 12.10 150 82 95 52 |, 38 27
b | 2.069 | 14.60 | 11.70 151 78 96 49 37 19
2.054 iy t2e8)s 151 80 96 51 38 20

76

GROWTH OF THE CEREBRAL CORTEX Tt

As already shown (Sugita, 717, 717 a), the longitudinal diameter
of the sagittal section (from the frontal pole to the occipital
pole), that is L. F, as well as the cortical thickness, are both
steadily increasing as the brain weight increases. The thickness
of the cortex is one component of its area in the section, the other
being obtained by dividing the area by the thickness, and the
length thus found is correlated with the longitudinal diameter
of the section (L.F') as defined above. The increase of the
cortical area will therefore depend on the increase in cortical
thickness and the increase in the longitudinal diameter of the
section (Z. F). Table 4 shows these relations. Column B gives
the average brain weight by groups, column C the average
corrected area of the cortex (taken from table 1), column D
the cortical thiekness (7’,) and column F the diameter L. F,
all in the fresh condition of the brain and the last two quoted from
the data already published (Sugita, ’17,’17 a). In column E is
given the ratio C/D or the computed length of the long side,
when the cortical area is reduced to a rectangle with the short
side equal to the cortical thickness. If these computed lengths are
compared with the actual longitudinal diameters of the cerebrum
(L. F), given in column F, it is of interest to note that, in brains
_ weighing more than 0.5 gram, the ratios, given in column G
as I/F, are quite similar, ranging between 1.16 and 1.25 (average
1.22).!. In the newborn or before birth (Group I), the ratio is
somewhat higher. So, if necessary, the cortical area in the
sagittal sections may be obtained by the following formula
ele SG Alo, (L. F and T,, in millimeters)

As the, sagittal cortical thickness in brains weighing more than
1.17 grams increases only slowly, the cortical area in the sagittal
section in brains older than twenty days is approximately
proportional to the longitudinal diameter of the cerebrum (L. F).

E. The area of the cortexin the frontal section

Reviewing table 2 and chart 1 (graph f), we see that the
cortical area in the frontal section increases in the same manner

1 In making comparisons with the Norway rat in part II of this paper, the
average ratio given by Groups XIII to XX will be that used. This average
ns) dale

THE JOURNAL OF COMPARATIVE NEUROLOGY, VOL. 29, NO. 2

78 NAOKI SUGITA

TABLE 4

Showing the relations of the cortical area in the sagittal section to the longitudinal
diameter (L. F) of the cerebrum and the cortical thickness. All values for the
fresh condition. Albino rat.

A B (@; D E F G
ae sna | “amc” |e] co | |
WEIGHT ghee SAGITTAL D BRAIN
grams mm.2 mm. mm. mm.

I 0.161 4.4 0.52 8.5 5.6 152
II (birth) 0.251 5.8 0.67 8.7 6.4 1.36
III 0.358 8.3 0.90 9.2 7.4 1.24
IV 0.432 10.1 0.99 10.2 8.0 eZ
V 0.542 12.6 1.14 iil (0) 8.9 1.24
VI 0.639 15.5 1.29 12.0 9.6 1.25
NEE 0.750 Seal 1.43 12a 10.4 22
VIII 0.841 20.1 1.48 13.6 11.0 124
IX (10 days) 0.964 Diller 155 14.0 1G 11 Pil
xX 1.040 Dame 1.59 14.8 12.0 LoS
XI (20 days) eval 26.6 eae, 15) .0) 125} 1.24
xem e253 Aol Yi is 14.9 12.8 1.16
XIII 1335 27.6 ee 16.0 1 1228
XIV 1.445 3 2 1.70 16.6 13.3 e25
XV 1.554 PrS\ 57h 1.76 16e3 13330 1.19
XVI 1.656 29.2 1 77 16.5 ital iL ey
XVII 1.726 Bille 1.79 17.4 14.3 122,
XVIII 1.839 32.8 1.86 17.6 14.7 1.20
XIX 1.924 37-83 1.80 17.9 15.0 1.19
XX 2.054 883.7 1.80 18.7 16) .8 eae
AVera ce: (GroupsaVvi— ro)! ha Pac alo cores cise ean ene Occ eee 1.22
Average. (GroupsecllI—XX)!* ROME oo. Solis coke stein» se see if

as in the sagittal section though more slowly. The cortical area
in the frontal section is a product of the cortical thickness (T’,)
and the length of the cortex along the cerebral surface. This
surface line of the cortex in the frontal section may be regarded
as a part of a circle and its length may be taken as propor-
tional to the length of the radius or the measurement W. D (the
frontal diameter of the cerebrum), which was measured across
the section horizontally (Sugita, 717). As shown in table 5,

GROWTH OF THE CEREBRAL CORTEX 79

which is comparable with table 4, the relative value C/D or
Cortical area

Cortical thickness

calculated. The ratio, given in column G, table 5, falls between
0.85 and 0.99 (average 0.91)? in brains weighing more than 0.5
gram, but shows a tendency to gradually increase as the brain
weight increases. In the newborn or before birth (Group I)
it is somewhat higher. If the average ratio be taken as usable
for all groups, as in the case of the sagittal section, the cortical
area in the frontal section may be approximately obtained by
the following formula:

W.D xT, X 0.91 (W.D and T., in millimeters)

As, in brains weighing more than 0.95 gram, the cortical thick-
ness in the frontal section (7’,) varies only slightly, the cortical
area in the frontal section in these brains will be practically
proportional to the frontal diameter of the cerebrum (W. D).
The agreement of the calculated with the observed values is
however not so good as in the ease of the sagittal section.

and the ratio of this value to W. D were

F. The area of the entire frontal section

In chart 1, the graph F, representing the total area of the
frontal section, is accompanied by a dotted line 7’, which repre-
sents the value of the square of the cube root of the brain weight
(in grams). Theoretically, under the assumption that the spe-
cific gravity of the brain remains the same throughout the life,
the latter should run a similar course to the former, if the brain
enlarges proportionally in all dimensions as it grows. Between
Groups II to XIV, both curves take nearly the same course, if
some slight discrepancies in the observed values are neglected.
But in brains weighing more than 1.4 grams, the differences
become so distinct, that they can no longer be regarded as due
to errors in measurement. This is probably due to the fact
that the brain is not enlarging proportionally in all diameters,

? In making comparisons with the Norway rat in part II of this paper, the

average ratio given by Groups XIII to XX will be that used. This average
is 0.93.

80 NAOKI SUGITA
TABLE 5
Showing, in columns ‘A to E, the relations of the cortical area in the frontal section
to the frontal diameter of the cerebrum (W. D) and the cortical thickness, and,
in columns H to J, the relations of the total area of the frontal section and the

frontal diameter of the cerebrum. All values for the fresh condition. Albino rat.

A B Cc D 1D) F G H I J

vcat | “CAL W.D pei fis
5 TWAIN |) RULES MEE | cn E or |SQUARE| H
sche THOS ee [ears | 2 aimee a a es ae WD i
seers Sacrton SEEEION
grams mm. mm. mm. mm. mm.2 mm.

i 0.161; 3.9} 0.56} 7.0] 6.6] 1.06 | 11.9! 43.6) 0.27

II (birth) Q.251| 5-7 -| 0.78 |) e723)| ~ 7. 79) 01954) 720) a5 9es eee

Ill 0.358} 8.0) 1.02 | 7.9) 8.7 | 0.91 | 20.6 | 75.7) 0.27

IV Or432)" OF i Lew | 8.21} 9.3 | 0.88 | 22:4 | 86.5) 0.26

V 0.542) 11.7 | 1.33 | 8.7 | 10.1 | 0.86 | 26.9 | 102.0) 0.26

VI 0.639) 14.4] 1.55 | 9.3 | 10.6 | 0.88 | 31.1 | 112.4] 0.28
VII 0.750; 16.4 | 1.7 9.5 | 11.2 | 0.85 | 32.6 |. 125.4) 0.26
VIII 0.841) 18.4:| 1.82 | 10.1 | 11.6 | 0.87 | 3819 | 134-6)50:29
IX(10 days) | 0.964) 20.4 | 1.86 | 11.0 | 12.1 | 0.91 | 42.3 | 146.4] 0.28

x 1.040) 20.8 | 1.82 | 11.4 | 12.4 | 0.92 | 44.2 | 153.8) 0.29

XI eudays) LV70) 21.7) 191-| 11245) 12:7 | O90.) 4527 16h. 30228
XII 1.253) 23.0 | 1.91 | 12.0 | 13.0 | 0.92 | 47.2 | 169.0) 0.28
XIII 1.335) 23.2 | 1.94 | 12.0 | 138.2 | 0.91 | 50.2 | 174.2' 0.29
XIV 1.445) 24.8 | 1.99 | 12.5 | 13.4 | 0.93 | 52.3 | 179.6) 0.29
XV 1.554) 24.3 | 1.97 | 12.3 | 13.5 | 0.91 | 54.0 | 182.3] 0.30
XVI 1,656) 24.3°| 1.94 | 12.5 | 1327)90.91 | 54.9) 187 sn 90228
XVII 1.726] 24.6 | 1.90 | 12.9 | 13.8 | 0.94 | 56.4 | 190.4) 0.30
XVIII 1.839] 26.0 | 1.97 | 13.2 | 14.1] 0.94 | 58.9 | 198.8] 0.30
XIX 1.924) 24.8 | 1.83 | 18.5 | 14.3 | 0.94 | 57.0 | 204.5) 0.28
XX 2.054 24.9 1.72 | 14.5 | 14.6 | 0.99 | 63.4 | 213.2) 0.30
Aversce (Groups iV §) 5435009 Lie ee ee ee 0.91 0.28

Average (Groups atl XX) fe i see ee eee 0.93

the increase in the frontal diameter being retarded relative to
the sagittal diameter in brains weighing more than 1.4 grams
(Sugita, 717).

If, as given in columns H. and JI, table 5, the area of the total
frontal section is compared with the square of W.D of the cor-
responding brain group, the above inference will be supported
by the fact that the ratio, given in column J of the same table,

GROWTH OF THE CEREBRAL CORTEX 81

is almost equal throughout all brain weight groups, swinging
within the narrow limits of 0.26 to 0.30.

G. Percentage of the area of cortex in the total area of the frontal
section (one hemicerebrum)

Figure 2 shows the outline of the frontal section. In the
section we see as the principal divisions the cortex, the striatum,
the thalamus, the capsula externa and the lateral ventricle,
and, among these, the cortex and the striatum stand in marked
contrast. In the young brains, the lateral ventricle is wide.
This cavity was not included in the measurement of the area.
In the wall of it, especially at the dorso-lateral corner, there
are seen masses of dividing cells and of neuroblasts, which are
due to migrate into the cortex. But in the older brains weigh-
ing more than 1.1 grams, the ventricular wall is almost free
from dividing cells and the cortex is no longer receiving new
cells. By determining the percentage of the cortical area to
the total area of the frontal section, we may obtain some clue
as to mass relation of the cortex to the other structures seen in
the frontal section.

As previously given in table 2, the cortical area in the frontal
section amounts to 34 per cent of the total area at birth. It
increases from birth up to brains weighing 0.7 to 1.2 grams,
when the percentage reaches its highest figure, that is, 50 or
sometimes 51, on the average 48 per cent. After this stage,
the percentage slowly diminishes as the brain weight increases,
and, at full maturity, it reaches 44 per cent or less; even 39 per
cent in an old brain weighing more than 2.0 grams. This means
clearly that the cortical area increases rapidly by receiving
new cells from the matrix and at the same time by the enlarge-
ment and separation of the cell bodies, during the first phase,
covering the first ten days after birth.

In this phase, as a matter of fact, the remainder of the sec-
tion is for the most part composed of the matrix and migrating
cells, the central nuclei being not yet so largely developed.
The transitional layers, or the areas previously occupied by the

82 NAOKI SUGITA

transitional layers, which will be replaced by the ecapsula ex-
terna, are relatively wide during this phase.

After twenty days, when the brain has attained nearly the
weight of 1.17 grams, the remainder of the section (the central
nuclei and the white substance) increases more rapidly than
the cortical area and the group of proliferating cells in the ven-
tricular wall disappears. The percentage of the cortical area
to that of the whole section consequently decreases under these
conditions, though the absolute value of the cortical area is
steadily increasing.

From the mode of the changes in the percentage value of the
cortical area, we may conclude that, in the albino rat, at least,
the period during which the brain weight increases from 0.25
gram (birth) to 1.2 grams (about 20 days), is the period when
the cortical elements are principally produced, matured and
arranged, and that the cortex is precocious in its construction.
The growth or construction of the remaining parts in the frontal
section, so far at least as this is expressed by increase in volume,
is relatively retarded or delayed until the cortex has acquired
all its characteristic elements.

H. The volume of the entire cortex

The true volume of the entire cerebral cortex can not be
measured by the methods here used. It will require a special
study for that purpose. My present object is to obtain relative
values for the cortical volume and a record of the change in
these relative values according to brain growth. If the data
for the area of the cerebral cortex as measured by me in the two
typical sections be reduced to a simple geometrical form, it will
be very easy to compare the changes in the computed volume in
successive brain weight groups. As already mentioned, the
cortical area in the sagittal and the frontal sections, which
sections cross one another at right angles, may be reduced to
rectangles which have as the long side the lengths proportional
respectively to the sagittal and the frontal diameters of the
cerebrum (L.F and W.D), and as the short side the cortical

GROWTH OF THE CEREBRAL CORTEX 83

thicknesses (7', and T',,). For the present purpose, the mean
cortical thickness (7') may be substituted for both the foregoing
values of the cortical thickness, when the brain weight is the
same, because 7’ falls at the mean of the 7, and T7',, so that
the gain in 7’, would be compensated by the loss in 7’, (fig. 3).
As a consequence the volume of the cortex may be represented
by an index value, the formula for which follows.®

ale, WED Xe SE (all in millimeters)

Fig. 3. The solid lines show the simplified geometrical form used to indicate
the volume of the entire cortex, which is assumed to be proportional to the rect-
angular form designated by dotted lines in the figure. The volume of the rect-
angular figure, which was obtained by the value: L. F X W. V X T, has been
tabulated in column F, table 6, and plotted as graph LWT in chart 2.

The values thus obtained—which mean the actual volume of
the rectangle denoted by dotted lines in figure 3—stand in a
fixed relation to the true cortical volume which is denoted by
solid lines in the same figure, as far as the latter retains a similar
form during growth.

’In this formula, the coefficients 1.22 and 0.91, which were empirically de-
termined, were eliminated, because these coefficients are fixed throughout all
the groups to be compared. For Groups XIII to XX, the coefficients are re-

spectively 1.21 and 0.93, and these will be taken into consideration when com-
parison is made between the Albino and the Norway rats.

84 NAOKI SUGITA

TABLE 6
Giving for each brain weight group the average brain weight, ratio in cerebral volume,
computed cortical volume and the data used to obtain the computed cortical volume,
and ratio in cortical volume

A B C D E F G
L.F X
BRAIN WEIGHT GROUP ; ae LF W.D Tf} W. DXeie pp aasanea
eater vonume aa ee “Contra ‘vous: youu
CEREBRUM ance Conn CORTEX
grams mim. mm. mm. mm 3
I 0.161 5.6 6.6 0.54 19.96
II (birth) 0.251 1.00 6.4 ool 0.73 35.97 1.00
Ill 0.358 | 1.34 a: 8.7 0.96 61.81 Lae
IV 0.452 1.66 8.0 9.3 1.10 81.84 2.28
V 0.542 22 ee) |) UO al 1.24 111.46 3.10
VI 0.639 ZOD 9.6 10.6 1.42 144.50 4.02
VII 0.750 Sez, 10.4 IN 1.58 184.04 9.12
VIII 0.841 3250): 11.0 16 1.65 210.54 5.85
IX (10 days) 0.964 4.04 11.6 Wall eg 240.02 6.67
x 1.040 4.10 12.0 12.4 172 255 . 94 mee
XI (20 days) all | Zeal 12.5 12.7 1.82 288 .93 8.03
XII 1.253 4.80 12.8 13.0 1.83 304.51 8.47
XTil 1.335 dba 13.0 13.2 1.83 314.03 8.73
XIV 1.445 5.40 13.3 13.4 1.85 | 329.71 9.17
XV 1.554 5.89 13).7 13.5 1.87 345.86 9.62
xXVI 1.656 6.05 14.1 Bie 7 1.86 | 359.30 | 9.99
XVII 1.726 | 6.44 14.3 13.8 1.85 365.08 | 10.15
XVITI 1.839 | 6.72 14.7 14.1 1.92 | 397.96 | 11.06
XIX 1.924 6.9 15.0 14.3 1.82 | 390.39 | 10.85
xX 2.054 7.85 1523 14.6 1.76 393.15 | 10.93

1T, here entered, is the mean value of Ts and T,, previously given in tables
4 and 5 and is not the general average thickness of the cortex of the sagittal,
frontal arid horizontal sections formerly presented in my second paper in this
series (Sugita, 717 a).

Table 6 shows the values for the cortical volume computed by
the above method and the ratios, the cortical volume at birth
being taken as the unit of the comparison.

Chart 2 (graph LWT) shows graphically the ratios obtained
(table 6, column G), accompanied by the graph (graph LWH)
which shows the increase in volume of the cerebrum (table 6,
column B). The volume of the cerebrum was computed ac-
cording to my previous procedure (Sugita, 17). From this

GROWTH OF THE CHREBRAL CORTEX so

chart we see that the cortical volume increases more rapidly
than the entire cerebral volume, until the brain attains the weight
of 1.17 grams (20 days) (see crosses in chart 2). If we take
these marks as the starting points, then the cerebral volume
increases to about 1.7 times at full maturity and in the same
way the cortical volume increases to about 1.4 times compared
with the value at twenty days (table 6). So, it may be stated
that after twenty days the increase in cortical volume becomes

f | T i T ] ] a] = | PR ail
| | | | !
13 | | | eee =
| | | | |
| | |
42 — | t | = |
| | | |
41 + = + + <a
! | | i Ipeeteha | | PCa ae |
} | | Or aa
10) ee See a SS = |
| LASS RERrr |
9 . ai T r = 1 |
47 ees | | |
od } |
8 T Zale } iI L | | aol
Wa | } | | | | | <\
7 Sal + a8 ae ¥
Or | | ees: | | ihe |
| | |
6- 7 a = =
\I | | Se om
‘ | | | | pee |
5) VY } | 1 Pha aI | it aie + | |
| NS | | | | ee | |
4) NN | | | == ie | a! Ne OE es Pe es
‘ QZ + | | |
; Sian | | | | |
ie el Se aclals mot!
ee an) ai ge aah | | isso
a | | aa = x i—x
1 Lez aa _ + ta | “ices | } Ly
fe] eevee cea | |

Of 02B03 04 05 06 07 08 09 10 ff 12 13 14 15 46 17 18 19 20 gs

Chart 2. Showing the ratios of the values for the cortical volume, the volume
of the cerebrum, the cell density in two unit volumes and the computed number
of nerve cells in the entire cerebral cortex of the albino rat, according to the
brain weight. e « LWT, The ratios of the computed volume of the cerebral
cortex, the volume at birth being taken as the unit. Based on the data in table
6. . LWH, The ratios of the volume of the entire cerebrum,
the volume at birth being taken as the unit. Based on the data presented in a
former paper (Sugita, 717) and given also in table 6. X——XN, The cell den-
sity in two unit volumes of the cortex. Based on the data given in column C,
table 7, as N, and plotted here according to the values corresponding to one one-
hundredth of the number given in column C, table 7. *— *—*NLWT, The
ratios of the computed number of nerve cells in the entire cortex, the value at
birth being taken as the unit. Here the unit chosen on the ordinate is 5. The
data are given in column E, table 7.

86 NAOKI SUGITA

slower and is somewhat less in rate than the increase in cere-
bral volume or brain weight, as is also seen in the graphs given
in chart 2. ;

I. Number of cells in a unit volume of the cortex

In the lamina pyramidalis of the newborn Albino brain, at a
dorso-lateral part of the pallium, where, in the frontal section,
the cell count was nYade (fig. 2, VII), there were in the fresh
condition about 500 pyramids crowded in a unit volume of 0.001
mm.’ This number decreases, as the brain grows, and falls to
110 in a brain weighing about 1.2 grams (20 days) (table 3).
In a brain weighing about 1.5 grams (50 days), the number has
dropped nearly to 90, from which it is only slightly reduced in
the heavier brains. In an old rat, whose brain weighs more
than 2.0 grams, the number is about 80, or less than one-sixth
the number at birth. According to another study, which will
be published later, the size of the cell body and of the nucleus
of the pyramids in the lamina pyramidalis, measured at this
same locality, increases very rapidly during the first ten days
after birth, till the brain has attained 0.9 gram in weight, when
these structures reach their maximum size (Cell body 16u X 20u;
Nucleus 14u X 15y). After this stage the cell body and the
nucleus are mature in their nucleus-plasma relation, but still
changing their chemical composition, as revealed by the stains,
while the neuron as a whole is still growing as shown by the
developing axon and the dendrites.’ This fact is in accord with
the observation that the number of pyramidal cells in the lamina
pyramidalis decreases rapidly after birth, until the brain weight
reaches about 0.9 gram (10 days), after which the rate of decrease
becomes slow.

The change in cell number in a given volume of the cortex
during the growth of the brain is determined by two main
factors: (1) the enlargement of the cell body proper and the
growth of the cell branches and (2) the development of the
intercellular structures (that is, incoming nerve fibers, neuroglia,
blood vessels) and myelin formation, separating the cells more
and more from each other.

GROWTH OF THE CEREBRAL CORTEX 87

As to the cells in the lamina ganglionaris, the relation is
somewhat different from that just described. ‘The total number
of cells, including both the small and large pyramids, decreases
relatively rapidly after birth, until the brain weight reaches
1.25 grams (25 days). It then shows a slight increase (table 3,
Groups XIII and XIV), but decreases again by slow steps and
remains almost fixed after 35 days (brain weight 1.4 grams)
at 60. Finally, in old rats, only 50 cells were counted in a unit
volume of 0.001 mm.,* or about one-fifth the number at birth.

If the number of the large pyramids alone is considered, then
the number decreases rapidly from birth to a brain weight of
0.8 gram (9 days). After this, it decreases slightly and remains
almost fixed at 23 up to a brain weighing 1.2 grams. In brains
weighing 1.3 to 1.5 grams it shows a tendency to increase slightly
for a time—corresponding to the increase in total number of
cells in this layer (above mentioned)—but finally becomes fixed
again at 23 to 24 throughout maturity. In old age, it has
diminished to 20 or about two-sevenths the number at birth.
The large ganglion cells attain nearly their full size (Cell body
21u X 28u; Nucleus 184 x 19%) at 0.9 gram in brain weight
(10 days), almost at the same time as the small pyramids.

I can not, from the data at hand, satisfactorily explain the
increase in cell number in the lamina ganglionaris in the period
during which the brain grows from 1.2 grams to 1.4 grams in
weight. This fact might however have some connection with
the chemical structure of the cells and consequently be related
to a change in reaction to the reagents used, so that the size of
the large pyramids, after having attained a maximum (21ly X 28.)
at a brain weight of 0.9 gram, diminishes slightly, at the same
time that their response to the stain changes somewhat, meas-
uring only 20u X 27y at a brain weight of 1.3 to 1.4 grams,
after which they again enlarge to a full size of the cell body
(sometimes over 23u X 30u). In the ecarbol-thionine staining
the sections from brains weighing less than 1.0 gram show a
violet tone, those from brains weighing more than 1.2 grams a
blue tone while those from brains weighing 1.0 to 1.2 grams are
intermediate in tone. We shall pass over this question now,

SS NAOKI SUGITA

as a detailed description of the size of each cell type and its
mode of enlargement according to age will be the theme of a later
paper.

To represent the relative cell density in the cerebral cortex
for each brain weight group, the sum of the cell numbers in the
lamina pyramidalis and the lamina ganglionaris, given in table
3, was used, in order to balance, in some measure, the inequality
of the cell distribution. These values are given in table 7,
column C, and in chart 2 (graph N). Both table and chart
show that the number of nerve cells in a unit volume of the cor-
tex decreases very rapidly during the first ten days after birth
(up to the brain weight of 0.95 gram) and after that time it
decreases slowly but steadily as the age advances. The cell
number at maturity. is nearly one-fifth the value at birth.

J. Values for the computed number of nerve cells in the entire
cerebral cortex, according to brain weight

The number of nerve cells given in table 3 does not means the
actual volume of complete cells contained in a unit volume,
because the parts of cells which showed a nucleus but no nu-
cleolus in the section were also counted. In spite of this, the
number in the table indicates fairly the relative number of cells
or the relative cell density at different ages in the localities
examined, and from this we may be able to get some indication
as to the number of nerve cells in the entire cerebral cortex.

If the actual number of cells in a unit volume be proportional
to the number of cells counted, the number of cells in the entire
cerebral cortex may be indicated (theoretically) by this number
multiplied by the number obtained by dividing the volume of
the entire cerebral cortex by the unit volume.

The actual volume of the cortex was not measured, but the
computed volume is indicated by the following formula, as
explained already.

BY RS |S OE (all in millimeters)

So, if N means the cell number in a unit volume (for example,

GROWTH OF THE CEREBRAL CORTEX 89

N is 240 for Group VIII, as shown in table 7, column C), the
relative value of the number of nerve cells in the entire cortex
may be. computed by the following formula.‘

INCL OE SOW). Det (L.F, W.D and T, in millimeters)

The results of this computation are shown in table 7 and in
chart:2 (graph NLWT), where the necessary data were all taken
from the present or former papers and the relative value of
NXL.F XW.D XT is calculated. For N, the corrected
sum of the cell numbers in the lamina pyramidalis and in the
lamina ganglionaris, given in table 3, was used (table 7, column
C). The results are quite interesting. As seen from table 7,
columns D and E, and chart 2 (graph NLWT based on column
’ BE), the relative value of the computed number of cells in the
entire cortex increases rapidly from birth to a brain weighing
0.9 gram (about 10 days), and then for a while the increase
becomes slow up to a brain weight of 1.17 grams (20 days),
attaining at this time nearly the complete number of nerve
cells (see graph NLWT, mark X in chart 2). After having passed
this phase, the value for the number of cells remains almost
constant throughout the life. The average of the values for
Groups XI—XX in table 7 is 530, so that between birth and ma-
turity the number of cells counted has increased two times,
but nearly al/ of this increase has taken place during the first
ten days of life. These results coincide very well with the con-
clusions of Allen (12), that in the cerebrum mitosis continues
with diminishing activity to the 20th day after birth.

4 By this computation the number of cells in the entire cortex will be equal
to the number of times the unit of volume, 0.001 mm.* in which the cells were
counted, is contained in the entire volume of the cortex, multiplied by the num-
ber of cells in a unit volume. The number of cells designated by N is however
the sum of the numbers in two unit volumes, that is, the number in one unit
volume of the lamina pyramidalis plus the number in one unit volume of the
lamina ganglionaris.

Since the numbers of cells used, N, is that in two unit volumes, the fore-
going product must be divided by two. As dividing the volume of the cortex
by 0.001 is equivalent to multiplying it by 1000, and as the product must be
divided by two, the operation may be expressed as follows:

NXL.F XW.D XT X 500 = Number of cells

90 NAOKI SUGITA °

TABLE 7
Giving the computed number of nerve cells in the entire cerebral cortex, obtained on
the basis of the measurements given in this series of studies. The ratio of the
number of cells of each later group to that of Group IT (birth) is also given

A | B | Cc D E
COMPUTED
oes weer ana | compurep | ‘Gromusin | CELLS | 3
ER CORTEX ee PLR. AND 7. ee OF NUMBER
WEIGHT L. Tesi _D Pe een W.DXT OF CELLS
voLuMEs, K x ay
100
grams mms
II (birth) 0.251 35.97 739 265.8 1.00
Ill 0.358 61.81 590 364.7 1.8)
IV 0.482 81.84 499 408 .4 1.54
Vi 0.542 111.46 394 439 .2 1.65
VI 0.639 144.50 305 440.8 1.66
Vil 0.750 184.04 257 473.0 1.78
VIil 0.841 210.54 240 505.3 1.90
IX (10 days) 0.964 240.02 213 Sul? 1.92
x 1.040 255 .94 198 506.8 1.91
XI (20 days) eal 288 .93 186 537.4 2.02
XII 1.2538 304.51 IZAl S201 1.96
XIII 350 314.038 176 902.7 2.08
XIV 1.445 329.71 165 544.0 2.05
XV 1.554 345.86 149 515.3 1.94
XVI 1.656 309.30 144 517.4 1.95
XVII 1.726 365.08 146 533.0 2.01
XVIII 1.839 397 .96 138 549.2 2.07
XTX 1.924 390.39 132 Sls) 253 1.94
xX 2.054 393 .15 131 playa) 1.94
Average ey (Groups Nens) eae dns Aa eee 530.0 2.00
Averages (Groups engl NON) 1a ne aes 530.2 2.00

1 As explained in a footnote (footnote 4), the actual number of cells contained
in the computed volume of the cortex should be N X L. F X W. D X T X 500,
but, for the convenience, 1/100 of N X L. F X W.D X T, or 1/50,000 of the
actual number of cells contained in the computed volume, was given here as
the computed number of cells in the cortex.

The above statement that between birthand maturity the
number of nerve cells in the entire cortex has increased two-
fold, does not necessarily mean that the additional cells have
been all newly formed after birth. As a matter of fact, we see,

GROWTH OF THE CEREBRAL CORTEX 91

in the sections of the newborn brains, many immature cells,
the indifferent cells and the neuroblasts, crowded densely to-
gether in the ventricular wall and in the transitional layers
and these are all migrating to the cortex. The number of cells
in the cortex is increased after birth by receiving these cells
already formed but lying at birth still outside of the cortex proper,
besides by receiving the cells which are newly formed after birth.
So the nerve cells, destined for the cortex, are largely present in
immature form in the cerebrum at birth, but lie outside of the
cortex proper, while the actual number of cells formed after
birth may amount only to a small fraction of the total number
of nerve cells in the cortex at maturity, though there is active
mitosis during the first days after birth.

I have previously recognized three developmental phases in
the growth of the cortex in thickness (Sugita, ’17 a), as follows:

First phase, from birth to the 10th day.

Second phase, from the 10th to the 20th day.

Third phase, from the 20th to the 90th day.

The first and the second phases here given may also be applied,
without any modification, to the changes in cell number in the
cerebral cortex, while the third phase does not appear in this
connection.

IV. CONCLUSIONS

In an earlier study on the cerebral cortex of the albino rat
(Sugita, ’17 a), I stated that the cerebral cortex attains nearly
its full thickness at the age of twenty days, before myelination
in the cortex had begun, and that the organization of the cerebral
cortex might be considered as precocious, having been provided
with all its mechanisms at the time of weaning. At this age,
the brain weight is only a little more than one-half the weight
at maturity. Size, volume and weight of the entire brain are
all midway in their growth, but there have appeared no striking
changes by which we might guess from the gross appearance of
the brain anything about the numerical completeness of its
cortical elements. Just at this stage, however, cell division in
the cerebrum has almost ceased (Allen, 712).

92 NAOKI SUGITA

From the data now available, I conclude that, in the albino
rat, the cerebral cortex exhibits the complete number of nerve
cells at about the 20th day after birth, at which age some of the
cells have attained their full size. The area of the cortex in the
sagittal and in the frontal sections has shown a continuous
increase throughout life and no radical change in rate occurs at
this time. But, if the thickness of the cortex be taken into
consideration and the volume of the entire cortex be calculated,
it becomes clear that the entire volume of the cerebral cortex
has stopped the more active increase, which it made earlier,
at about the 20th day, and after that the increase becomes
slow, and lower in rate than the increase in the volume of the
cerebrum. If, further, the cell density in the cortex be con-
sidered, it is found that the number of cells as computed for
the cerebral cortex (table 7, column E) increases rapidly,
especially during the first ten days after birth, but exhibits
nearly its complete number at the age of twenty days, after
which it shows no significant change.

We may conclude therefore that the cerebral cortex has been
completely organized at the age of about twenty days, and that
the further development of the cortex does not involve:an in-
crease in cell number, but involves mainly the maturing of ele-
ments already provided. The education of the cerebral cortex
as a whole might properly be said to begin after this age, the
preceding period having been largely one of preparation or
construction. It is of interest to note that this epoch cor-
responds to the weaning time of the rat.

According to the study of Donaldson (’08) on the comparison
of the albino rat and man, the rat grows thirty times as fast as
man. When however the brain of the rat is to be compared
with that of man, it must be remembered that at birth the human
brain is somewhat more mature and corresponds in organiza-
tion not with the rat brain at birth but at five days of age (Don-
aldson MS8.). This being the case, the rat cortex at the 20th
day of postnatal life probably corresponds with the human
cortex at the 15th month (20 less 5). This conclusion has not
yet been tested. 7

GROWTH OF THE CEREBRAI:. CORTEX 93
V. SUMMARY

1. Employing the sagittal and the frontal sections of 78
albino rats, which were formerly used for the investigation on
the thickness of the cerebral cortex (Sugita, 717 a), I made
further measurements on the area of the cortex in these sections
and counted at a fixed locality the number of nerve cells contained
in a unit volume of 0.001 mm.,? in brains from birth to maturity.

2. The observed data were all corrected to the values for the
fresh condition of the material, by the use of the correction-
coefficients based on the observations. The results were grouped
and averaged according to the brain weight groups and the
postnatal growth changes systematically analysed.

3. The area of the cortex shown in the sagittal section is found
to be proportional to the value L. F x T,, where L. F is the
longitudinal diameter of the cerebrum and T’, is the average
thickness of the cerebral cortex in the sagittal section. The
actual area (after five days of age) may be calculated by the
formulas H.6F <x 22 Ch. F and T.;. im. mullumeters)):
where 1.22 is a constant coefficient which was empirically de-
termined (see table 4, column G).

4. The area of the cortex shown in the frontal section (of one
hemicerebrum) is found to be proportional to the value W.D x T,,,
where W. D isthe frontal diameter of the cerebrum and T, is
the average thickness of the cortex in the frontal section. The
actual area (after five days of age) may be calculated by the
formula: W.D x T, X 0.91 (W.D and T,, in millimeters),
where 0.91 is a constant coefficient which was empirically de-
termined (table 5, column G).

5. The percentage of the total’ area of that frontal section
which is represented by the cortical area is least at birth (34
per cent) and increases as the age advances till it reaches the
maximum (50 per cent) at the period of 7 to 20 days (brain
weight 0.75 to 1.25 grams). It then decreases, slowly and at
maturity is less than 44 per cent (table 2). This means that
during the first 7 days the cortex is increasing in area more
rapidly than the remainder of the section, while during the

THE JOURNAL OF COMPARATIVE NEUROLOGY, VOL. 29, NO. 2

94 NAOKI SUGITA

following 13 days its rate of increase is similar to that of the re-
mainder. After 20 days the rate of increase for the remainder
surpasses that for the cortex.

6. The actual volume of the cortex could not be obtained by
the use of the data now available, but the computed volumes
of the cerebral cortex at different ages (comparable among
themselves), may be found by the use of the formula: L. F x
W.D x T (all in millimeters), where L. F is the longitudinal
diameter of the cerebrum, W.D is the frontal diameter of the
cerebrum and 7’ is the average thickness of the cortex. The
volume increases most rapidly during the first ten days after
birth and the rate of increase in the cortical volume continues to
surpass the rate of increase in the entire cerebral volume, dur-
ing the first twenty days. After twenty days the cortex increases
at a somewhat lower rate than the increase of the entire cere-
brum in volume (chart 2).

7. The number of cells contained in a unit volume of 0.001
mm.’ of the cortex indicates the cell density of the locality where
the count was made. In the lamina pyramidalis the pyramids
are most crowded at birth and the number in the unit volume
decreases rapidly during the first ten days after birth. After
twenty days it decreases slowly but steadily, the number at
maturity being about one-sixth the number at birth. As for
the lamina ganglionaris, the total cell number in the unit volume
(the small and the large pyramids taken together), is at its
highest value at birth. It decreases relatively rapidly during
the first twenty-five days after birth, then is slightly increased
for a time, after which it decreases again slowly and at full
maturity it shows about one-fifth the number present at birth.
Taking the large ganglion cells alone, we find that the number
decreases rapidly during the first eight to ten days, then remains
the same up to twenty days, after which it decreases again,
showing two-sevenths the initial number at full maturity. The
decrease in cell-density according to brain growth is due to the
enlargement of cell bodies, the development of cell attachments,
the separation of cells from each other through myelination,
ingrowing fibers and other changes. The average cell density,

GROWTH OF THE CEREBRAL CORTEX 95
represented by the sum of the numbers in the lamina pyra-
midalis and the lamina gariglionaris, given as N in table 7, de-
creases rapidly during the first ten days and after that the de-
crease becomes very slow and steady, showing at maturity a
density of about one-fifth of that at birth.

8. The computed value for the number of cells in the entire
cerebral cortex may be determined by the formula: NV x L. F Xx
W.D xT (L.F,W.D and T, all in millimeters), where L. F
is the longitudinal diameter of the cerebrum, W.D the frontal
diameter of the cerebrum, 7 the average thickness of the sa-
gittal and frontal cortex and N the average number of the
nerve cells in two unit volumes of the cortex, at the particular
locality (locality VII) where the counts were made. This com-
puted value for the number of nerve cells in the entire cerebral
cortex increases rapidly during the first ten days, at the end of
which period it attains nearly 1.9 times the value at birth.
During the following ten days, it increases slowly but steadily,
and it attains its complete number at the age of twenty days
(brain weight 1.17 grams). After this age the number of nerve
cells is almost constant. The number of cells at maturity is
twice the number at birth.

It is recognized that this conclusion concerning the number
of nerve cells in the cortex at various ages is based on enumera-
tions in only two cortical layers at but one locality, and that
on this ground its general value might be questioned. When
it is recalled however that table 11 in a preceding study on the
growth of the cortex in thickness (Sugita, 717 a) shows all the
localities measured in the cortex to undergo the same relative
increase in thickness between birth and maturity, and always
to stand in the same relation to one another, the doubts with
regard to the general value of these particular results are largely
removed.

9. Considered all together, the data on the development of
the cerebral cortex indicate that it has been completely organ-
ized in the albino rat at the age of twenty days. The further
development after this age represents a maturing of the elements.
The completion of the cerebral organization corresponds to the

96 NAOKI SUGITA

weaning time of the rat... If the cerebral organization of the rat
brain at five days of age is similar to that of the man at birth,
and the growth processes in the rat are thirty times as rapid as
in man, then the completion of the cortex which occurs in the
rat brain at twenty days should occur in the human brain at
about fifteenth month of age.

PART

ON THE AREA OF THE, CORTEX AND ON THE NUMBER OF CELLS
IN A UNIT VOLUME, MEASURED ON THE FRONTAL AND SAGITTAL
SECTIONS OF THE BRAIN OF THE NORWAY RAT (mus NOR-
VEGICUS), AND COMPARED WITH THE CORRESPONDING DATA FOR
THE ALBINO RAT

VI. INTRODUCTION

In the Part I of this paper, I have presented the data on the
area of the cerebral cortex measured on the sagittal and the
frontal sections of the Albino rat brain and on the number of
nerve cells in a unit volume of the cerebral cortex, and, by cal-
culations based on these data, I have come to the conclusion
that the entire volume of the cerebral cortex is increasing most
rapidly during the first ten days after birth, while from twenty
days onwards it increases at a lower rate than the entire cerebral
volume. Further, the computed number of nerve cells in the
entire cerebral cortex also increases very rapidly during the first
ten days after birth and attains nearly its complete number at
the age of twenty days.

I now wish to compare these relations in the Albino with
those in the Norway rat, in the same manner as I have already
done in the matter of the growth of the brain in size (Sugita,
18) and of the thickness of the cortex (Sugita, ’18 a).

Employing for the Norway brains the sections on which the
cortical thickness was measured earlier and for which the in-
dividual body measurements have been already given in table
1 in my fourth paper (Sugita, ’18 a), I have measured the area

GROWTH OF THE CEREBRAL CORTEX 97

of the cortex in the sagittal and the frontal section, following
methods of measurement just described (part I) in the case of
the Albino rat. Correction of the observed values to the
values in the fresh condition of the material was also made
by the use of the correction-coefficients obtained in the same
way as those used for the Albino.

This study was made between March and May, 1917, at the
Wistar Institute of Anatomy and Biology.

VII. MEASUREMENTS AND ENUMERATIONS
K. Area of the cortex in the sagittal section (Norway rat)

Table 8 shows the observed and corrected areas of the cere-
bral cortex in the sagittal section of the Norway brain, also the
data for the correction-coefhicient for each individual, and the
correction-coeffiicient for each brain weight group. The method
of measurement and the positions of the borderlines of the
measured area have been already described in part I of this
paper, so that the explanations need not be repeated here (fig.
1). Chart 3 (graph s) has been plotted on the basis of table 8.

L. Area of the cortex in the frontal section (Norway rat)

Table 9 gives the observed and corrected areas of the cortex
and the total area of the frontal section (one hemicerebrum) of
the Norway brain with the data for the correction-coefficient
for each individual and the correction-coefficient for each brain
weight group. It gives also the percentage of the cortical area
to the total area of the section. Chart 3 shows also in graphs
(graphs F and f) the corrected data given in table 9.

M. Number of nerve cells (Norway rat)

Table 10 gives the observed and corrected number of nerve
cells in a unit volume of 0.001 mm.’ (0.1 mm.” in area and 0.01
mm. in thickness) at a fixed locality (locality VII) of the cortex
in the frontal section, for each individual and for each brain
weight group. The locality was chosen at a middle part of the
cortical band in the frontal section as shown in figure 2, VII,

QS NAOKI SUGITA

for the Albino rat. The numbers of cells in the lamina -pyra-
midalis and in the lamina ganglionaris respectively and the num-
ber of ganglion cells only in the lamina ganglionaris in five
adjoining squares, each 100 micra on each side, were counted
and the numbers in the unit volume of 0.001 mm.’ computed
(see part I) and recorded in table 10. The relative cell density

mm
Sa = SS SS SS SS
| 7 |r
| gal SE aa Gaia eT et} tt
| ee
60 |— ——;— +--+ : Bea + - ——-+— _
He aan Pe ola bela
+ — +- —+> +4———— _ + + —t —— Se
55 i t | =< iat
| |
| |
ee al pal alae —
ae | } | | |
| ia ==
| | | |
| | | | | |
40} t—:——, “2 + ———— |
| |
5 = SSS SS ESSE = leeks)
| | eres ee sauna
| [Pcs eee cela a
0 +— ———— p<" ———= — a a ns Cn ———
ma ees ee 2S SaaS
| eal| SS ein | |
25) Bee =a an GT alae oe
| ile | | |
20 —t a == es = — st
| | | ] |
| | |
ee ie i a ees eee
10 (ees el Ae ee eee [ave oe oo =
| | | }
| | | | | | | ¢
5\— - Ro bp pt
leer | | | |
eaesatl aed

0! yeas =| af al | | | eee || ih ee aed [bee a)
a TR GIS EE SUS IS SE SES PMS) a al IR 3 gms.

Chart 3. Showing the areas of the cerebral cortex in the sagittal and the
frontal sections and the areas of the whole frontal section according to the brain
weight. Norway rat. This chart is comparable with chart 1, which gives the
corresponding graphs for the albino rat. X—.—.— Xs Cortical area in the
sagittal section. °¢ ef, Cortical area in the frontal section. *——eF, Area of
the whole frontal section. All graphs were based on the data in tables 8 and 9.

represented by the sum of the numbers of nerve cells in the lam-
ina pyramidalis and the lamina ganglionaris is tabulated in table
16, column D, and plotted in chart 4 as graph N’.

VIII. DISCUSSION AND COMPARISON

The foregoing data, treated in a manner similar to that adopted
in the case of the Albino (part I), may now be used for discus-
sion and comparison.

GROWTH OF THE CEREBRAL CORTEX

TABLE 8

99

Showing the observed and corrected values of. the area of the cerebral cortex in the
sagittal section of the Norway rat brain, accompanied by the data for the correc-
tion-coefficient in the individual cases and the correction-coefficient for each
brain weight group. L. F is the longitudinal diameter of the cerebrum

CORRECTION-COEFFICIENT

OBSERVED
GROUP BRAIN WEIGHT AREA
OF CORTEX ¢ The same
on fresh brain on slide
grams mm .2 mm. mm.
N XI b 1155 18.4 ILL} 10.40
a 1.160 17.0 12.10 10.15
1 eS 14.2 12.55 9.60
1.163 16.5 1.21?
N XII
N XIII a .369 16.7 12.95 10.10
1.369 16.7 ees
N XIV b 1.407 18.2 13.45 10.50
g 1.429 16.3 13.05 10.10
a 1.431 19.1 13215 10.40
1 1.431 18.1 13.05 10.25
e 1.437 15.8 12.80 10.05
k 1.445 19.2 13).35 10.30
1.430 iar) 1.28?
N XV ¢ sas le 16.4 12.70 10.10
e 557 1723 to 10.30
1.537 16.9 1.30?
N XVI a 1.619 WZ 13.50 10.20
g 1.632 16.8 13.45 9.7
e 1.636 15.9 13.55 10.00
1.629 16.6 1.35?
N XVIle 1.710 18.8 13.70 10.40
g e721 18.7 13.40 10.20
a 1.738 16.8 13.60 10.40
c 1.788 20.1 14.20 11.00
1.739 18.6 eve
N XVIII ec 1.825 18.1 14.30 10.70
a 1.833 22.0 14.20 11.50
1.829 20.1 1.28?

CORRECTED
AREA
OF CORTEX

mm.
23.
24.
24.
24.

2S Wb or

bo
ou

we vw
: Sows a
MR OW0O &

8
~wN

oo
Se cia
0S

oo
bo
AN SO wv

bo
i.)
aowwma

100 NAOKI SUGITA

TABLE 8—Continued

C ORRECTION-COEFFICIENT
OBSERVED CORRECTED
GROUP BRAIN WEIGHT AREA AREA
OF CORTEX L.F The same OF CORTEX
on fresh brain on slide
“ grams mm.? mm. : mm. mm.2
N XIX b 1.962 19.9 14.70 TL 4s) 34.1.
a 1.981 19.5 14.40 11.00 3520
1.972 ORT ihaesike2 33.8
N XX ¢ 2.015 20.6 14.55 11.30 34.2
a 2.089 20.7 14.95 11.80 33.3
2.052 20.7 1.28? 8358
N XXI ¢g 2.156 21.1 N55 11s) 11.90 34.2
d PR MC 20.2 15.30 | 11.50 35.7
2.172 20 .7 1.307 35.0
N XXII
N XXIII a 2.345 22.4 14.50 11550 Bian
2.3845 22.4 1.267 85.7

N. The area of the cortex in the sagittal section. Norway rat
compared with the Albino

Table 11 shows the relations between the cortical area in the
sagittal section and the longitudinal diameter of the cerebrum
(L. Ff). Column B gives the average brain weight by groups,
column C the average area of the cortex in the sagittal section,
column D the average cortical thickness in the sagittal section
(7), column F the longitudinal diameter of the cerebrum (L. F),
all of these being the corrected values. In column FE the value
C'/D or relative length of the long side, when the cortical area
-was reduced to a rectangle with the short side equal to the cor-
tical thickness, appears. As shown in column G as E/F. these
computed lengths show similar ratios when divided by the actual
diameters L.F (column F), that is, 1.16 to 1.24 or on the average
1.20 for Groups N XI-N XXIII, but 1.19 for Groups N XIII-
N XX. If necessary, therefore, the cortical area in the sagittal

~

GROWTH OF THE CEREBRAL CORTEX 101

TABLE 9

Showing the observed and corrected values of the area of the cerebral cortex and of
the total section in the frontal section and the percentage of the cortical area in the
total frontal section of the Norway rat brain, accompanied by the data for the
correction-coeficient in the individual cases and the correction-coefficient for the
group. W. Dis the frontal diameter of the cerebrum,

OBSERVED Beer aa CORRECTED epee
GROUP BRAIN CORTICAL
Nae Area of | W.D The Arena) reno
A f : Area of
corter | ttt, | “brain | mS” | cortex | sce, | szcri0N
grams 4 mm. mm,2 mm. mm. mm .* mm 2 per cent
INEXGIG bos led 13.8 28.1 13.00 10.00 | 23.4 47.5 49
a 1.160 12.8 27.9 12.70 9.80 21.5 47.0 46
1 1-175 10.9 23.6 12.50 8.80 | 22.1 47.7 |« 46
1.163 12.5 26.5 1.34? 22.3 47 4 47
N XII
N XIIla) 1.369 307 27.9 13.00 9.80 24.2 49.2 49
L869 13.7 27.9 Meo" 24.2 49.2 49
N XIV b]| 1.407 14.0} 27.8 13.05 9.50! | 26.5 52.7 £0
g| 1.429 14.0} 28.5 13.20 S)eai0) PAY Al 55.0 49
a 1.431 14.6 30.4 12.85 10.20 23.2 48.4 48
1 1.431 14.9 29.6 13.40 10.30 25.3 50.2 50
e 1.437 12.6 28.7 13'.25 9.60 24.1 54.1 44
ke 1445 13-2 28.4 13.30 9.50 26.0 05.8 47
1.480 13.9 28.9 1.35? 25 4 52.7 48
NXVe aly 13.0) 29.0 13.20 9.60 24.7 55.0 45
e il aay WA, 20.0 13.50 9,20 27.4 55.4 49
a| 1.564 14.1 29.0 13.50 | 9.80 |, 26.8 55.0 49
1.546 13.3 27.9 1.40? 26.3 55.1 48
N XVI a| 1.619 14 oles 13.80 10.50°| 25.4 54.2 47
g 1.632 13.8 27.6 13.70 9.50 28.8 57.6 50
e 1.636 13.2 | 28.2 13.80 GHGON 2% Se gaen2 47
1.629 13.9 29.0 1.40° 27.2 56.7 48
NXVile 1.710 13.4 | 29.5 13.80 970) 27-2 59.8 44
g 1.721 15.7 32.1 13.60 10.10 28.5 58.4 49
a| 1.738 I5s2)) y3d520| ello 10.60 | 27.0 98.8 46
c 1.788 15.0 | 30.7 13.95 10.10 | 28.6 58.6 49
LUE) LS) Sl 12ol 27.8 58.9 47

102 NAOKI SUGITA

TABLE 9—Continued

CORRECTION- PERCENT-

OBSERVED c TED
COEFFICIENT | DIS AGE OF
AIN
GROUP | erat ; ; | ek
Areniat Area of | W.D The Agoavot Area of DA,
cortex total in fresh same on cortex total nanos
i section brain slide ; section =

grams mm. mm 2 mm. mm. mm.2 mm .2 per cent

IN PXGVA CH S25) | or Os| i S2eon |e leeA Dae lORSON i =e2956 63.7 47
BY || dbase || EON, S.74 less) || ALL AAD ADS 61.0 49

1.829 | 17.0 | 35.8 1.32? 29.6 62.4 48

N XIX b)| 1.962) 166) 36.6) 14:60 11.20) 2873 62.3 44
a| 1.981 15.3 | 32.9 | 18.95 10.30 | 28.1 60.5 47

LOTSA Pe LOLOR S48 Uk 33)" 28.2 61.4 46

NXXe| 2.015 | 14.6] 38.1 14.30} 10.20) 28.7 65.2 44
a |) 2.089 |" 1527 | 35-5) || 14250" 10595) 2726 62.3 44

2.052 | 15.2| 34.3 1.36? 28.2 63.8 44

Ni XOX gi) 022156) oie 35.2 1A Coy) LOE AON 28.0 67.0 43
ds| 2-187, |) 15c3F | 3460 15.05 | 10.70 | 30.3 67 .4 45

2.172 | 15.2 | 34.6 il Gh 29.5 67.2 44

\

section may be calculated by the following formula, in which
T., denotes the average cortical thickness in the sagittal section.

Ee EEX TS 20 (L. F and 7’, in millimeters)

The corresponding coefficient was found to be 1.22 in the
Albino brains weighing more than 0.5 gram (table 4), but 1.20
for brains weighing more than 1.3 grams (Groups XIII-XX).
The coefficients in the two forms may therefore be considered
similar, that for the Albino being a trifle the larger.

If comparison is made between the absolute values of the cor-
tical areas in the sagittal sections of the Norway and the Albino
brains of like weight, no great difference appears (table 12). In
the pair of Groups N XI and XI, the Norway is 10 per cent
smaller in the area. This may be explained by the fact that the
Norway brain weighing 1.16 grams is in a younger stage of cor-
tical development, as compared with the Albino brain of like
weight, the cortex of which is already provided with nearly all
its nerve elements. But, in the pairs of Groups N XIII-XIII

GROWTH OF THE CEREBRAL CORTEX 1038

TABLE 10
Giving for each individual and for each brain weight group the number of nerve
cells in 0.001 mm.* of the cerebral cortex, in the lamina pyramidalis and in the
lamina ganglionaris, and also the number of the ganglion cells only in the same
volume of the lamina ganglionaris, counted at locality VII in the frontal section,
as shown in fig. 2. Norway rat

CORRECIION- NUMBER OF CELLS IN A VOLUME OF CORTEX,
COEFFICIENT 0.001 mM.3
GROUP etal W.D Lam. pyramid. Lam. ganglion. Sanit
in fresh ee e
eens Ob-_ | Cor- | oOb- | ‘Gor | Ob-. | Cor-
served | rected | served | rected | served | rected
grams mune. mum.
N XI b| 1.155 | 13.00 | 10.00 253 115 170 78 44 20
a | 1.160 | 12.70 | 9.80) 242 itil 164 76 41 19
Vole el 2eo0 8.80 271 95 199 69 48 17
1.163 (1/1.34)8 255 107 178 74 44 19
N XII
N XIII a | 1.369 |.13.00 | 9.80 25 96 164 70 45 19
1.369 (1/1.33)8 225 96 164 70 45 19
N XIV b} 1.407 | 13.05 | 9.50} 248 94 174 67 46 18
CN IEA2OE | al3R20) | e9e50) |) 227 85 176 65 48 18
a | 1-431 | 12.85 | 10.20) 200 100 142 Al 40 20
AS ets. 400) 10L30 222 101 175 79 47 PA
e | 1.4387 | 13.25 9.60 225 86 165 63 49 19
Ne} Tees |) Ts3e8%o) 9.50 230 84 178 65 51 19
1.430 (1/1 .35)8 225 92 168 68 47 19
NEXSVica Ie a7 |, 1320) | 9/60) |) 285 90 169 65 52 20
e | 1.557 | 13.50 | 9.20) 250 79 176 56 58 18
a | 1.564 | 13.50] 9.80] 208 79 166 63 55 21
1.546 (1/1.40)8 231 8&3 170 61 55 20
N XVI a | 1.619 | 13.80) | 10.50 | 203 90 143 63 50 22
CAA GS2 a leloncON| mos 00) e250 78 159 56 60 20
ev IE6SGe|P1aesOe|- 9260!) 2 GZ 164 55 57 19
1.629 (1/1 .40)* 217 80 155 58 56 20
NEXAFS ego iets s80n) 92700) 23 74 155 54 58 20
g/l 721 | 13.60 | 10.10 182 75 147 60 54 22
a | 1.738 | 14.10 | 10.60 190 81 ail 56 54 23
Cole (SSe lsh oom el Oat 192 73 142 54 53 20
1.739 | (1/1.87)8 194 NGA 144 56 | 55 | 21

104 NAOKI SUGITA

TABLE 10—Continued

CORRECTION- NUMBER OF CELLS IN A VOLUME OF CORTEX,
COEFFICIENT 0.001 mo.3
~ KERN SEE ae W.D eae Lam. pyramid. Lam. ganglion. ee
in fresh | on slide
brain . ~
Ob- Cor! | Ob=” |) “Gere ope) cor
served rected | served rected | served | rected
grams mm. mm. ; |
Ni XaVildiee | 1.825) | 14.45") 10:30.) 200) 1" “73 146) |) 53 ras) 20
ay | alse) ||) shy} nS 220) 147 76 ta 59 42 22
15829 @/12732)i8 174 70. 130 56 49 21
|
N XIX b| 1.962 | 14.60 | 11.20 164 74 120 | 54 45 20
a | 1.981 | 13.95 | 10.30 176 71 134) 54 48 19
1.972 (1/1.33)8 TO ale es LOR oN ere Wy 20
N XX c¢ } 2.015 | 14.30 | 10.20 189 69 140 | 51 49 18
a | 2.089 |} 14.50 | 10.95 170 74 116 50 44 19
2.052 (1/1.36)3 180 72 128 51 47 19
N XXII g | 2.156 |} 14.75 | 10.70 180 69 118 45 45 leh
Gu 2atS8 7) loads 0s 70 186 67 120 43 46 17
2.172 (1/1.39)3 183 68 119 44 46 17

to N XX-XX the Norway shows a slight excess in the area;
on the average 2 per cent.

In spite of the fact that an adult Norway brain has a thicker
cortex (by about 6.7 per cent in the sagittal section) than the
Albino brain of the same weight, yet between the two a smaller
difference in the area of the cortex in the sagittal section is found,
because of the shorter longitudinal diameter of the cerebrum
(L. F) in the Norway (Sugita, °18).

O. The area of the cortex in the frontal section. Norway rat com-
pared with the Albino

Just as in the case of the sagittal section, table 13 shows rela-
tions between the cortical area in the frontal section and the
frontal diameter of the cerebrum (W. D). As a result, we see

é Cortical area
that the relative value C/D or ict aii higladiess stands almost
in a fixed ratio to the frontal diameter W. D, that is, from 0.94

GROWTH OF THE CEREBRAL CORTEX 105

TABLE 11

Showing relations between the cortical area in the sagittal section and the sagittal
diameter of the cerebrum (L. F). Colwmn E gives the relative lengths of the long
side when the area is reduced to.a rectangle with the short side equal to the cortical
thickness. These values have almost a fixed ratio to the sagittal diameter of the
cerebrum (L. F) in each group, the average being 1.20. For the explanation see
the text

A B Cc ED E E G
CORTICAL CORTICAL
BRAIN WEIGHT BRAIN AREA IN | THICKNESS Cc L.F E
GROUP WEIGHT SAGITTAL IN SAGITTAL D F
SECTION SECTION
grams m m2 mm. mm. mm.
N XI 1.163 24.0 1.61 14.9 Tee 22,
N XII
N XIII 1.369 Diao) 1783 15.9 eel 1LPAl
N XIV 1.430 29.2 1.84 15.9 13.2 1 all
N XV I 5RY/ 28 .4 1.82 15.6 (3e5 1.16
N XVI 1.629 30.5 1.88 16.2 13.6 1.19
N XVII 1.739 31.8 1.94 16.4 13.9 1.18
N XVIII 1.829 33.0 1.93 ffi 14.3 120
N XIX 1.972 33.8 1.97 Nie? 14.6 1.18
N XX 2.052 33.8 1.92 17.6 14.7 iL ile
N XXxI PD AN 35.0 1.99 17.6 15) sal sles
N XXII

N XXIII 2.345 30 1.86 19.2 15eo 1 2A:
Average (Groups) N XIN Xxexlil). 2.5. eae - Pe eee Hon a Ay 1.20
ACV ETA Mey (GO US IN ENOL MING EROXG) tate yi ncic ete eee eraih Gpetett coleoia a1 Se EN 1.19

to 1.00 or on the average 0.97 for Groups N XI-N XXI, so
that the cortical area in the frontal section may be obtained by
the following formula, in which 7’, denotes the average cortical
thickness in the frontal section:

Wa Dee TS COSGu (W. D and T;,, in millimeters)

For Groups N XIII-N XX, the coefficient is 0.98 (table 13).
The corresponding coefficient in the Albino, Groups XIII-XX,
is about 0.93, as shown in table 5. Comparing the absolute
values of the cortical area in the frontal sections in two forms of
like brain weight group (Groups N XIII-N XX to Groups
XIJI-XX), we find that in the Norway it is on the average
larger by about 10 per cent (table 12).

106 NAOKI SUGITA

TABLE 12
Comparison of the Norway rat brain with the Albino rat brain of like weight in the
areas of the cortex,in the sagittal and the frontal sections and in the area of the
total frontal section. The data were taken fram tables 1, 2, 8 and 9

Gene | sore ay AREA OF
Saar cioee 2 ae ar meu mRonraL [TON RCTION
Albino | Norway| Albino | Norway| Albino |Norway| Albino | Norway
grams | grams | mm. mm2 | mm? mm? mm.2 | mm.2
XI AL e638 2OeG e450 Mle S22R Si Ayden
XII 1.253 26.1 23.0 47.2
XIII 1.335| 1.869) 27.6.) 27.5 | 238.2 | 24:2 | 50.2 | 4922
XIV 1.445} 1.480) 28.2-| 29.2 | 24.8 | 25.4 | 52.3 | 52.7
XV 1.554 1.542) 28.7 | 28.4 | 24.3 | 26.3 | 54.0 | 55.1
xeViT 1.656) 1.629) 29.2 | 30.5 | 24.3 | 27.2 | 54.9 | 66.7
XVII 1.726) 1.789) 31.1 | 31.8 | 24.6 | 27.8 | 56.4 | 58.9
XVIII 1.839] 1.829) 32.8 | 33.0 | 26.0 | 29.6 | 58.9 | 62.4
XTX 1.924) 1.972) 32.3 | 33.8 | 24.8 | 28.2 | 57.0 | 61.4 .
xX 2.054) 2.052) 33.7 | 33.8 | 24.9| 28.2 | 63.4 | 68.8
xXXI 2.172 35.0 29.5 ; 67.2
XXII
XXIII 2.345 35.7
Average for Groups XIII-
RONEN cas oe hee 12692) 227695) 30.5437 (0) 2463 2727 95529 o7 25!

The total area of the frontal section is also slightly in favor
of the Norway (table 12).

P. Percentage of the area of the cortex to the votal area of the frontal
section (one hemicerebrum). Norway rat compared
with the Albino

As for the percentage of the cortical area to the total area of
the section, a comparison between the two forms is interesting.
In the Albino this percentage value increases from birth to a
brain weighing 0.7 to 1.2 grams when it attains the value of
about 48 per cent (table 2), but in the Norway the highest per-
centage is attained in brains weighing 1.1 to 1.8 grams. This
indicates that the cortical organization is more retarded in the
Norway, if the brain weight be taken as the basis of comparison.
In a fully mature Norway brain (from Group N XX onwards,

GROWTH OF THE CEREBRAL CORTEX 107

TABLE 13
Showing relations between the cortical area in the frontal section and the frontal
diameter of the cerebrum (W. D). Column E gives relative lengths of the long
side when the area is reduced to a rectangle with the short side equal to the cortical
thickness. These values have almost a fixed ratio to the frontal diameter of the
cerebrum (W. D) in each group, the average being 0.97. For the detailed expla-
nation see also the text. Norway rat

A B Cc D E F G
CORTICAL CORTICAL
BRAIN WEIGHT BRAIN AREA IN THICKNESS Cc W.D E
GROUP WEIGHT FRONTAL IN FRONTAL D F
SECTION SECTION
grams mm.2 mm. mm. mm,
N XI 1.163 22.3 1.88 11.9 12.7 0.94
N XII
N XIII 1.369 24.2 1.96 1263 13.0 0.95
N XIV 1.430 25.4 1.95 13.0 13.2 0.98
N XV 1.546 26.3 2.04 - 12.9 13.4 0.96
N XVI 1.629 Daz 2.08 1321 1324 0.96
N XVII 1.739 27.8 2.07 13.4 13.9 0.96
N XVIII 1.829 29.6 2.08 14.2 14.2 1.00
N XIX 1.972 28.2 2.00 14.1 14.3 0.99
N XX 2.052 28 .2 1.96 14.4 14.4 1.00
N XXI Qe Mi2 29.5 2.08 14.2 14.9 0.95
Atyieramen (GOU pS) Niece INNCNOI) erates ee ctci= iets cccola Shasta tien) ses eee 0.97
Awerarem (Gro upsy Ne Scull INe XN) eran sce atinea so. cteriansacc acti 0.98

table 9) this percentage amounts to 44 per cent, which is equal
to that seen in the mature Albino brain (Groups XVI to XIX,
table 2), if we disregard one case of advanced age (Group XX).

Q. Number of cells in a unit volume of the cortex. Norway rat
compared with the Albino

Reviewing table 10 which gives separately the numbers of
nerve cells in the unit volume of 0.001 mm.’ of the lamina pyra-
midalis and the lamina ganglionaris at a fixed locality in the
frontal section of the cerebrum and counted by the same method
used for the Albino rat and comparing these numbers with those
in table 3 in part I, it is easily seen that, if the like brain weight
groups of the two forms are paired, the number of cells in the
unit volume of both layers is slightly lower in the Norway rat.

108 NAOKI SUGITA

These relations are shown in table 14. As for the number of the
ganglion cells only in the lamina ganglionaris, it is always lower
by 2 to 6 in the Norway and the highest figure (21) in the Nor-
way is seen in Groups N XVII and N XVIII, while in the
Albino the highest figure (25) is attained in Groups’ XIII and
XIV and again in Group XVII. In the Albino a temporary in-
crease of cell number in the lamina ganglionaris was seen in
Groups XIII and XIV, and in my Norway sections a similar
phenomenon is indicated in Groups N XVII and N XVIII.
Generally speaking, therefore, the cell density in the cerebral
cortex, as far as represented by my observations, is slightly

600 2S : :
Rees il | eam (ein eal ra
550 [eee SAEELO SI eX De Se a tea ee
[oo le "| a ee ee eed eee Tg |
500 - call ; = - .
| | | | | | | LWT!
450 | —— eS eee = oo ee
| | [a |
EN ee Ze alee
pate T | | Tree | | | | |
| Bue RSs aa CY oak ae gl
350 == Se | a. oa
zl ine ol ae a
500 aes T —— —
| | | | _L LW!
250 . 1 - — | +2
| | | Bee | | |
200} + === 4== ae a = ——+
ee ee |
150 oe ee a at
400 MTA real | AS ee al ELE DUE | Sahessnven |
ao phe ea He id
50 ae The = | = | = ~ | a eee =a (i
he tthe | Rea | |
rate | eee ee emer | ec eae Pas ie he
4 HL Pal aie) sh be SI EP Tie HSh= Gon Ss] AO Ree gms.

Chart 4 Showing the computed values for the cortical volume, the volume
of the cerebrum, the cenn density in two unit volumes and the computed num-
ber of nerve cells in the entire cortex of the Norway rat, according to the brain
weight. This chart is equivalent to, but not directly comparable with chart 2,
which gives the similar data in the Albino in ratios of the values at birth.
«——* LWT’, The computed volume of the cerebral cortex, based on table 15.
------ LWH’, Therelative volume of the entire cerebrum, based on the data
presented in a former paper (Sugita, ’18) and given also in table 15. XX——XN’,
The cell density in two unit volumes of the cortex. Graph based on the data
given as N in column D, table 16. °—-—. eNLWT’, The computed number of
nerve cells in the entire cortex, based on the figures given in column E, table 16.
Mark X shows the phase in growth corresponding to that indicated by the same
mark in chart 2, which shows the end of the second developmental phase in the
Albino.

GROWTH OF THE CEREBRAL CORTEX

TABLE 14.

109

Comparison of the Norway rat brain with the albino rat brain of like weight for the
numbers of nerve cells in the lamina pyramidalis and in the lamina ganglionaris
and the number of ganglion cells only in the lamina ganglionaris, in a unit volume
of 0.001 mm.3, and also for N, which is the sum of the numbers in the lamina

The data were taken from tables

pyramidalis and in the lamina ganglionaris.

3 and 10
NUMBER OF CELLS IN A UNIT VOLUME N,
OF CORTEX, 0.001 mM.3 THE SUM OF
; NUMBERS
weit Ganglion ae aL ee os
BRAIN WEIGHT GROUP Lam. pyram.| Lam. gangl. | cells in lam. AND IN
gangl. LAM. GANG.
Al- Nor- | Al- Nor- | Al- | Nor- | Al- Nor- | Al- | Nor-
bino | way | bino | way | bino | way | bino | way | bino | way
grams| grams

Xai AES) AS 07 73 74 23 19 | 186 | 181

XID 1.253 108 68 23 171
SGUGL 1.335]1.369| 99 96 Ue 7 25 19 | 176 | 166
XIV 1.445}1.430| 94 92 71 68 25 19 | 165 | 160
XV 1.554|7.546| 87 83 62 61 23 20 | 149 | 144
Nevall 1.656|1.629) 84 80 60 58 24 20 | 144 | 138
XVII 1.726|1.739| 83 76 63 56 25 21 | 146 | 132
XVIII 1.839/1.829| 79 7 59 56 23 21 | 138° || 138i
XIX 1.92417.972| 81 73 51 54 24 20 | 1382 | 127
xx 2.054/2.052| 80 72 51 b1 20 He) | Mesh || aes
XxI 2.172 68 44 iG 112

Average for Groups

OTIS XOX eee nants 1.692:1.695| 86 81 62 | 60 24) 20] 148 | 140

lower in the Norway rat, if the brain weight be selected as a

standard of comparison.
R. The computed volume of the entire cerebral coriex. Norway rat
compared with the Albino

The computed volume of the cerebral cortex for the Norway
may also be obtained and expressed in values comparable among
themselves, by the use of the formula: L. F x W.D x T (where
T’ denotes the mean thickness of the cortices in the sagittal and
the frontal sections), as already explained in detail in part I
(see p. 82). But for a comparison between the cortical volumes
of the Norway and of the Albino brains, the direct comparison

THE JOURNAL OF COMPARATIVE NEUROLOGY, VOL. 29, NO. 2

110 NAOKI SUGITA

of the values obtained by the above formulas is not allowable,
since, comparing the areas in the Albino among themselves, the
fixed coefficients? 1.21 and 0.98 were eliminated from the for-
mula, as already stated, and similarly in the Norway the corre-
sponding coefficients’? 1.19 and 0.98 were also eliminated from
the formula. In order to compare the areas in these two forms,
the coefficients must be taken into consideration. As the product
1.19 x 0.98 is higher by 3.6 per cent than the product 1.21 x 0.93,
the value of L. F x W.D x T for the Norway should be raised by
3.6 per cent to be directly comparable with the value of L. F x
:
W..D Xf for the Albino: ~The’ ratio Pages oe (= 1.036)
121093 te
being represented by C, the comparable value of the cortical
volume for the Norway may be obtained by the corrected formula
as follows:
EA X Vie Dax Se € (C1803)

Table 15 gives the computed cortical volume of the Norway
brain, obtained according to the above corrected formula, and
this is shown graphically in chart 4 (graph LWT’).

As the available data in the Norway do not extend to the
earlier ages, I could not determine the early increase in the
cortical volume of the Norway, but our data show that the cortical
volume is increasing somewhat more rapidly during the period
when the brain weight is increasing from 1.16 to 1.54 grams and
after that it increases more slowly but steadily as the entire
cerebral volume increases, as shown in table 15 and in chart 4
(graph LWH’). In the Albino, as has been shown, the cortical
volume increases relatively rapidly until the brain attains 1.17
grams in weight, a phase which probably corresponds to the
phase in the Norway of 1.48 grams in brain weight.

To compare the cortical volume in the Norway rat with that
of the Albino, I have paired, in table 15, the Norway data
(L.F x W.D x T x C) directly with the corresponding Albino

° For a proper comparison, the coefficients here used are those for the same
brain weight groups compared in both forms, being respectively the averages
for Groups XIII to XX and for Groups N XIII to N XX, taken from tables 4,
5, 11 and 13.

GROWTH OF THE CEREBRAL CORTEX sab

TABLE 15

Showing the computed volume for the entire cerebral cortex of the Norway rat brain,
calculated by the formula: L.F X W. DX TX C for each brain weight group,
C being a fixed coefficient used to convert the computed volume of the Norway
cortex so as to make it comparable with that of the Albino (C = 1.036). The
computed volume of the cerebrum is quoted from my previous presentation (Sugita,
718). These values are paired with the corresponding values for the cortical
volume of the Albino and the ratios between them calculated

NORWAY RATS ALBINO RATS
A B G | D E F G H I

; ; Corre-

sponding Ratio
Computed L. I’ & |ecomputed | of cortical
; f ; volume LF W.D flee W. DXT| volume volume
Brain weight) Brain of ; tr 7 smireaet average KIC of the of the
group weight cerebrum a Ares ; GE inesh cortical |Computed| Albino Norway
ES Ga yea open thickness | volume | cortex, of | to that of
W.DXHt. of cortex | the same the

group Albino

number

grams mm. mm. mm. mm. mm 3 mm .3
N XI 1.1638 156 12.2 PAA 1S 281.00 | 288.93 0.973

N XII 304.51
N XIII 1.369 182 Sel 13.0 1.85 326.51 | 314.03 1.040
N XIV 1.480 185 1S )2 133,73 1.90 343.09 | 329.71 1.040
N XV 1 BY 194 13.5 13.4 1.93 361.83 | 345.86 1.046
N XVI 1.629 203 13.6 1133-7 1.98 382.32 | 359.30 1.064
N XVII 1739 218 13.9 13.9 2.01 402.47 | 365.08 1.102
N XVIII 1.829 226 14.3 14.2 2.01 | 423.00 | 397.96 1.063
N XIX 1.972 241 14.6 14,3° ‘|| 1299 430.57 | 390.39 1.1038
N XX 2.052 249 14.7 14.4 1.94 425.59 | 393.15 1.083

N XXI MsMG 2645) 15 14.9 2.04 475.66

Aer amen (GOW Ss) NjeXGlolIESINi BNOXN@ ene es ee 386.92 | 361.94 1.069

1'T, here entered, is the mean value of Ts and T,, previously given in tables
11 and 13 and is not the general average thickness of the cortex of the sagittal,
frontal and horizontal sections formerly presented in my fourth paper in this
series (Sugita, 718 a).

data (L. F x W. D x T) according to the brain weight groups,
quoted from part I. In table 15 the ratios show the volume of
the cortex in the Norway to be greater (1.040 to 1.103) in all the
comparisons for brain weights above Groups XIII (brain weight
1.37 grams). The average value is about 1.07. In Group XI
(brain weight 1.17 grams), the ratio for the Norway is less than 1.
At this weight the Norway brain is regarded as less mature than

1 NAOKI SUGITA

the corresponding Albino brain. The ratio tends to increase as
the brain weight increases, showing roughly the relative growth
in the Norway cortex.

Since, as has been shown (Sugita, 718 a), the cortex in the
mature Norway is about 8 per cent thicker (average of the sagittal
and frontal sections) than in the Albino, and since this value
enters as 7’ into the formula under discussion, this would tend
to give a greater volume of the cortex in the Norway than in the
Albino. The mean value found for the ratio of the cortical
volume—1.07—is about that to be expected, in view of the
relatively smaller value of L. F in the Norway.

S. Computed number of nerve cells in the entire cortex. Norway
rat compared with the Albino

As described in part I, the computed number of nerve cells
in the entire cerebral cortex may be obtained by the following
formula :°
NCEE XW. DX XC GE. FW. D and 71m millimeters)
where L. F X W. DX T XC is the computed volume of the
Norway cortex made comparable directly with the correspond-
ing volume for the Albino, as explained in the foregoing chapter,
and N is the cell density, represented by the sum of the num-
bers of cells in a unit volume in the lamina pyramidalis and in a
unit volume in the lamina ganglionaris (two unit volumes alto-
gether), given separately in table 10 and combined in table 16.

Table 16 gives the computed value of the cell number in the
entire cerebral cortex for each brain weight group of the Norway
rats (column FE), calculated by the use of the above formula,
and also in the corresponding case of the Albino (column G).

On examining table 16, column H, we find the computed num-
ber of nerve cells in the cortex to be nearly completed in a brain
weighing 1.37 grams (Group N XIII), while in the Albino this
condition was reached in a brain weighing 1.17 grams (Group
XI). The value of the completed cell number is indicated in

6 The formula for the total number of nerve cells in the Norway cortex is
like that for the Albino cortex with the addition of the factor C (footnote 4).

GROWTH OF THE CEREBRAL CORTEX ig [Ss

TABLE 16

Giving the computed number of nerve cells in the entire cerebral cortex of the Nor-
way rat brain, obtained on the basis of the measurements given in this series of
studies. These values are made to be comparable with the corresponding values
of the computed number of nerve cells in the cortex of the albino rat brains of
like brain weight groups

NORWAY RATS ALBINO RATS

A B Cc D E F G
Sum of aD Computed ll : Corresponding
mber of cells
| Computed | Meello | entire. "| numberof |, omUeM
Brain weight Brain weight artes in Jam. pyr. cortex,! cells in fetes ; e
group FXW. p|_2ndJam. NXE. | the Nowray, |) apis of the
TC | gang. in two xD xe to that = or
GES unit cy + {in the Albino Sale Sroun,
volumes, NV CX 100 pumabek
grams mm 3
N XI 1.163 281.00 181 508 .6 0.946 537.4
N XII ; o20au
N XIII 1.369 326.51 166 542.0 0.981 5P4 71
N XIV 1.480 348 .09 160 548.9 1.009 544.0
N XV oS 361.83 144 521.0 1.011 o15.3
N XVI 1.629 382.32 138 527.6 1.020 517.4
N XVII 1.739 402.47 132 doles 0.997 533.0
N XVIII 1.829 423 .00 131 554.1 1.009 549.2
N XIX 1.972 430.57 127 546.8 1.061 S15RS
N XX 2.052 425 .59 123 92520 1.016 515.0
N XXI PAS LP 475.66 MP SB VAaU/
Average (Groups N XIII-N XX)........ 536.9 TRO 530.2

1 As remarked in a note to table 7, the number given in this column corre-
sponds to 1/100 of N X L. F X W. D X T, or 1/50,000 of the actual number of
cells contained in the computed volume of the cortex.

the Norway by about 537 (the average of Groups N XIII-
N XX) or about 1 per cent more than that of the Albino, which
has been indicated by about 530 (the average of Groups XIII-—
XX, see table 7), so that the number of nerve cells in the entire
cortex of the mature Norway and of the Albino rats may be re-
garded as practically the same, as suggested by Donaldson
(Donaldson and Hatai, 711).

114 NAOKI SUGITA

IX. CONCLUSIONS

Putting together the foregoing observations, we come to the
conclusion that in the case of the Norway rat brain the entire
volume of the cerebral cortex is actively increasing up to a
brain weight of something more than 1.43 grams (Group N XIV)
and that the number of nerve cells in the cortex is completed in
a brain weighing something less than 1.43 grams (Group N XIV)
(chart 4). After this, the increase in cortical volume keeps
pace with the enlargement of the entire cerebrum, showing that
the cortical mass and the remainder of the cerebrum are growing
at the same rate. So, the end of the short period during which
the brain has attained 1.37 to 1.54 grams in weight (Groups
N XIII to N XV) marks an epoch in' the development of the
cerebral cortex of the Norway rat, at which the structural com-
pletion of the cortex has been acquired and the full prepara-
tion for the functional education has been established. This
period corresponds approximately to the age of twenty days.

In the Albino, the same degree of development is ‘reached
when the brain attains a weight of 1.17 grams or is twenty days
old. As I suggested in an earlier paper (Sugita, ’18 a), a Nor-
way brain corresponds in the development of the cortex to an
Albino brain weighing about 18 per cent: less. This assumption
has held true in the present examinations of the cortical volume
and cell number, because an Albino brain weighing 1.17 grams
just corresponds to a Norway brain weighing 1.43 grams.

The number of cells in the Norway cortex has been shown to
be but slightly (1 per cent) different from that in the Albino rat
cortex and may be regarded as the same in both forms. This
fact justifies at the same time a conclusion reached by Donald-
son in his former comparison of the Norway with the Albino rats,
that the greater weight of the brain in the Norway rat, compared
with the Albino of the same body weight or of the same age, is
probably due to an enlargement of the constituent neurons rather
than to an increase in their number (Donaldson and Hatai, ’11).
The results of my study regarding the cell size in the cortex in
these two forms will be discussed in a forthcoming paper and
will support the statement just made.

GROWTH OF THE CEREBRAL CORTEX Je
X. SUMMARY

1. On the sagittal and the frontal sections from 28 Norway
rats, whose brain weights fall between 1.1 and 2.4 grams and
which were formerly used for the investigation on the cortical
thickness (Sugita, 718 a), the area of the cortex was measured
and the number of nerve cells, in a unit volume of 0.001 mm.* at
a fixed locality of the cortex, was counted. These values were
all later corrected to the corresponding values in the fresh con-
dition of the material, using the correction-coefficients devised
for this purpose. These results have been grouped and aver-
aged according to the brain weight and then compared with the
corresponding data in the Albino, which were presented in part I
of this paper.

2. The actual area of the cortex in the sagittal section may
be obtained by the formula: L. F x T, x 1.20 (L. F and T,, in
millimeters), where L. F is the longitudinal diameter of the
cerebrum, 7’, is the thickness of the cortex in the sagittal sec-
tion and 1.20 is a constant coefficient which was empirically
determined (table 11, column G).

3. The actual area of the cortex in the frontal section may be
obtained, though less precisely, by the formula: W. D x T,, x 0.97
(W. D and T,, in millimeters), where W. D is the frontal diameter
of the cerebrum, 7’, is the thickness of the cortex in the frontal
section and 0.97 is a constant coefficient which was determined
empirically (table 12, column G).

4. The percentage of the cortical area to the area of the whole
frontal section is highest (48 per cent) in brains weighing 1.1 to
1.8 grams. In a fully mature brain it has fallen to 44 per cent.

5. The computed value for the volume of the entire cortex,
mcdicated by theformula:b. F x W.DxT xC df, W.D
and 7, in millimeters), where L. F is the longitudinal diameter,
W. D is the frontal diameter of the cerebrum, 7’ is the average
thickness of the cortex in the two sections and C a theoretically
determined coefficient necessary to make the values directly
comparable with the corresponding values for the albino rat,
shows that the cortex is increasing relatively rapidly in the

116 NAOKI SUGITA

Norway brains weighing less than 1.483 grams. After that stage
its increase nearly keeps pace with the increase in the volume
of the entire cerebrum.

6. In Norway brains weighing from 1.1 to 2.2 grams, the cell
density or the number of nerve cells in a unit volume of the
lamina pyramidalis and the lamina ganglionaris, in a fixed lo-
cality of the cortex, decreases slowly but steadily as the brain
weight advances. It has proved slightly less than that in the
Albino (compare table 16, column D, with table 7, column C).
In the lamina ganglionaris the number of ganglion cells only in a
unit volume is at its highest in the brains weighing 1.7-1.8 grams
(table 14).

7. The value for the computed number of nerve cells in the
entire Norway cortex, indicated by the formula: N x L. F x
W.DxTxC (L. F, W. D and T, in millimeters), where N
is the number of cells in two unit volumes andl. F x W.D x
T x C is the computed volume of the cortex, shows that it is
almost completed in a brain weighing something more than — .37
grams.

8. Comparisons in respect of the above characters between
the Norway and the Albino brains of the like weight show that,
in the cortical areas in the sagittal and the frontal sections and
in the volume of the entire cortex, the Norway rat surpasses the
albino rat, but the number of cells as computed for the entire
cortex may be regarded as the same in both forms. We conclude
therefore that the difference in absolute brain weight between the
two forms is not correlated with a difference in the number of
nerve cells in the cerebral cortex. In a Norway brain weighing
1.4 to 1.5 grams, which corresponds to an Albino brain weighing
1.17 grams and is about twenty days in age, the elemental or-
ganization of the cerebral cortex in the Norway rat is considered
to be almost completed.

GROWTH OF THE CEREBRAL CORTEX Wye

LITERATURE CITED

ALLEN, Ezra 1912 The cessation of mitosis in the central nervous system of
the albino rat. Jour. Comp. Neur., vol. 22, no. 6.

Donatpson, H. H. 19 8 A comparison of the albino rat with man in respect
to the growth of the brain and of the spinal cord. Jour. Comp. Neur.
and Psychol., vol. 18, pp. 345-392.

1915 The Rat. Memoirs of The Wistar Institute of Anatomy and
Biology, no. 6.

Donatpson, H. H. and Harar, 8. 1911 A comparison of the Norway rat with
the albino rat in respect to body length, brain weight, spinal cord
weight and the percentage of water in both the brain and the spinal
cord. Jour. Comp. Neur., vol. 21, pp. 417-458.

Suerra, Naoxr 1917 Comparative studies on the growth of the cerebral cor-
tex. I. On the changes in the size and shape of the cerebrum during
the postnatal growth of the brain. Albino rat. Jour. Comp. Neur.,
vol. 28, no. 3. :

1917 a Comparative studies on the growth of the cerebral cortex.
II. On the increase in the thickness of the cerebral cortex during the
postnatal growth of the brain. Albino rat. Jour. Comp. Neur., vol.
28, no. 3.

1918 Comparative studies on the growth of the cerebral cortex. III.
On the size and shape of the cerebrum in the Norway rat (Mus nor-
vegicus) and a comparison of these with the corresponding characters
in the Albino rat. Jour. Comp. Neur., vol. 29, no. 1.

1918 a Comparative studies on the growth of the cerebral cortex.
IV. On the thickness of the cerebral cortex of the Norway rat (Mus
norvegicus) and a comparison of the same with the cortical thickness in
the Albino. Jour. Comp. Neur., vol. 29, no. 1.

i kes Pere a i

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AUTHOR’S ABSTRACT OF THIS PAPER ISSUED
BY THE BIBLIOGRAPHIC SERVICE, MARCH 2.

COMPARATIVE STUDIES ON THE GROWTH OF THE
CEREBRAL CORTEX

VI. PART I. ON THE INCREASE IN SIZE AND ON THE DEVELOP-
MENTAL CHANGES OF SOME NERVE CELLS IN THE CEREBRAL
CORTEX OF THE ALBINO RAT DURING THE GROWTH OF THE
BRAIN

VI. PART II. ON THE INCREASE IN SIZE OF SOME NERVE CELLS
IN THE CEREBRAL CORTEX OF THE. NORWAY RAT (MUS NOR-
VEGICUS), COMPARED WITH THE CORRESPONDING CHANGES
IN THE ALBINO RAT

NAOKI SUGITA

From the Wistar Institute of Anatomy and Biology

WITH SIX FIGURES AND FOUR CHARTS

PAR I
I. PRELIMINARY STUDIES

As a preliminary to the study of cell size, I made a comparison
of effects of several fixatives and imbedding media on the size and
shape of the cortical nerve cells in a small number of albino rats.
These studies were made after considering the results of King
(10) and Allen (16), both of whom were endeavoring to find
methods which caused the minimum alteration in the nerve cells.

For this comparison, ten kinds of preparations were made from
albino rat brains of like age: thus, as the fixative, (1) Bouin’s
fluid, (2) 4 per cent formaldehyde, (3) 95 per cent: alcohol, (4)
Miiller’s or Orth’s fluid, and (5) Ohlmacher’s fluid were suc-
cessively tried, and each sample was inbedded in (A) parafine
and in (B) celloidin.

119

120 NAOKI SUGITA

Formaldehyde fixation and paraffine imbedding (2A) causes
considerable shrunkage of nuclei and cell bodies, especially in
young brains, but material so prepared takes any aniline dye ex-
cellently well (fig. 1, 6). Fixation in Miller’s or Orth’s fluid and
paraffine imbedding (4A) eauses also shrinkage and deformation
of the cell bodies and nuclei, the contours of which become zigzag.
Formaldehyde fixation and celloidin imbedding (2B) give good
figures of cell bodies, which stain excellently with any aniline
dye. The shrinkage of cells and nuclei which was seen after
paraffine imbedding of the material similarly fixed (2A) is no
longer observed. But the size of cell bodies and nuclei seems to
have suffered some diminution. Miller or Orth fixation and
celloidin imbedding (4B) causes considerable deformation of the
contours of the cells and nuclei, which is probably an affect of the
potassium bichromate.

In material fixed in 95 per cent alcohol, the brain is subject to
much shrinkage, and consequently the cell size and cortical
thickness diminish also, though, after paraffine imbedding (3A),
the contours of cells and nuclei are preserved pretty well (fig. 1,°
a). Aleohol fixation only or alcohol fixation and celloidin im-
bedding (3B) is ideal for the study of the cytoplasmic structure as
originally emphasized by Nissl. The cell bodies stain very well
with aniline dyes, but the section shrinks so that the individual
cells must have been more or less reduced in size. Fixation in
Ohlmacher’s fluid and paraffine imbedding (5A) or celloidin im-
bedding (5B) proved to be most excellent for cell study, as
pointed out by King (10), but it is followed after fixation by a
considerable reduction in the volume of the total brain and some
change in shape.

After a number of tests, I decided to use as the fixative Bouin’s
fluid, which is composed of:

Picrieracid-esaturabedsagueousisOlmblone ath eenanr sete neers 75
40pericent formaldehyde (formalin). eee cmeeel ke bioeeeneecee 25
Glacialvacetiesacidis sae lt tthe, 3. ces tue Se ote ad Oe leet ee Tae eG 5

Fixed in this fluid the total weight or volume of the brain
suffers no significant change after complete fixation and preserves
its original shape quite well, though a slight shrinkage occurs,

GROWTH OF THE CEREBRAL CORTEX AL

no matter what the age of the brain is. It takes only a couple
of hours to complete fixation in this fluid, if the fluid is kept in
the oven at 37°C., but, as a matter of convenience, I left each
brain in 20 ee. of this fluid for 24 hours at the room temperature.
By this treatment the form of the cells was well preserved, even
after imbedding in paraffine (1A) (figs. 3 and 4).

Comparing this with the material which was fixed in the same
fluid but imbedded in ecelloidin (1B), the contours of cell bodies
were, in the former, somewhat indistinct and the size of the
nuclei somewhat larger (fig. 1, ¢). But after paraffine imbedding
the nuclei have yet good contours which are not zigzag and the

Fig. 1 Showing pyramids from the lamina pyramidalis at a fixed locality
(locality VII) of the cerebral cortex of Albino brains weighing 1.3 to 1.5 grams.
Magnification of about 950 diameters, measured directly on the slide. a = from
a brain imbedded in paraffine after fixation in 95 per cent alcohol. b = from a
brain imbedded in paraffine after fixation in 4 per cent formaldehyde. c = from
a brain imbedded in celloidin after fixation in Bouin’s fluid.
so-called Nissl bodies are also well stained. Since paraffine was
used exclusively for the imbedding medium, Bouin’s fluid proved
to be the best fixative for the albino rat brain, when it is re-
quired to follow the growth changes of the cortex by the measure-
ments of the cells of the cortex.

Figure 1 shows a comparison of the effects of several fixatives
on the shape and contours of the cell bodies and the nuclei when
applied to albino rat brains of like age. The examples are all
from Albino brains weighing 1.3 to 1.5 grams and represent
pyramids in the lamina pyramidalis taken near the locality VII
in frontal sections, being comparable with VII in figure 2, a
and b.

22s NAOKI SUGITA

II. MATERIAL

For the present study on cell size in the cerebral cortex, the
frontal and horizontal sections of the Albino brains which were
used earlier for studies on the cortical thickness, cortical areas,
and cell density (Sugita, ’17 a, ’18b) were alone taken. No
locality in the sagittal sections was examined. ‘These sections
were from 128 individuals, sexes combined. The data for these
128 rats appear in tables 1 and 2 in a previous paper (Sugita,
17 a) and it is not thought necessary to repeat the tables here.
This study was begun in January, 1916, and carried on with in-
terruptions till February, 1917, at The Wistar Institute of
Anatomy and Biology.

a. F b
We
H Xe H’
a
F’

Fig. 2 Showing on the brain surface the localities at which the sizes of the
pyramids and the ganglion cells were measured. FF’ indicates the level from
which the frontal section was taken and HH’ indicates the level from which
the horizontal section was taken. VII = locality VII; X = locality X. a = the
dorsal view of an Albino brain weighing 1.5 grams. Enlarged 1.8 diameters.
b = the lateral view of the same.

Ill. TECHNIQUE

The nerve cells have been measured at fixed localities in the
sections; that is, in the frontal sections at locality VII (fig. 4,
Sugita, 717 a) and in the horizontal sections at locality X (fig. 6,
Sugita, 717 a). For convenience, these localities are here shown
on two corresponding figures (fig. 2, a and 6). From the lamina
pyramidalis and the lamina ganglionaris at each of these locali-
ties, ten of the largest cells were selected and measured. The
cells in the other layers were not systematically investigated,

GROWTH OF THE CEREBRAL CORTEX 123

but in several stages of growth, a few were measured, in order
to be able to make some comparisons.

The study of the cells under the microscope was made with a
Zeiss Comp. Ocular no. 6 with a micrometer, combined with the
objective 2 mm., oil immersion. Each division in the micrometer
scale was equal to two micra. The measurement of the cell
size was executed in the following way: the transverse diameter
of the cell body (the greatest width of the cell body) was meas-
ured on a line, parallel to the base line, which crossed about the
middle of the nucleus. For the longitudinal diameter the meas-
urement Was made vertical to the transverse diameter from the
base of the cell body to the beginning of the apical dendrite.
This last limit was assumed to be at the point where the Nissl
bodies are no more to be seen and the side lines of the apical
dendrite begin to run nearly parallel to each other. Sometimes
this upper limit was very hard to determine, especially in fully
grown cells, because of the irregularity of the cell outline and
the relatively slow transition from cell body to the apical den-
drite. In these latter cases, the upper limit Was somewhat arbi-
trarily fixed, but this procedure has apparently been without
much effect on the results.

The measurements of the ten largest cells of the same kind
from within the fixed locality in the same individual were then
averaged for each diameter and recorded on cards without any
correction. The average measurements from the frontal section
and the horizontal section are denoted in the records by the
letters F and H, respectively. The individual averages for each
series of ten cells in each section have all been tabulated and
the respective averages for the brain-weight groupsfound. The
values for the individuals in each brain-weight group are so
well correlated with their respective individual brain weights
that it has seemed necessary to publish only the averages for the
successive brain-weight groups. Table 1 contains the cell
measurements on the frontal section averaged for each brain-
weight group. The results of the measurements on the hori-
zontal sections, Which were taken from the other individuals,

124 NAOKI SUGITA

are given in table 2, and here also only the averages for the
brain-weight groups are given.!

The maximal diameters of the nuclei of the same cells were
measured in the two directions in which the cell measurements
were made. The nuclei have sharp contours, so that it Was al-
Ways easy to find the border points of the diameters. The re-
sults of the nuclear measurements have been treated in the same
manner as the cell-body measurements and the average values
are recorded also in the same way—without any correction—in
tables 1 and 2.

In table 3 the final average diameters of the cell bodies and
their nuclei for each brain-weight group are given for each sec-
tion. These final average values were obtained by multiplying
the values of the transverse and longitudinal diameters together
and by extracting the square root of the product, thus assuming
the cell- and nucleus-figures to form a plane instead of a solid
body. By this treatment, the results for the nucleus do not differ
much from those which would be obtained by using a planimeter,
because the nucleus has a nearly spherical or ellipsoidal form.
The cell body, on the contrary, appears as a somewhat irregular
cone or pyramid in the outline. Nevertheless, its relative vol-
ume may be denoted by a’b, or its area by ab, in which a is the
transverse and 6 the longitudinal diameter. Accordingly, the
relative values of the average diameter may be represented by
Vab, but these values should not be compared directly with
the average diameter of the nucleus, because the forms of the cell
body and of the nucleus are quite different. The size of cell
bodies and their nuclei was assumed to have shrunken in the
same proportion as the total brain volume during the procedure
of fixation, imbedding and mounting and the values observed
were therefore corrected for the fresh condition of the material
by the use of the correction-coefficient which was formerly used
for the correction of the cortical thickness or other measure-
ments made on the same section. The cell bodies and nuclei
Were assumed to have shrunken similarly in transverse and

‘The detailed data for tables 1 and 2 and also for tables 6 and 7 have all
been tabulated and are on file at The Wistar Institute of Anatomy and Biology.

GROWTH OF THE CEREBRAL CORTEX 15

TABLE 1
Giving the average uncorrected diameters of the nerve cells and their nuclei in the
lamina pyramidalis and the lamina ganglionaris measured at the fixed locality
(locality VII) on the frontal sections of the albino rat brain. The data are given
for each brain weight group only

LAMINA PYRAMIDALIS LAMINA GANGLIONARIS

BRAIN WEIGHT | NO. OF | BRAIN Cell body Nucleus Cell body Nucleus

GROGE SSS BS) | Weert iirdiameter diameter diameter diameter
Transv.| Longit.|/Transv.| Longit.)/Transv.| Longit. Transv.| Longit.

grams | mn a Lu LL Ke wel Bp
I 3 OPIGH Ie onl elOkd/ 6.6 7 OvLOP 1s ela Sa WlOlo
II (B) 5) O- 251 M1OFS) | =1320 PA) MO ses aS 2 |) PR) | SRG
WU 5 08353 POF Seon lO) 12.4) Gale le 2ORGn | Mlseon| el onO
IV 6 OFAS2 Ee ion |e tea NS: 5) | lise eel lemon meld a
V 9 OeS42 14 Aa S| 194, 134 19m |) 2274 1G Bok hg 4
VI 3 OF059 (SOR liad el 2aO Mie. 29) | OmAe esr ieel Ornelas
VII 2 ORO I Se2h Save isron 42) | 2ON2a 25r al Grlee al yn)
VIII 6 OFSAN IGE SOFAS TALON 1458) | 2028) 2627 | eli7e4 Ses
IX 3} OF964) 1659) 52082) 15o7 |) 1624) 21545) 2856) |) TOR 1Ok6
xX 3 12040 MGAG | e20 sy PP 4AsS: os. | ZION 2G elie alms
XI 4 Pe W628) |) 2065) 14a | W6E 1 | 215) |) 2864) 18s se e1or4
XII 2 1253 Geer lecOn Me man Gn mld: Ole 1s eee pel Se O Mae Sia
XIII 5 Te 3350l) 1680) 8208 (2) TANG a V5.2) 20°44) 26.8) lvesnl) Lse4
XIV 3 AAO lea E20 4S aS ot 20et 27 Onell lsies
XV 5 S54 S pon | 2OKOM MASS 21 Qn \e2ie4 elenOn ail snG
XVI 4 12656) 21520 TOUGH esas: | 14a 217 |) 291 |) Wea Toe:
XVII 4 O20 |S eig (ONO NA con elo, 2220) | 28 Onl l Saal One:
XVIII 8 1839) AS | 194s SG 145 2273) | 28:5 | Sear 1920
XTX 1 1.924) 15.6 | 19.9 | 14.0 | 14.3 | 22.7 | 29.3 | 18.8 | 19.4
XxX 2 ZnO D4 ae 2a LORS Soma 2os2uil) ole Anno on izle

1 The uncorrected measurements of the cell body and the nucleus of the
ganglion cells in these groups (Groups XII—-XIV) show a slight decrease, while
in the corrected measurements (see table 3) no diminution in cell size has oc-
curred in this stage. This slight decrease in size on the slide is probably due to
some chemical changes which takes place in cytoplasm during this phase of
development. The same phenomenon is to be seen also in the ganglion cells
measured on the horizontal section, given in table 2, in Groups XII-XVI.

longitudinal diameters and in the same proportion as the
width of the brain has shrunken. As in the other measure-
ments (Sugita, 717 a, ’18 a, 718 b), the correction-coefficient was

W. D in fresh brai :
based on irae. ad. for the frontal section and on

THE JOURNAL OF COMPARATIVE NEUROLOGY, VOL. 29, NO. 2

126 NAOKI SUGITA

TABLE 2

Giving the average uncorrected diameters of the nerve cells and their nuclei in the
lamina pyramidalis and the lamina ganglionaris measured at the fixed locality
(locality X) on the horizontal sections of the albino rat brain. The data are
given for each brain weight group only

=

LAMINA PYRAMIDALIS LAMINA GANGLIONARIS

BRAIN WEIGHT | NO. OF | BRAIN Cell body Nucleus Cell body Nucleus

GROUP CASES |WEIGHT diameter diameter diameter diameter
Transv.| Longit.|Transy.| Longit.|/Transv.| Longit.|Transv.| Longit.

grams u eg Lu Lu Mu uM Le Le
II (B) Ze O292\5 O29 Rr 8.5 9.8 | 15.4) 19.3 | 13.0 | 14.2
III 3 0.317) 10.6 | 138.8 9.4 | 10.9 | 14.6 | 19.0 | 12.7 | 14.4
IV 3 0.419) 18.0 | 14.0 | 10.2 | 12.9 | 16.0 | 21.4 | 14.2 | 16.3
V 5 OF546/S89 | MGr os 2 Fon Sr omits lle Zao | GROM learn
VI 2 e@esill) isysCy |) Tsoi} tesa) | SSD Pere | Pah |p iy | IS.
Vail 2 0.761) 15.6 | 18.5 | 14.3 | 15.7 | 19.4 | 24.9 | 17.6 | 19.0
Aang a OFS48 Seo TOR ae a 15 Sal eZO ne 26eSe Sele eon
IX 2 05939) 15-9) | 19.8) | 1458 | 1620) |) 20).9 928. 1) 188") T9k6
x 3 12054) GR 20267) MAO be 20 a 2S8ro ses ORS
XI 1 TIP) MG GS |) PAPA NW GS) |) AGG |) ADatoy | Bsiccs |e) |) ).@)
XII 3 1240/16 ON F202 55 | MAR toe OM Ora L277 Ss Ou
XIII 3 (Sol S298 P2089) | 146s a5 2053 e259 os eG mel ORO
XIV 2 (e455 eo A ZOE 1329) 4S OF 20s e2SeA selves tO ea
XV 2 ibesiota}) Taye) |) AO ecor i) LAO) |) eset AD) |) PRG) |) si a) 2:
XVI 4 IPC7S) M522) | PL9EO) | 1420 15.0) 20k e279 lie Sa aloes
SWAMI 2, Ie cek0)) sy |) ZOey i) WS es ab OS || 2EG Wiss 2) |) 1).
XVIII 2 S25 Moron ecO0eo) Ae Soleo len eee 2ORO sa Se4 LOR
xX 1 2.004) 14°67) 1953 | 1325 |) 1470) 2175) S70) |) Skane T9R6

1 See note on table 1.

W. B in fresh brain

W. B on the slide

rectly to the final average diameters for the cell bodies and the
nuclei. The corrected results, with the average correction-
coefficient for each brain-weight group, taken from previous
papers (Sugita, “17a, 718 b), are tabulated in table 3, accom-
panied with the averages of all the diameters in both sections
for each brain-weight group.

for the horizontal section, and applied di-

GROWTH OF THE CEREBRAL CORTEX 127

TABLE 3

Giving the corrected final average diameters of the nerve cells and their nuclei of the
lamina pyramidalis and the lamina ganglionaris measured on the frontal and the
horizontal sections of the albino rat brain. The average values of the two for
each brain weight group are also given. The correction-coefficient for each brain
weight group was taken from previous papers (Sugita, ’17 a, ?18b). F = the
frontal section. H = the horizontal section.

LAMINA PYRAMIDALIS LAMINA GANGLIONARIS
BRAIN WEIGHT BRAIN CORRECTION-
enone Nee teeee CURRIE NTS Gell body Nucleus Cell body Nucleus
diameter diameter diameter diameter
grams be K be i
1 JL 0.161 1.14 1053 8.1 13.6 10.9
HI = = = == = —
0.161 10.3 8.1 13.6 10.9
F II 0.251 1.16 135 12 18.8 14.8
Jel IGl 0.292 1.10 12° 3 10.0 18.9 15.0
(Birth) 0.272 12.9 10.6 18.9 14.9
F III 0.358 alts 15.4 13.0 20.6 16.0
ial N00 0.317 2 14.6 22 eal! 16.3
0.338 15.0 1256 20.4 Gree
FIV 0.432 110 24 14.2 22.8 17.9
HIV 0.419 1.30 UC 14.8 24.0 19.6
0.426 (sch 14.5 23.4 18.8
FV 0.542 1.138 17.9 14.6 24.2 19.0
Jal \¥% 0.546 eZ 18.5 15.9 25.6 20.4
0.544 18.2 15.3 24.9 19.7
F VI 0.639 1.19 19.4 16.0 25.4 19.9
EO Wil 0.631 1.24 20.4 18.0 26.8 21.9
0.635 19.9 17.0 26.1 20.9
F VII 0.750 1.24 21.0 17.2 28.2 20.5
H VII 0.761 Wee 21.6 19.0 28.0 Dae
0.756 21.3 18.1 88.1 21.9
F VIII 0.841 1.20 21.5 1533 28.3 21.4
H VIII 0.848 1.38 B33. 7/ 20.8 31.8 25.8
0.845 22.6 19.1 30.1 23.6
FIX 0.964 1 AA 22.4 19.4 29.9 23.4
HIxX 0.939 131 PB 74 20.2 31.7 PAD 24

(10 days) 0.952 22.8 19.8 30.8 24.8

28 NAOKI SUGITA

TABLE 3—Continued

——

LAMINA PYRAMIDALIS LAMINA GANGLIONARIS
BRAIN WEIGHT BRAIN CORRECTION-
SLIDERS NJOSRREA EH CSE ER GLaN ED ial Glel body Nucleus Cell body Nucleus
diameter diameter diameter diameter
grams a Me be Me
FX 1.040 112233 re) 18.6 29.6 22.4
H X 1.054 1.36 24.8 20.8 33.0 26.3
1.047 93.7 19.7 31.3 24.4
F XI 1} a7Al 1.26 23.4 19.4 31.4 23.8
H XI i Pal 1.26 PES Tf 20.4 31.0 24.6
(20 days) 1.146 ® 23.6 19.9 31.2 24.2
F XII e253 ial 24.0 19.6 31.6 24.0
H XII 1.240 1.36 24.6 20.0 old 25.9
1.247 94.3 20.3 Slate 24.5
F XIII 12335 1.29 23.4 19.2 30.2 23.4
H XIII isi 1.34 24.4 20.2 32.6 24.5
Tl GYAS) 23.9 Wf 31.4 24.0
F XIV 1.445 1.34 23.8 19.7 31.2 24.0
H XIV 1.455 1-31 22.8 18.9 ail 7 24.4
1.450 LBS 93 19.3 BES 24.2
| Oe. Of 1.554 1.30 22.9 18.9 31.4 23.8
TOG: 1.566 1.28 22.9 18.6 31.6 24.1
1.560 22.9 18.8 O20 24.0
F XVI 1.656 1.33 22.9 19.0 33.4 24.8
H XVI 1.678 iLe8Y7 23.0 19.2 31.4 24.4
1.667 DIA” 19.1 82.4 24.6
F XVII 1.726 1.26 D2 18.6 alee 24.1
H XVII 1.730 1.36 23.9 19.8 SP a/ 25.6
1.728 By il 19.2 38.0) 24.9
F XVIII 1.839 ilsey DP) 33 18.5 Sone 24.7
H XVIII 1.823 1.29 23.0 19.0 32.4 24.5
1 831 ea 18.8 BY2 ooh 24.6
F XIX 1.924 1.29 22.7 18.2 33.2 24.6
lel RODS — — — — — —
, 1.924 ERO, 18.2 BOue 24.6
F XX 2.054 1.23 Zee I 1 Sone 24.2
H XX 2.004 isi 22.0 17.9 33.8 24.9
2.029 BING: thot BORO) 24.6

GROWTH OF THE CEREBRAL CORTEX 129

IV. GROWTH IN THE DIAMETERS OF THE CELL BODY AND OF THE
NUCLEUS

Chart 1 shows graphically the data given in table 3. As ordi-
nates the average diameters of the cell body and of the nucleus
of the pyramids (lamina pyramidalis) and of the ganglion cells
(lamina ganglionaris) are plotted on the abscissa for the average
brain weights.

Diameter in micra

56 ean) ae 7 = T T T Sree 1 T —— SS
34 a | =| | | _— cal | i | — |
| | | | See
| | BE | pee eee GC
SZ eal nae | Ls ell | Y ee 1 xx = SS Atal aa lela
| | + |
30 | ia T —— Sanit 1 I T7 a aa ee aaa & a i _— To at cal + ——s
| | | | |
| a4) | | lees
28 a “i | t = = = = =
A (ot
26 pe —_ == se = | } i ee
a | |
| : | eo ee
24 sae ee ee Se Ee a oe sew t —— GN
r | | | eo a | | SSR | | |
: | | Vga en | ee 0 ec ee ee ee
22 A We ei Ea Ne Pe |e | | ae ies 3 a |
Tals | | | | 3
j Sole pai as ee | Pe
20 linemen Zax oe ye == areal ar SI ad ead ae |
is I a | | Uae | | pages oat ios ea
a | ee ] | |
| WA | | | | PN
16 = {——
7 Wa | | | T
Peed PEs
44 yes VA | 18 | | nal ji i >. |
| ]
6 He | | |
/ | |
12 7 = hia | 7 + ai t
A A |
° / | |
10 =I yr = 7 = = = = 1 =
y | |
8|_+ = = =r iba =
| |
6 a Ie a! £
4 =p | =|
| T + t + — —
Ba sa ' ! -
| | |

ol Je LL
O1 02B03 04 05 06

07 08 09 10

————
THI lioie 1 1 i Gi dif Seed OMe AO) gins

Chart 1 Showing the corrected average diameters of the cell body and the
nucleus of the cortical nerve cells of the albino rat, plotted according to in-
creasing brain weight. Based on the data in table 3. Graph GC, average diame-
ter of the cell body of the ganglion cells in the lamina ganglionaris. Graph GN,
average diameter of the nuclei of the ganglion cells in the lamina ganglionaris.
Graph PC, average diameter of the cell body of the pyramids in the lamina pyra-
midalis. Graph PN, average diameter of the nuclei of the pyramids in the
lamina pyramidalis. X,10daysof age. XX and *, 20 days of age. **, 30 days
of age.

130 NAOKI SUGITA

If the length of the average diameters represents relatively the
cube root of the volume of the cell body or of the nucleus, the
actual volume of them may be comparable among themselves
by the cube of the diameters. It is clearly seen from the chart
that the pyramids in the lamina pyramidalis of the Albino cortex
attain their maximum size in a brain weighing from 1.1 to 1.8
erams or 20 to 30 days in age, the curve showing the maximum
size in a brain weighing about 1.25 grams, and after that they
diminish slightly but steadily in size as the age (brain weight)
advances, while, on the other hand, the ganglion cells in the
lamina ganglionaris attain nearly their full size in a brain weigh-
ing about 0.95 gram or ten days in age; that is, earlier than the
pyramids, and after that slowly but steadily increase their size
as the brain weight increases. The nuclei in the pyramids and
in the ganglion cells change their sizes in much the same way
as the cell bodies to which they belong, the graphs for the cell
body and that for the nucleus for each kind of cell running nearly
similar courses (chart 1).

As shown in chart 1, the graphs suggest that both kinds of cells
increase in size very rapidly during the first ten days after birth,
and then the rate diminishes rather abruptly during the following
ten days (0.95 to 1.15 grams in brain weight) or more, at the
end of which phase the pyramids reach the maximum size,
after which they decrease slowly, while the ganglon cells still
continue to increase somewhat even after this phase.

On examining all the sections which I made, it was seen that
the ground tone of the sections uniformly stained with the
carbol-thionine has been gradually changing as the age of the
brain, from which the sections were taken, increases. In suc-
cessfully stained sections—even if stained by decoloration—of
brains from birth to those weighing less than 1.0 gram, the
ground tone is rather purple or violet, when viewed with the
naked eye by transmitted light. On the other hand, the sec-
tions from brains weighing more than 1.3 grams have a rather
distinetly blue tone. The intercellular tissue takes more easily
the pale blue color—owing to a less decoloration—in older
brains, while in younger brains the intercellular tissue remains

GROWTH OF THE CEREBRAL CORTEX igs)

quite unstained. The period during which the brain weight in-
creases from 1.1 to 1.3 grams coincides with a transitional phase
of the color. I regret that I have not been able to reproduce
these distinctions of color for the illustration of this paper.

These changes in color suggest that at the 20 to 30 day phase
some chemical changes in the structure of the cell body and the
nucleus have been occurring.’ At this phase of growth, the cells
having attained nearly the full size, the rate of increase in size
abruptly diminishes, suggesting that during this phase important
changes have occurred. Myelination is proceeding very actively
after the brain has attained the weight of 1.0 gram (Sugita, 717 a),
and the fact that the cell bodies and nuclei of the pyramids de-
crease in size as the brain weight passes 1.3 grams while the
growth of the cell body and of the nucleus of the ganglion cells
become very slow may have some connection with the myelin
formation.

Table 3 enables us to examine the measurements for the frontal
and for the horizontal sections separately. Generally speaking,
at the locality VII, measured in the frontal section (lines de-
noted by F in table 3) and at the locality X measured in the
horizontal section (see lines denoted by H in table 3), the cor-
rected sizes of the cell body and of the nucleus show some differ-
ences in the younger brains, but the sizes may be regarded on
the whole as practically the same in these two localities in
mature brains. If stated more minutely according to the data
presented in table 3, the pyramids and the ganglion cells at
locality VII (frontal section) grow in size somewhat more slowly
as compared with those at locality X (horizontal section), so
that in Groups IV to X the diameters are all smaller for the
frontal section than for the horizontal section, in averaged
values (see table 3). But if these slight discrepancies be not

2 As noticed in tables 1 and 2, the size of the ganglion cells directly meas-
ured on the slides shows a slight decrease during this phase (1.0 to 1.3 grams
in brain weight), while, in corrected measurements given in table 3, there can-
not be detected any diminution in cell size during the same phase. This de-
crease in size of the ganglion cells on the slide may have some connection with the
chemical changes occurring in the cytoplasm and karyoplasm, which cause
different reactions to the reagents used for fixation.

132 NAOKI SUGITA

taken too seriously, it may be stated that on the average the
cell bodies and the nuclei of the pyramids attain their maximum
size at about twenty-five days (brain weight, 1.25 grams) and
those of the ganglion cells attain nearly the full size at about ten
days of age (brain weight, 0.95 gram).

The largest ganglion cells (lamina ganglionaris) in the cerebral
cortex of the adult albino rat brain are found in the middle part
of the sagittal section, denoted by locality III (Sugita, 717 a).
The size of these largest cells at different ages was not syste-
matically investigated by me, but a careful comparison of them
with the ganglion cells at localities VII and X, tabulated in this
study, show them to be on the average (in brains weighing more
than 1.3 grams) 4 to 7 micra greater in the transverse diameter,
7 to 10 micra greater in the longitudinal diameter of the cell
body, and 3 to 5 micra greater in both diameters of the nucleus—
all in corrected values—than the corresponding diameters of the
ganglion cells in localities VII and X, as shown in the following
summary :

Average corrected diameters of the cell body and of the nucleus of the ganglion cells
in the lamina ganglionaris (Groups XITI-XX)

LOCALITIES VII AND X LOCALITY III
Cells bodyaneeen cs. 28 x 37 w (average 32.4 pv) 33 x 46 uw (average 39.0 pu)
INGICleuUstes. a5 nose | 24 x 25 uw (average 24.4 pu) 28 x 30 uw (average 29.0 p)

The size of the cell bodies and their nuclei in the other layers
of the Albino cortex will be considered in a later chapter in this
paper.

Figures 3 and 4 give the typical appearance of the pyramids
and the ganglion cells, respectively, for each brain-weight group
(with a few omissions), all drawn proportional in size to the un-
corrected diameters and magnified about 950 times.

V. MORPHOLOGICAL CHANGES IN THE CORTICAL NERVE CELLS
DURING GROWTH

Figures 3 and 4 illustrate the typical pyramids and the ganglion
cells from each brain-weight group, as seen in the sections pre-

GROWTH OF THE CEREBRAL CORTEX 133

pared by me, from the material fixed in Bouin’s fluid, imbedded
in paraffine, stained with the carbol-thionine, and projected and
enlarged by a fixed number of diameters. The size of the pictures,
therefore, corresponds to the uncorrected measurements given in
tables 1 and 2.

Though they are increasing in volume very rapidly after birth,
the pyramids in the lamina pyramidalis retain up to a brain
weight of 0.6 gram (VI, 6 days in age) the characteristics of the

:
7 a

Fig. 8 Showing semi-diagrammatically the increase in size and the morpho-
logical changes, in the typical pyramids in the lamina pyramidalis of the cerebral
cortex of the albino rat. The Roman number by each cell figure indicates the
brain weight group from which the typical pyramid was selected and the drawing
made. All cell figures have been uniformly magnified to 950 diameters, according
to the uncorrected measurements.

134 NAOKI SUGITA

Fig. 4 Showing semi-diagrammatically the increase in size and the morpho-
logical changes in the typical ganglion cells in the lamina ganglionaris of the
cerebral cortex of the albino rat. The Roman number by each cell figure indicates
the brain-weight group from which the typical ganglion cell was selected and
the drawing made. All cell figures have been uniformly magnified to 950 diame-

ters, according to the uncorrected measurements.

GROWTH OF THE CEREBRAL CORTEX 135

fetal form of the cells,*? represented by a relatively large, round
nucleus thinly enveloped by a small amount of homogeneous
eytoplasm and with processes from both poles. The Nissl
bodies begin to appear first in a brain weighing 0.8 gram (VIII),
showing first in a part of cytoplasm adjoining the nucleus at the
apical pole and forming the so-called ‘Kernkappe.’ The cyto-
plasm matures rapidly in structure as the brain weight increases
from 0.8 to 1.2 grams. As the measurements show, the nucleus
attains nearly the full size when the brain weighs 0.95 gram (10
days), but at that phase the cytoplasm has not yet been fully
developed. It is meagre in mass, enveloping the nucleus thinly,

Fig. 5 Showing the cerebral cortex proper at the locality II (fig. 2, Sugita,
‘17 a) ona fetal brain of the albino rat. Body weight about 1.0 gram, body length
(neck-rump) about 19.5 mm., eighteenth day of gestation. Magnification of
about 500 diameters, measured directly on the slide.

the Nissl bodies not being yet fully differentiated, but only sug-
gesting the ‘Kernkappe.’ The cell continues to grow very
slowly up to a brain weight of 1.1 to 1.3 grams or about 20 to 30
days in age. Then, as the age advances, the sizes of both the cell
body and of the nucleus slowly diminish, while within the cyto-
plasm the differentiation of the Nissl bodies progresses. As the
differentiation progresses, the general tone of color of the section

’'The form of the fetal nerve cells from the locality II of the cerebral cortex
of the albino rat is shown diagrammatically in figure 5, which was taken from
an Albino fetus of 1.0 gram in body weight, 19.5 mm. in body length at the
eighteenth day of gestation. The cortex proper, not regarding the transitional
layer, consists of four or five rows of cells with scanty cytoplasm. The aver-
age diameter of the nucleus is about 5 to 7 micra on the slide and the thickness
of the cortex at this age is about 0.06 mm. on the slide.

136 NAOKI SUGITA

changes from violet to blue, owing to the deeper staining of the
Nissl bodies and of the intercellular tissue with the carbol-
thionine. The apical dendrite thickens rapidly during the period
in which the brain weight increases from 1.0 to 1.3 grams, but
the basal dendrites are not clearly stained until the brain at-
tains 1.6 grams in weight. Throughout the later life, the cyto-
plasm is slowly but continuously decreasing in the absolute mass
as the age advances, and the size of the nucleus is also diminish-
ing. The nucleolus in the nucleus attains also its full size (the
diameter is somewhat less than 2 micra) at the time when the
nucleus has attained the maximum size, but it tends to grow
slightly in late rages, while the nucleus show some decrease in size.

The structure of the nucleus of the pyramids is not clearly
demonstrable with this stain. As far as can be judged from the
present preparations, the chromatin substance in the nucleus
begins to develop notably only after the brain has attained the
weight of 1.0 gram, and after the nucleus has passed its phase of
rapid enlargement.

From the foregoing it will be seen that up to a brain weight of
0.95 gram, the pyramids may be regarded as in the preparatory
stage of structural development, attaining at the end of this
period nearly the full size of the cell body and of the nucleus.
And after this stage increase and differentiation in the cytoplasm
and the nucleus chromatin continue slowly until a brain weight
of 1.1 to 1.3 grams. After that time they begin rather to di-
minish in size, but nevertheless, to advance more and more in
differentiation, which latter change probably indicates the matur-
ing of the function of the pyramids. Morphologically, the
pyramids first attain their fully mature aspects at a brain weight
of about 1.6 grams (about 50 days in age).

In my previous studies on the development of the cortex
(Sugita, 717 a, 718 b), I named three phases of cortical growth in
the early life of the albino rat; the first phase: from birth to the
tenth day; the second phase: from the tenth to the twentieth
day, and the third phase: from the twentieth to the ninetieth
day. Applying this series of phases to the cytological develop-
ment of the pyramids, the following appears.

GROWTH OF THE CEREBRAL CORTEX kai

In the first phase occurs the rapid enlargement of the cell
body and the nucleus, the cell retaining still the fetal form, and
not showing any significant differentiation in the internal struc-
ture. The Nissl bodies first appear as the so-called ‘Kernkappe’
at the end of this phase. The tone of color of the sections stained
with the carbol-thionine is rather violet.

In the second phase, the size of the cell body and of the nucleus
continues to increase, but very slowly, and both attain their
maximum sizes at the end of this phase. The differentiation in
cytoplasm goes slowly on and the chromatin in the nucleus be-
gins also to differentiate. The tone of the stain is transitional
from violet to blue.

Throughout the third phase and afterwards, the size of the cell
body and of the nucleus decreases slowly from the maximum
values attached at the end of the second phase. But the differ-

-entiations of the cytoplasm and the nucleus chromatin steadily
continue as the age advances. The apical dendrites gain in
diameter and the basal dendrites begin to take the stain. The
nucleus sometimes shows the ‘Kernfalte. The tone of the
stain is rather blue and the contour of the pyramids clear cut.

The ganglion cells of the lamina ganglionaris enlarge very
rapidly and attain nearly their full size at the age of ten days—
somewhat earlier than do the pyramids. But the morphological
changes which take place in the ganglion cell body and the nucleus
are similar to those just described in the pyramids. In the
lamina ganglionaris there can be recognized two distinct kinds
of nerve cells, one the smaller-sized pyramids, which seem to be
very like the pyramids in the lamina pyramidalis, and the other,
the larger-sized neurons, which are usually called ganglion cells
or giant cells and which characterize the layer. Some of the
cells found in the lamina ganglionaris and which grow to be the
ganglion cells are from the first somewhat large-sized. These
develop more rapidly than the other small’ cells in this layer,
which are intermingled with them. In earlier stages the gan-
glion cells manifest no structural difference or characteristics
marking them off from the smaller cells, but differ only in the
size of the cell body and of the nucleus. They retain their fetal

138 NAOKI SUGITA

appearance, that is, an ovoid form with a relatively large nucleus
also ovoid or ellipsoid in form and a small amount of envelop;
ing cytoplasm, which seems almost homogeneous in its staining,
together with slender processes, until a brain weight of 0.75 gram.
The Nissl bodies begin at first to appear in a brain weighing 0.9
gram, as the ‘Kernkappe’ covering the apical part of the nucleus.
The differentiation of the cytoplasm becomes more and more
distinct as the brain weight increases and, in brains weighing
more than 1.3 grams, the section as a whole takes a blue tone.
This change in color tone is probably due to the development
of the Nissl bodies in the cytoplasm and the structural changes
in the intercellular tissue. The apical dendrites rapidly thicken in
brains weighing 1.1 to 1.8 grams and, in brains weighing more
than 1.3 grams, we see distinctly some relatively thick basal
dendrites and the axis-cylinder becomes visible. The mass of
the cytoplasm and the differentiation of the Nissl bodies proceeds
steadily as the age advances. In the fully grown brain we see
very often small satellite cells surrounding or indenting the
cytoplasm of the ganglion cells, though satellite cells appear in
relation to some other types of neurons also. Whatever the sig-
nificance of these satellite cells, it is to be noted that in younger
brains they are very rarely seen. The outline of the ganglion
cell body is not necessarily sharp nor is the form regularly pyra-
midal, being sometimes indeed quite irregular and often appear-
ing ovoid or ellipsoid in shape. Lipochrome or fat pigment,
usually seen in the adult human cells of this type, is never seen
in those of the adult albino rat, even in old age. ;
The nucleus of the young ganglior cell seems quite simple in
structure and it attains nearly the full size in a brain weighing
0.95 gram. After passing this stage, the chromatin structure
of the nucleus begins to appear. ‘The size of the nucleus may be
said to remain practically the same after this stage, while the
cytoplasmic development continues relatively rapidly. The
‘Kernfalte’ is sometimes visible in brains weighing more than
1.5 grams. The nucleolus in the nucleus of the ganglion cells
attains also nearly the full size (diameter is somewhat less
than 4 micra) at the phase when the nucleus has reached nearly

GROWTH OF THE CEREBRAL CORTEX 139

the full size (10 days), but continues to grow steadily, though
slightly, throughout later life. The size of the nucleolus in the
ganglion cells is relatively much larger than in the pyramids.

As for the developmental phases of the ganglion cells accord-
ing to age, a statement similar to that made concerning the pyra-
mids of the lamina pyramidalis holds true, though in the ganglion
cells the size development seems to be accomplished in general
somewhat earlier. In a brain under 1.2 grams in weight, more
mature ganglion cells are seen mixed up with those less mature,
indicating that the development of the ganglion cells is not uni-
form, but that some progress more slowly. In a brain weigh-
ing more than 1.3 grams, all the ganglion cells seem to have
already passed the first phase of development in size, and all the
cells are now of full size and probably fully functional.

One observation which I think it important to notice here is
that cells in the same layer but in different parts of the cortex
do not always show a like degree of development at a given age.
Some cells or some cell groups are more precocious or more re-
tarded than their neighbors. My observations apply only to the
size and morphology of the most developed cells found together
in a selected locality, regardless of the relative maturity of that
locality. So the statement that the ganglion cells attain full
size at ten days does not necessarily mean that the lamina gang-
lionaris is completely mature at that age, but it only applies to
the size or morphology of the most advanced cells found in the
layer. As a matter of fact, the lamina ganglionaris matures in
toto earliest, so that in a brain weighing 1.3 grams all the gang-
lion cells found in the lamina ganglionaris are apparently com-
pletely mature, while at the same age the lamina pyramidalis
still contains many immature cells among the mature ones, and
the full maturity of the latter layer is attained only in a brain
Weighing more than 1.6 grams (more than 50 days in age).

In respect of cell size and morphological changes, the lamina
ganglionaris and the lamina multiformis are the earliest to mature
all the elements in them, while the lamina pramidalis matures
more slowly, for example, and in a section from a brain twenty
days old, we can still see many immature cells mixed with the
mature ones in this latter layer.

140 NAOKI SUGITA

VI. ON THE NERVE CELLS IN OTHER LAYERS OF THE CEREBRAL
CORTEX

Figure 6 shows a diagram of cell-lamination of the adult albino
rat brain, taken from locality II of the sagittal section (fig. 2,
Sugita, 17a). In comparison with the data on the pyramids in
the lamina pyramidalis (IIT) and the ganglion cells in the lamina
ganglionaris (V), the measurements of the cells found in the
lamina granularis interna (IV) and the lamina multiformis (VI)
show nothing peculiar. Generally speaking, the cell body and the
nucleus of the granules do not take the stain as well as in the ease °
of the pyramids and remain rather pale in color. The cells of
the lamina multiformis, on the other hand, generally stain
deeply. Especially the cytoplasm of the cells forming the inner
(ental) sublayer of the lamina multiformis tints very well, so
that this sublayer is easily distinguished even at a low magnifi-
cation by the deep staining of the elements.

The granules in the lamina granularis interna (IV) are smaller
in size and lie more crowded than do the pyramids. This layer is
not clearly differentiated in brains weighing less than 0.6 gram or
less than six days of age, at which stage the immature cells of
fetal form prevail in both the lamina pyramidalis and the lamina
granularis interna and no characteristic granules are shown.
On the sections from a brain weighing 0.5 to 0.6 gram, which had
been fixed in formaldehyde and imbedded in paraffine, I could
see distinctly a dark band due to the deep staining of the ground
substance and characteristic for the adult lamina granularis in-
terna (ef. Sugita, 717 a, p. 526), though the contained cells do
not show any of the characteristics of the granules. This is
probably the first step in the differentiation of the granular layer.
Later we see that the cells lying near the lamina ganglionaris
become more and more crowded and somewhat small in size com-
pared with the cells lying in the lamina pyramidalis. In an adult
brain weighing more than 1.3 grams, a distinct band of smaller-
sized cells (the lamina granularis interna) appears above the
lamina ganglionaris.

141

GROWTH OF THE CEREBRAL CORTEX

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THE JOURNAL OF COMPARATIVE NEUROLOGY, VOL. 29, NO. 2

142 NAOKI SUGITA

TABLE 4
Giving both corrected and the uncorrected values for the two diameters of the cell
body and the nucleus respectively, of the granule cells in the lamina granularis
interna (IV, fig. 6) for several brain weight groups

CELL BODY NUCLEUS
BRAIN WEIGHT GROUP
Corrected On the slide Corrected On the slide
Ml Ke Me M

Group Tih(birgh) se. eee 125 (10 x 12) Iv x12 (9 x 10)
Groupsihlinwge seach) 546 (11 x 18) 12x 14 (10 x 11)
GroupsVin See cee 15 x18 (12 x 14) 14x15 Ges)
Groups Vil Valle eee 16 x 20 (13 x 16) 15 x 16 (12 x 18)
Groupsex oleae ae ee 19 x 21 @5ix 17) 16x19 (13 x 15)
Groups XUMPEVi.. ies. : 16 x 20 (13 x 16) 15 x 16 (12 x 18)
Groups XVI and above...... 15 x 20 (12 x 16) 14x 16 (11 x 18)

The average size of the granules measured on the sections here
used is given in table 4. In brain-weight Groups II—V, at which
stages the layer is not yet clearly differentiated, the measure-
ments were made on the small cells which lie nearest to the lamina
ganglionaris and the cells were assumed to be the future granules.

So, in brains weighing more than 1.6 grams (Group X VJ), the
size of the granules diminishes slightly as the age advances.
Most of the nuclei of the granules are more or less elongated or
elliptical in shape and the cytoplasm is very scanty, so that
sometimes there can be seen only a thin envelope of the cytoplasm
around the nucleus.

In short, the granules at the earlier age are almost equal to
the growing pyramids in size, but they increase in size somewhat
less rapidly as compared with the pyramids, among which they
are interspersed at first. They reach their maximum size in a
grain weighing between 1.2 and 1.4 grams, and after that period
the size decreases as the age advances, showing a somewhat com-
pact nucleus.

As already indicated in a former paper (Sugita, 717 a), the
lamina multiformis is divided by a pale band (fig. 6,*), poor in
cells, into two sublayers. The polymorphous cells in the ectal
sublayer have the shapes indicated by their name, but in general
they are pyramidal in form, the apex directed ectally, being
somewhat flattened and rich in cytoplasm, as compared with the

GROWTH OF THE CEREBRAL CORTEX 143

pyramids. The density of the polymorphous cells in this sub-
layer is greatest at the earlier ages. During the early ages the
most densely crowded pyramids are in the lamina pyramidalis,
while by contrast the lamina multiformis seems rather poor in
cells. But in adults the cell population of the ectal sublayer of
the lamina multiformis appears to be only slightly less than that
of the lamina pyramidalis and the size of the polymorphous cells
appears nearly equal to that of the pyramids, though, by an
exact measurement, they prove to be slightly larger (fig. 6).
The shape of polymorphous cells is not uniform and they show
many dendritic processes, irregularly arranged. Some, though
pyramidal, lie obliquely or transversely, while some hold a re-
versed position, with the apical dendrite directed entally (Marti-
notti’s cells).

The cells of the ental sublayer of the lamina multiformis are
quite different in their appearance. They are polygonal or
spindle-shaped and generally lie with their long axis in the plane
of the lamina. The cytoplasm of the cells is massive and takes
the stain well. The Nissl bodies, however, are not well dif-
ferentiated. Though not always pyramidal in shape, the as-
sumed apex of the cells appears to be directed towards the oc-
cipital pole in the sagittal and the horizontal sections or towards
the ventral surface in the frontal section, thus indicating the
direction of the migration of the nerve cells from the matrix
to the cortex proper. As already stated by me (Sugita, ’17a),
this sublayer probably serves as a secondary station for cells
migrating from the matrix at the ventricular wall to their final
destination in the cortex and the number of cells in this sub-
layer diminishes as the age of the brain advances. So one has
some reason to think that a fraction of the cells found in this
sublayer are still in transit, at least during the early ages. It
should be noted at least that the cells of this sublayer have a
morphology in respect of the mass and the staining reaction of
their cytoplasm which indicates the stage of migration.

The neuroglia nuclei are abundantly scattered in the ental
cortical layers (that is, in the lamina multiformis and the lamina
ganglionaris) as compared with the ectal layers (that is, in the

144 NAOKI SUGITA

TABLE 5

Giving the cubes of the average diameters of the cell bodies and of the nuclei of both
the pyramids (lamina pyramidalis) and the ganglion cells (lamina ganglionaris)
at birth, 10 days, 20 days and 90 days, the ages indicating respectively the begin-
ning of each developmental phase. The values given represent merely the rela-
tive volumes of the cell bodies and of the nuclei. Ratios based on the initial value
taken as unity are given for each column. The data, on the basis of which the
calculations were made, were taken from table 3

PYRAMIDS IN THE LAMINA GANGLION CELLS IN THE LAMINA
PYRAMIDALIS GANGLIONARIS
AGE INDICATING
THE BEGINNING OF LOAVES Cell body Nucleus Cell body Nucleus
EACH WEIGHT
DEVELOPMENTAL GROUP oe = a ae
SUNeue ba TA) ae a
B53 z= 25 zs BS Z| 25 $
Sei serines Woe age: a) ee yee
3 3 3 B33
Birtheeeeernee ee Jit PANSY WU (0.0 119 | 1.00 675 | 1.00 330 | 1.00
MO CPR o me 05 0 XO | TSS) | 5 775 | 6.50 | 2925 | 4.33 | 1440 | 4.86
AWCENippaoss bee GL || assy || @ 790 | 6.63 | 8070 | 4.55 | 1415 | 4.29
S0vdaySee sees cee OV LT 4) 70) |) oe A4: 665 | 5.58 | 35380 | 5.23 | 1490 | 4.52
|

lamina granularis interna and the lamina pyramidalis) (see fig.
6). At earlier ages, neuroglia nuclei are comparatively scarce
-in the lamina pyramidalis, but at maturity they are well distrib-
uted in this layer, though in the lamina multiformis they are found
always abundantly. With the method of staining here used,
we can distinguish two kinds of the neuroglia nuclei, one staining
a relatively deep blue, which is the smaller in size (2 to 5 micra
in diameter on the slide), with crowded granules in the chromatin
sometimes arranged radially (‘Radkern’), and surrounded by
evident cytoplasm, and the other staining rather paler and with a
violet tone, vesicular (‘blasig’) in appearance, somewhat larger in
size (3 to 6 micra in diameter on the slide), with seanty chromatin
and enveloped by a small amount of cytoplasm. This meta-
chromatism in the staining of the two kinds is very remarkable.
Both kinds are found intermingled. In the white matter gha
cells are distributed in rough chains, while in the cortex they are,
under normal conditions, less well distributed than in the white
matter. Sometimes, especially in old age, the glia cells are
found gathered around the ganglion cells or the pyramids or near
the blood-vessels. The satellite cells which are attached to or

GROWTH OF THE CEREBRAL CORTEX 145

even invade the cytoplasm of the nerve cells, are usually regarded
as neuroglia cells.

.The method here used, of staining with the carbol-thionine the
material fixed in Bouin’s fluid and imbedded in paraffine, reveals
clearly only the size and shape of the nerve cells in the cerebral
cortex. The more detailed structure of the cytoplasm and of the
nucleus or the structure of the axis-cylinder and dendrites is not
brought out by this method, and for the investigation of these
characters other methods are required.

VII. DISCUSSION

According to the foregoing observation, the full size of the
largest pyramids in the lamina pyramidalis (about 25 days in
age)‘ is about 21x 27 uw for the cell body and 19x 21 y» for the
nucleus, and the measurement of those largest at- birth® is 11 x 15 »
for the cell body and 10 x 11 » for the nucleus, in the fresh con-
dition of the material. The full size of the largest ganglion cells
in the lamina ganglionaris (at localities VII and X, about 25
days, for example)! is 27 x 37 uw for the cell body and 24x25 u
for the nucleus, and the measurement of the largest ganglion cells
at birth’ is 17x21 uw for the cell body and 14x16 wu for the
nucleus, all in the fresh condition of the brain. .

If the volume of the cell bodies or of the nuclei be comparable
among themselves according to the cubes of their average diame-
ters, the figures given in table 5 which presents the cubes of the
average diameters of the cell bodies and of the nuclei of the nerve
cells at different ages, and which were calculated from the data
in table 3, may be used as the basis of discussions on the volume
development of the cells. It will be seen from table 5, by a

4 To obtain the values here given, the uncorrected diameters of the cell body
and the nucleus in Groups XI-XIII in the frontal and the horizontal sections
(tables 1 and 2) were respectively averaged and the results were corrected b
multiplying by the mean correction-coefficient of Groups XI-XIII for the
frontal and the horizontal sections (see table 3).

> To obtain the values here given, the uncorrected diameters of the cell body
and the nucleus in Group II in the frontal and the horizontal sections (tables 1
and 2) were respectively averaged and the results were corrected by multiplying
by the mean correction-coefficient of Group II for the frontal and the hori-
zontal sections (see table 3). 5

146 NAOKI SUGITA

simple calculation, that at birth the largest ganglion cells are
almost 3.1 times as voluminous, at 20 days about 2.3 times, and
at 90 days 3.0 times, as the pyramids of the same stage, and the
nuclei of the ganglion cells are at birth 2.8 times as voluminous,
at 20 days 1.8 times, and at 90 days, 2.2 times as the nuclei of
the pyramids of the same stage, if both kinds of cells are assumed
to have the similar forms throughout their enlargement.® It is
also seen that, using the same method, the cell body of the pyra-
mids has increased from birth 6.1 times in volume at 20 days and
5.4 times at 90 days, and the nuclei 6.6 times at 20 days and5.6
times at 90 days, while the cell body of the ganglion cells has
increased only 4.6 times at 20 days, 5.2 times at 90 days and the
nuclei of the ganglion cells 4.3 times at 20 days and 4.5 times
at 90 days, as compared with their initial volumes at birth.

It may therefore be concluded that, throughout the develop-
mental stage of the nerve cells after birth, the rate of enlarge-
ment is almost similar in the nuclei and in the cell bodies of both
kinds of cells, though the rate is slightly higher in the pyramids
than in the ganglion cells in both the cell body and the nucleus
during the first twenty days after birth, because the initial
volume of the pyramids is small at birth.

As the shape of the cell body is different from that of the
nucleus, it is not proper to compare directly their respective -
volumes as determined by the foregoing use of their diameters,
but they must be first reduced to forms which are comparable as

6 Here the nucleus was considered as an ellipsoid, the volume of which is to be
calculated by the formula $7a2b, when 6 is the long radius and a is the short
radius of the body. Asthe transverse diameter (n:) of the nucleus is equal to
2a and the longitudinal diameter (n2.) is equal to 2b the volumes of the nuclei
may be compared among themselves simply by the factor a*b or 2m.

On the other hand, if the volume of the cell body was considered as a circular
cone, in which the diameter of the basic circle is equal to the transverse di-
ameter (c;) of the cell body and the height of the cone is equal to the longitu-
dinal diameter (c,) of the cell body, then the volume of the cell body will be
an (G )Pes, and the values for the relative volumes of the cell bodies may be com-
pared on the basis of the factor ¢12c:.

As the average diameters given in table 3 are respectively the square roots
of the products mim, and c,¢2, the cubes of the average diameters will be approxi-
mately proportional to the values ni2n. and c,2c., respectively.

GROWTH OF THE CEREBRAL CORTEX 147

explained in the accompanying note and then table 5 may be con-
sulted again.’? It is seen from table 5 that at birth the entire
cell has almost double the volume of the nucleus, so that the
cytoplasm and the nucleus have nearly the same volume. The
nucleus-plasm relation changes according to the brain weight.
In the pyramids, the total cell body comes to 1.7 times at 20
days and to 1.8 times at 90 days, compared with the volume
of the nucleus at the same age. This is owing to the relatively
rapid growth of the nucleus. In the ganglion cells, on the
other hand, the total cell body is 2.2 times at 20 days and 2.4
times at 90 days, compared with the volume of the nucleus at
the same stage. As the pyramids decreases in size after 30
days, the cell size of the pyramids in old age (brain weight more
than 2.0 grams) becomes almost equal to that at 8 days of age,
but the nucleus-plasm relation is quite different at the two stages.
At 8 days the nucleus is relatively large (total cell body is 1.7
or less times the nuclear volume), but in old age the volume of
cytoplasm has increased somewhat in relation to the nuclear
volume (total cell body is nearly 2.0 times the nuclear volume).

These values for comparison were taken from the data here
used alone, but, as already noted, sections which were taken
from material fixed in 95 per cent alcohol or in Bouin’s fluid and
imbedded in celloidin show a nucleus which is relatively smaller.
In series of sections which have been prepared by methods other
than that used by me, the volume relations between the cell body
and the nucleus (nucleus-plasm relation) would probably be dif-
ferent from those which I have reported here, but I think it will
be fair to assume that the growth changes in the cell body on

7 Tf the cell body were considered as having an ellipsoidal form with diame-
ters equal to ¢; and c, which denote respectively the transverse longitudinal diam- *

: a 3
eters measured on the cell body the volume, would be i(3)*(G) or agTer'C2.
And if, on the other hand, the same cell body were considered as a circular cone,
C 1 ,
the volume may be calculated by in(Z) 2¢5, OF omeves. As the difference between

these two formulas is not higher than of cc, I have here compared the

aus
96
volumes of the cell body and of the nucleus under the assumption that both have

the ellipsoidal form, employing once more the figures given in table 5 as the
basis of comparison.

148 NAOKI SUGITA

one hand and in the nucleus on the other would probably be simi-
lar by the use of any uniform method, even if the absolute values
differed for the different methods, and none of them gave exactly
the fresh values.

It is remarkable that both the cell body and the nucleus of the
cortical cells attain nearly their full size at an early stage of
development (at about ten days of age) and then continue to
undergo cytomorphic development, without much change in cell
size (chart 1). As already pointed out in former papers (Sugita,
17 a, 718 b), the elementary completeness of the cerebral cortex
of the albino rat is attained at the age of twenty days, the final
thickness of the cortex and the total number of the cortical nerve
cells being apparently reached at this age. After this age, the
volume of the cortex increases as the age advances nearly in pro-
portion to, or at a slightly slower rate than, the total volume of
the cerebrum. As noted, the size of the pyramidal cells in the
lamina pyramidalis attains the maximum size in brains weighing
1.1 to 1.3 grams and the volume of the cell body and the nucleus
becomes slightly less during later phases, while the size of the
ganglion cells in the lamina ganglionaris increases slightly as the
age advances, even after the above-named stage. It must be
concluded, therefore, that the subsequent increase in cortical
volume is effected. by changes in structures other than the cell
bodies themselves. And, as a consequence, in mature brains,
the cell density in the cortex diminishes more and more, as has
been already pointed out in a previous paper (table 3, Sugita,
718 b).

It is very interesting to find that the thickness of the cortex,
the total number of the cortical nerve cells, and the size of the
- cortical cells all have reached nearly their maximum at the same
age of twenty days, which is the weaning time of the rat. These
relations appear also in the mouse. According to the results
obtained by Isenschmid (’11), the thickness of the cerebral cor-
tex of the mouse, measured at a fixed locality—corresponding to
locality VII in my sections—attains nearly its full value some-
thing before seventeen days in age. And according to the
systematie work of Stefanowska (’98), who has studied the devel-

GROWTH OF THE CEREBRAL CORTEX 149

opment of the cortical nerve cells by the’ method of silver im-
pregnation of Golgi, the cortical nerve cells of the mouse have
completed their development in respect of their attachments at
the age of fifteen days, and the age of fifteen days is the weaning
time of the mouse. It appears, therefore, that the completion
of certain features of cortical development in relation to the
Weaning time, the time when the young become independent
of the mother, is similar in both the albino rat and the mouse.

VIII. SUMMARY

1. The size of the nerve cells most advanced in development
from a fixed locality of the cerebral cortex was systematically
measured and the developmental changes during postnatal growth
studied on the material represented by the grains of 128 albino
rats of different: ages. The data have been averaged for each
brain-weight group and then corrected for the fresh condition
of the material, using the correction-coefficients devised for this
purpose. The results are given in tables and charts.

2. The full size of the pyramids in the lamina pyramidalis
(about twenty-five days in age, average of Groups XI-XIIT)
is cell body 21 x 27 » and nucleus 19 x 21 uw and the largest size
at birth is cell body 11x15 uw and nucleus 10x11 uw. The size
of the ganglion cells in the lamina ganglionaris at the same stage
(about twenty-five days in age, average of Groups XI-XIII)
is cell body 27 x 37u and nucleus 24 x 25 yu, while the largest size
at birth is cell body 17 x 21 uw and nucleus 14 x 16 up.

In the full-grown albino rat (Groups XVI-XX), the average’
size of the pyramids is cell body 20 x 26 uw, nucleus 18 x 19 » and
the average size of the ganglion cells is cell body 28x 38 u,
nucleus 24 x 25 uw.

3. The cell body and the nucleus of the pyramids attain their
maximum size at twenty to thirty days in age (1.1 to 1.3 grams
in brain weight). Up to the tenth day of age they retain their
fetal morphology. After having passed the maximum at twenty
to thirty days, they diminish in size, but the internal structure
matures more and more as the age advances.

150 NAOKI SUGITA

4. The cell body and the nucleus of the ganglion cells attain
nearly their full size at ten days (0.95 gram in brain weight),
when they still show the fetal appearance. After this stage,
the size of the cell body increases slowly but steadily as the age
advances, while the nucleus remains nearly unchanged in size
throughout life.

5. Both the pyramids and the ganglion cells retain clearly
the fetal character of form until the brain weighs 0.6 gram or
more. The differentiation of the cytoplasm and the Nissl bodies
begins to appear in my preparations first in a brain weighing
something more than 0.9 gram, the latter showing first as the
‘Kernkappe’ at the apex of the nucleus. The cells exhibit the
mature appearance in a brain weighing more than 1.4 grams.

6. As for the maturation of the several layers, in general, dis-
regarding the maturation of the individual cells in them, the
lamina ganglionaris is completed earliest, so that in a brain weigh-
ing 1.3 grams (thirty days in age) all the ganglion cells in this
layer are apparently mature, while at the same age the lamina
pyramidalis is less mature as it contains relatively many imma-
ture cells mingled with the others. The full maturity of the
lamina pyramidalis is attained, probably, in a brain weighing
1.6 grams (more than fifty days in age).

7. Throughout the developmental stage of the nerve cells, the
rate of enlargement is almost similar in the nucleus and in the cell
body in both the pyramids and the ganglion cells; but when the
pyramids are compared with the ganglion cells it appears that the
rate is more rapid in the pyramids than in the ganglion cells in
both the cell body and the nucleus during the first ten days
after birth.

8. The lamina granularis interna is first differentiated in brains
Weighing more than 0.6 gram. In younger brains it is confused
with the pyramidal layer and cannot be clearly discriminated.
The granules attain their maximum size in brains weighing 1.0
to 1.8 grams and then diminish slightly. The final size ( or-
rected) of the granules in Groups XVI and above, is cell body
15 x 20 ww and nucleus 14x 16 u.

GROWTH OF THE CEREBRAL CORTEX ill

9. The polymorphous cells in the ectal sublayer of the lamina
multiformis are slightly larger than the pyamids of the same age.
The polymorphous cells in the ental sublayer of the lamina multi-
formis are somewhat larger than those of the ectal sublayer,
but are irregular in shape and rich in cytoplasm.

10. Two kinds of the neuroglia nuclei are found in the cortex.
One staining deep blue with the carbol-thionine, smaller in size
(2 to 5 micra in diameter on the slide) and having a radiating
structure of the chromatin, and the other staining paler, swollen
(‘blasig’) and somewhat larger in size (3 to 6 micra in diameter
on the slide).

11. Taking a general view of the ddta already presented in
this series of studies, it is very interesting to note that the thick-
ness of the cortex, the total number of the cortical nerve cells,
and the size of the cortical cells all attain nearly their full
values at the same age of twenty days (1.15 grams in brain
weight); that is, at the weaning time of the albino rat.

PAR sii

ON THE INCREASE IN SIZE OF SOME NERVE CELLS IN THE CEREBRAL
CORTEX OF THE NORWAY RAT (MUS NORVEGICUS) COMPARED
WITH THE CORRESPONDING CHANGES IN THE ALBINO RAT

To compare with the results of the preceding study on the
growth in size of the cortical nerve cells in the albino rat brain,
data were gathered for the cortical cells of the Norway rat also.
According to my previous studies (Sugita, ’17 a, 718 a, ’18b),
the measurements of the cerebral cortex in the Norway rat in
thickness, in total number of cells, etc., have shown some inter-
esting relations to the corresponding measurements for the
Albino. Donaldson and Hatai (11) made a comparison of these
two animals in respect of their body measurements and the size
of the central nervous system, and concluded that the greater
weight of the brain in the Norway rat is probably due to an en-
largement of the constituent neurons rather than to an increase
in their number. As my former study (Sugita, 718 b) has de-

LoZ NAOKI SUGITA

TABLE 6
Giving the average wncorrected diameters of the nerve cells and their nuclei in the
lamina pyramidalis and the lamina gangvionaris measured at the fixed locality
(locality VII) on the frontal sections of the Norway rat brain. The data are given
for each brain weight group only. This table is comparable with table 1

LAMINA PYRAMIDALIS LAMINA GANGLIONARIS

BRAIN WEIGHT | NO. OF | BRAIN Cell body Nucleus Cell body Nucleus

GROUP CASES |WEIGHT diameter diameter diameter diameter
Transv.| Longit. Transv.| Dongil eramee Longit.)|Transv.| Longit.

| grams Mh KM 3 | M in K M 7
N XI 3 1164) 15325) 20-8) |) 1405") 155) 2025. | 2920") TSE i Loks
N XIII 1 1.369] 15.5 | 20.9 | 14.4. )°15-:5 || 20.6 | 29:9) | 18.3) | 2052
N XIV 6 1.430) 19.4 | 20.6 | 14.2 | 15.1 | 21.6 | 29.6 | 18.4 | 19.4
N XV 3 1.546) 14.8 | 19-8) 13-8 | oT 2025 |) 28-9) | 17.8) | T9k6
N XVI 3 1.629) 14.6 || 19-8 |) 13.4) 14.1 | 21.2) 29.0!) 17-8) 19e2
N XVII 4 1-739) 1479 | 20.4 |) #3.3 |) 14% |) 219) | 29:8) | 18.9) |) 2022
N XVIII 2 | 1 S29 aS ON 20 | 14 WS =) Doan S28) ZO nea leelene
N XIX Dy 12972 (4S) 1924 | SR On Aron eae om ao( | 20cm moieno
N XX 2 2.052] 14.5 | 19.8 | 13.6 | 14.3 | 23.9 | 33.2 QS e2aG
N XXI 2, DE WiZ ASSN ZOL OM 13hor hae SOS RON 4s On lO RA eae
N XXIII 1 |S 25345 ASG) QO a3 335) 132902570) Ps6n0n 1S s5e E20 Rs

1Tn this group the size of the nucleus of the ganglion cells has fallen down
remarkably (see also chart 2), which fact was not seen in the Albino (Group
XX). Whether this is due to an actual change in old age or due to incidental
variation cannot be definitely affirmed here.

termined that in both forms the total number of the nerve cells
in the cerebral cortex is practically the same, it becomes desir-
able to compare the size of the nerve cells in the two animals in
order to test the assumption of the above authors.

The material used in. this study comprised 54 Norway rats,
sexes combined, the data for which are given in tables 1 and 2
in a former paper (Sugita, 718 a) and which are the same ma-
terial that was formerly employed for the other measurements
on the cortex. It seems unnecessary to repeat these tables
here. .

In the selection of the localities in which the largest cells in the
lamina pyramidalis and the lamina ganglionaris were measured
and in making the measurements, the same procedure was fol-
lowed as has been described minutely for the albino rat in part
I of this paper.

GROWTH OF THE CEREBRAL CORTEX 153

TABLE 7

Giving the average uncorrected diameters of the nerve cells and their nuclei in the
lamina pyramidalis and the lamina ganglionaris measured at the fixed locality
(locality X) on the horizontal sections of the Norway rat brain. The data are
given for each brain weight group only. This table is comparable with table 2

LAMINA PYRAMIDALIS LAMINA GANGLIONARIS
BRAIN WEIGHT | NO. OF | BRAIN Cell body Nucleus Cell body Nucleus
GROUP CASES |WEIGHT diameter diameter diameter diameter
Transv.| Longit. Transv.| Longit.|/Transv.| Longit. Transv.( Longit.
grams L B bb im 7 Me M M
N XI 3 TOS es 2068F AST 15.4) 2066) e29E3R | 180m) 19.2
N XIII 1 S43) | LORS TA 15. | 20k 2825 elite Sale Loeo,
N XIV 5 1.447) 15.4 | 20.6 | 14.4 | 15.3 | 20.8 | 29.0 | 18.4 | 19.7
N XV 3 e520 Asa le 2Oe2nelasGul los Ie20k 5 p2enonloaen lL OLO,
N XVI 4 1663/5149) 22050) 13.85) 14.9 | 2020) 2988) i tSesnialOr3s
N XVII 4 LATA S| 2080) | WSe7 1 V5.0) | 2ZOESN 29F a" Seon) ORS
N XVIII 2 1.843) 14.5 | 20.2 | 18.8 | 14.7 | 20.2 | 29.4 | 18.0) 19.5
N XIX 1 95S LOSE ZORSe elas onllons || Zoom ras orm One meo Ore
N XX Ps PAV ss) MEG) | PRES) ESA a Bree 3 is) WEBLO Alssatst |) IR
N XxI 2 ZOO 147 || 2089") 1368) 14.4 | 238.0) 29245) 188319200
N XXIII 1 2340| 1520) |) 2028) 13-4 | 14.0 | 2528 || 32201) 184s get

1 See note on table 6.

The results of the measurements are presented in tables 6 and
7 arranged in the same way as in the corresponding tables 1 and
2 for the Albino. Chart 2 shows graphically the data presented
in table 8 which gives the average diameters of the cell bodies
and the nuclei for each brain-weight group, corrected for the
fresh condition of the material, by multiplying by the correction-
coefficient for the group, which is cited from my previous paper
(Sugita, 718 a) and explicitly given in table 8 also. Charts 3
and 4 show some comparisons in cell sizes in the two forms.
Chart 3 was plotted according to the actual brain weights of the
two forms, and chart 4 was plotted, using the same data for
the Norway, but entering these according to the brain weights
reduced by 18 per cent, which presumably correspond to the
brain weights-of the Albino at the same age (see Sugita, 718 a),
while the data of the Albino were plotted according to the actual
brain weight.

154

NAOKI

SUGITA

TABLE 8

Giving the corrected final average diameters of the nerve cells and their nuclei in the
lamina pyramidalis and the lamina ganglionaris measured on the frontal and
The average values of the two

the horizontal sections of the Norway rat brain.
The correction-coefficient for each

for each brain weight group are also given.
brain weight group, was taken from previous papers (Sugita, ’18 a, 718 b).

F = frontal section.

BRAIN WEIGHT

BRAIN

CORRECTION-
COEFFICIENT

GROUP WEIGHT
grams

FN XI 1.164 1

H N XI. 1.164 1
1.164

F N XII 1.369 1

H N XIII 1.343 1
1.356

FN XIV 1.430 1

H N XIV 1.447 1
1.439

FN XV 1.546 i

H N XV 1.520° 1
1.533

F N XVI 1.629 1

H N XVI 1.663 1
1.646

F N XVII 1.739 1

H N XVII 1.747 1
1.748

F N XVIII 1.829 1

H N XVIII 1.843 1
1.836

F N XIX 1.972 af

EDN Sole 1.953 1
1.963

FN XX 2.052 1

H N XX 2.018 1

2.035

34
30

30
39

39
36

.40
42

40
34

7
00

32
.39

33
34

06
02

H = horizontal section.

LAMINA PYRAMIDALIS

LAMINA GANGLIONARIS

Cell body
diameter

u
23.8
23.0
23.4

bo bo
Ct Ww Ww
nq Ore

cos)

Nucleus
diameter

Cell body Nucleus
diameter diameter
Le B

Sot Pass 0)
31.8 24.2
32.3 24.6
33.0 PAG
33.4 25.6
83.2 25.6
34.2 745005)
BOLO 25.9
38.9 Gad
34.2 26.2
34.5 26.4
84.4 26.3
34.7 25.9
3o20 PAPA
o4 od 25.6
3155, 11 26.7
33) 50) PAS.
384.8 26.2
36.7 27.8
34.0 26.0
SOy 26.9
38.0 27.9
aia. 7 26.5
36.8 Bie,
38.3 28.5

* 35.6 75) (0)
37.0 26.8

GROWTH OF THE CEREBRAL CORTEX 155

TABLE 8—Continued

LAMINA PYRAMIDALIS LAMINA GANGLIONARIS
BRAIN WEIGHT BRAIN CORRECTION-
CUAOIHE RGEC COE CEB NE at Gellibody: Nucleus Cell body Nucleus
diameter diameter diameter diameter
grams BL BL B BL
FN XxXI 9) Me 1.39 23.5 19.2 39.6 28.1
HN XXI 2.156 1.34 23050 18.9 34.8 26.0
2.164 23.5 19.1 lane, Dial
FN XXIII 2.345 1.26 22.0 Lae 37.8 24.6
HN XXIII 2.345 1.28 22.6 17.4 36.8 24.1
2.3846 22.3 HPht) EN) 24.4}

1See note on table 6.

Chart 2 shows for the Norway also that the ganglion cells are
enlarging slowly but steadily throughout life, while the pyramids
rather decrease in size slightly in later life, after having attained
the maximum size in brains weighing 1.3 to 1.5 grams. So, in
the Norway as in the case of the Albino, the pyramidal cells in
the lamina pyramidalis undergo some diminution in the adult
brain.

Chart 3 gives a comparison of the cell sizes in brains of like
weight in the two forms. In Group N XI, the sizes of the cell
body and the nucleus of the pyramids are slightly smaller in the
Norway than in the Albino. This is probably explicable by the
fact that the Norway brain at this stage is still immature and
younger than the Albino brain of like weight. Such a relation
has been revealed in other measurements also; for example, in
the cortical thickness, the cortical area, etc. (Sugita, 7°17 a,
18 b). The ganglion cells in the Norway are larger than in the
Albino and the difference in the size of the ganglion cells in the
two forms increases somewhat as the brain weight advances.

In Groups above N XIII, the cell size (pyramidal and ganglion
cells) in the Norway proved to be generally larger than that in
the Albino of the same brain weight.

The summary in table 9 gives the average diameters for the
adult Albino (Groups XIII to XX) and the adult Norway
(Groups N XIII to N XX).

156 NAOKI SUGITA

TABLE 9

Comparison of diameters of cortical cells in the Norway and the albino rats. The
data used here are the averages in Groups XIII to XX and in Groups N XIII
to N XX, taken from tables 3 and 8. Differences in diameter and in volume are
calculated here, the data of the Albino being taken as the standard of comparison

2 PYRAMIDS GANGLION CELLS
AVERAGE
BRAIN WEIGHT
Cell body Nucleus Cell body Nucleus
grams 7 7 i 7) Lu
IA bInOse ee oe oak 1.691 22.9 18.8 32.4 24.9
INOE Ways oo --2e 1.694 23.7 19.6 34.9 26.3
Difference in diameter...... 3.5% 4.2% GIG 5.6%
Difference in volume....... 10.9% 1B11G% 24.9% 17.8%

This summary shows that in mature brains of like weight, the
pyramids (cell body and nucleus) in the Norway exceed those
in the Albino in avérage diameters by about 4 per cent and in
volume by about 12 per cent, and the ganglion cells (cell body
and nucleus) in the Norway exceed those in the Albino in aver-
age diameters by about 7 per cent and in volume by about 20
per cent, if the Albino be taken as the standard of comparison.
It may be said, therefore, that in the Norway the ganglion cells
in the lamina ganglionaris exceed much in size those in the Albino,
while the pyramids in the Norway-are only somewhat greater
than those in the Albino.

In chart 4, which gives a comparison of the nerve-cell sizes
between brains of presumably the same age in the two forms, it is
shown clearly that the changes in sizes of cell body and the
nucleus according to age are quite similar in both forms. The
pyramids attain the maximum size at about twenty to thirty
days (in the Albino in brains weighing 1.1 to 1.8 grams, in the
Norway in brains weighing 1.3 to 1.5 grams, which both come to
the same relative position in the curves), and after that they de-
crease slowly. The ganglion cells in the Norway grow more
rapidly than those in: the Albino, even in later life. In the
latter the ganglion cells remain almost unchanged in size in
brains weighing 1.0 to 1.6 grams, while those in the Norway
increase in size rather steadily as the age advances.

GROWTH OF THE CEREBRAL CORTEX 157

Diameter in micra
40,

7 af
| |
38|——+ i SSS
| | | za ire | ~oSs
36 + — + poste
| | Go “a
ee a 4
pe |
32 Cae t : 7
30; a+ —
i} ale
28 =
| | ta eee ie
26 i= oe Se 3 ise +
= = ple = hs — = FO. —
24 = S=s So ES = Sa GN
Sse
22) ih ==
H |
20 | Sp tee + +
| | o—__—_@ ————
-—_}—*.
* | | a [al aS
| | | DN!
P| | PN
40} T in |
| | |
44 — ib + = {
| | | |
|
42. |
|
| | | |
40 | ; Il Walt f= 4 =f
8h | = T =? =
6 a |
| |
4 + — } + == i 4 j Je Fe t 1
2 | =} + ‘= - + utes 4 |
ea

A egeh ( a Ml |
40 if i 13 4 15 ie iT 18 19 20 2 22 23 2¢ pms

Chart 2 Showing the corrected average diameters of the cell body and the
nucleus of the cortical nerve cells of the Norway rat, plotted according to in-
creasing brain weight. Based on the data in table 7. Graph GC’, average
diameter of the cell body of the ganglion cells in the lamina ganglionaris. Graph
GN’, average diameter of the nucleus of the ganglion cells in the lamina ganglion-
aris. Graph PC’, average diameter of the cell body of the pyramids in the
lamina pyramidalis. Graph PN’, average diameter of the nucleus of the pyra-
mids in the lamina pyramidalis.

THE JOURNAL OF COMPARATIVE NEUROLOGY, VOL. 29, NO. 2

158 NAOKI SUGITA

Diameter inmicra
40,
| | |

tical } |
if | |
38; t 7 T Teves! |
| : ass

| | |

|
|

= + |
| |

2)

i]
| |
|

|
| |
243 15) 16 17 48 19 20 20 ,22)03 2h ns

+
|

| |
| |
i !
| ea |
: |
|

Co ¢j ees ee ee
LOL:

Chart 3. Showing a comparison of sizes of the cell bodies and of the nuclei
of the ganglion cells in the lamina ganglionaris and of the pyramids in the lamina
pyramidalis in brains of the Norway and the Albino, according to the actual brain
weights. The data are taken from tables 3 and 7. The chart has been divided
and the values 22-26 on the ordinate repeated to prevent confusion among graphs
for the cell bodies of the pyramids, PC and PC’, and the graphs for the nuclei
of the ganglion cells, GN and GN’. In the upper chart: Graph GC’, cell body
of the ganglion cells in the Norway. Graph ‘GC, cell body of the ganglion cells
in the Albino. Graph GN’, nucleus of the ganglion cells in the Norway. Graph
GN, nucleus of the ganglion cells in the Albino. In the lower chart: Graph
PC’, cell body of the pyramids in the Norway. Graph PC, cell body of the
pyramids in the Albino. Graph PN’, nucleus of the pyramids in the Norway.
Graph PN, nucleus of the pyramids in the Albino.

GROWTH OF THE CEREBRAL CORTEX 159

Diameter in micra
40/—

334

36

|
|
|

5 eee ee | ee | | ee
|

|

|

ea
+ + :

|
i a
i] | |
| oe ae |
2 = haem |i — j | T
| |

ee ae es ea as
Chart 4\!Showing a comparison of sizes of the cell bodies and of the nuclei
of the ganglion cells in the lamina ganglionaris and of the pyramids in the lamina
pyramidalis in brains of the Norway and the Albino, according to age. The
Norway brain weight was reduced by 18 per cent and entered at the correspond-
ing brain weight of the Albino. The data were taken from tables 3 and 7. The
chart has been divided and the values 22-26 on the ordinate repeated to prevent
confusion among the graphs for the cell bodies of the pyramids, PC and PC’,
and the graphs for the nuclei of the ganglion cells, GN and GN’. In the upper
chart: Graph GC’, cell body of the ganglion cells in the Norway. Graph GC,
cell body of the ganglion cells in the Albino. Graph GN’, nucleus of the ganglion
cells in the Norway. Graph GN, nucleus of the ganglion cells in the Albino.
In‘the lower chart: Graph PC’, cell body of the pyramids in the Norway. Graph
PC, cell body of the pyramids in the Albino. Graph PN’, nucleus of the pyra-
mids in the Norway. Graph PN, nucleus of the pyramids in the Albino.

s

160 NAOKI SUGITA

My study of the Norway cortex did not extend to the early life
of the animal, but, from the courses of the curves shown. in chart
4, it seems probable that, in early life, before ten days after birth,
the developmental changes in the cell size would be quite similar
to those in the Albino, which have been minutely described in
part I, and that we may therefore apply to the Norway rat also
the same developmental phases as were formerly applied to the
Albino.

Morphological changes in the cytoplasmic and nuclear struc-
tures in the Norway rat cells are similar to those in the Albino,
if the comparison is made at like ages, so that figures 3 and 4
in part I of this paper may be considered to represent Norway
cells as well.

Briefly stated, in the case of the Norway rat, the maximum size
of the pyramids in the lamina pyramidalis (in brains weighing
1.3 to 1.5 grams) is cell body 21 x 28 uw and nucleus 20 x 21 py;
values only slightly larger than those in the Albino. The final
size of the ganglion cells in the lamina ganglionaris (in brains
weighing 1.9 to 2.3 grams) is cell body 32 x 48 uw and nucleus
26 x 27 yw, which is much larger than the corresponding measure-
ments for the Albino.

Nissl bodies are already seen in brains weighing 1.13 grams—
the youngest case in my material—but these bodies assume their
mature appearance first in brains weighing more than 1.6 grams...
As regards other developmental changes both in the cytoplasm
and in the nucleus, the statements made for the Albino are all
applicable to the Norway, if the comparison is made at like ages.

SUMMARY

1. In the full-grown Norway rat (Groups N XIX to N XXIII),
the average size of the pyramids in the lamina pyramidalis is cell
body 20x 27 u, nucleus 18x 19 y, and the average size of the
ganglion cells in the lamina ganglionaris is cell body 32 x 43 u,
nucleus 26 x 27 un.

2. The cell body and the nucleus of the pyramids attain their
maximum size (cell body 21 x 28 », nucleus 20 x 21 w) in brains
weighing 1.3 to 1.5 grams, and after that they slightly diminish

GROWTH OF THE CEREBRAL CORTEX 161

in size, but the internal structure matures progressively as the
brain weight increases. The cell body and the nucleus of the
ganglion cells increases in size continuously throughout life.
The last entry for the nucleus of the ganglion cells is an exception
to this statement.

3. As compared with the corresponding cells in the albino rat,
the pyramids in the adult Norway rat (Groups N XIII to N XX)
exceed those in the Albino in diameter on the average by 4 per
cent and in volume by 12 per cent and the ganglion cells also
exceed in diameter on the average by 7 per cent and in volume
by 20 or more per cent.

4. The course of development and the morphological changes
in the Norway cells are similar to those in the albino rat, if com-
pared at like ages. At the same age, the Norway brain weight,
less 18 per cent, is taken as equal to the brain weight of the
Albino.

162 NAOKI SUGITA

LITERATURE CITED

ALLEN, Ezra 1916 Studies in cell division in the Albino rat (Mus norvegicus
var. alba). II. Experiments: on technique, with description of a
method for demonstrating the cytological details of dividing cells in
brain and testis. Anat. Rec., vol. 10, pp. 565-586.

Donatpson, H. H. 1915 The Rat. Memoirs of The Wistar Institute of Anat-
omy and Biology, no. 6.

Donatpson, H. H., anp Harar, S. 1911 A comparison of the Norway rat with
the albino in respect to body length, brain weight, spinal cord weight
and the percentage of water in both the brain and spinal cord. Jour.
Comp. Neur., vol. 21, pp. 417-458.

IseNScHMID, Ropert 1911 Zur Kenntnis der Grosshirnrinde der Maus. Ab-
handl. der Kénigl. Preussischen Akad. d. Wissenschaften.

Kine, Heten Dean 1910 The effects of various fixatives on the brain of the
albino rat, with an account of a method of preparing this material
for a study of the cells in the cortex. Anat. Rec., vol. 4, pp. 213-244.

SteraNowska, MicuHerine 1898 Evolution des cellules nerveuses corticales
chez las souris aprés la naissance. Annales de la Soc. Royale des
Sciences méd. et naturelles de Bruxelles, vol. 7.

’ Sucira, Naoxi 1917 a Comparative studies on the growth of the cerebral

cortex. II. On the increase in the thickness of the cerebral cortex

during the postnatal growth of the brain. Albino rat. Jour. Comp.

Neur., vol. 28, no. 3.

1918 Comparative studies on the growth of the cerebral cortex.

III. On the size and shape of the cerebrum in the Norway rat (Mus

norvegicus) and a comparison of these with the corresponding charac-

ters in the albino rat. Jour. Comp. Neur., vol. 29, no. 1.

1918 a Comparative studies on the growth of the cerebral cortex.

IV. On the thickness of the cerebral cortex of the Norway rat (Mus

norvegicus) and a comparison of the same with the cortical thickness

in the Albino. Jour. Comp. Neur., vol. 29, no. 1.

1918 b Comparative studies on the growth of the cerebral cortex.

V. Part I. On the area of the cortex and on the number of cells in a

unit volume, measured on the frontal and sagittal sections of the

albino rat brain, together with the changes in these characters ac-
cording to the growth of the brain. Part II. On the area of the
cortex and on the number of cells in a unit volume, measured on the
frontal and sagittal section of the brain of the Norway rat (Mus
norvegicus), compared with the corresponding data for the albino rat.
Jour. Comp. Neur., vol. 29, no. 2.

AUTHOR’S ABSTRACT OF THIS PAPER ISSUED
BY THE BIBLIOGRAPHIC SERVICE, MARCH 30.

ON TACTILE RESPONSES OF THE DE-EYED HAMLET
(EPINEPHELUS STRIATUS)!

W. J. CROZIER

1. The observations herein discussed grew out of a first attempt
to examine the physiology of excitation of the ‘common chemical’
sense in a teleost bearing a well-developed investment of scales.
The work contemplated was rendered impossible, for reasons
which will shortly appear, but the cause of the failure has a, dis-
tinct bearing upon the original problem and a certain signifi-
cance in several other directions as well.

Epinephelus striatus Bloch, the ‘hamlet’ or ‘grouper,’ was
used in these experiments. The tests which were contemplated
involved the local application of. solutions to the skin of the
hamlet, and it was necessary to employ fishes in which the
chance of visual response had been eliminated. Recourse was
had to the removal of the eyes rather than to the use of temporary
blinding devices. Hamlets are exceedingly handy, and the re-
moval of one or both eyes, usually while under chloretone anaes-
thesia, was followed. by quick recovery. Blinded individuals
lived in the laboratory for more than four months.

In preliminary tests different regions of the surface of de-eyed
hamlets were examined by applying to them from a pipette small
volumes of acid and other solutions. Control experiments quickly
demonstrated, however, that these fishes were reactive to the
mere presence (or near approach) of the undischarged pipette,
even when it contained only sea-water. A thoroughly cleaned
glass rod, when carefully brought near a de-eyed hamlet, also
induced responses of a deliberate and well-defined character.

A very pronounced degree of sensitivity is manifest in these
responses, and the source of stimulation is rather precisely located

1 Contributions from the Bermuda Biological Station for Research. No. 86.
163

164 W. J. CROZIER

by the blind fish. When a clean glass rod is carefully and very
slowly brought near one side of the head, say to within 4.5 or 5
em. of the gill cover, the fish bends in the opposite direction and
swims slowly backward; or it may back deliberately away for
10 or 15 em., then abruptly turn away from the side stimulated
and assume a position at right angles to that held before being
stimulated. When one side of the caudal peduncle is stimulated
in this way, the tail is caused to bend away from that side, and the
fish swims forward and usually turns in a complete half-circle
away from the area of activation.

Unblinded fishes, when not resting on the bottom, usually give
somewhat similar responses, although rarely so if any region
other than the anterior end is being ‘stimulated’ by the near
approach of a glass rod. With de-eyed individuals the best re-
sults are obtained when the fish is quietly swimming or is sta-
tionary in mid-water. As noted by Jordan (’17, p. 447), the
normal hamlet usually les on the bottom of an aquarium, par-
ticularly in the angle between a wall and the base of the con-
tainer. When in the latter position, the hamlet does not usually
react by body movements to the close approach of a glass or
metal rod, although eye movements and increased vibrations of
the pectoral or other fins may show that the foreign object is
seen and perhaps also sensed in some additional manner. It
frequently happened that responses of the kind described were
not obtained from totally blinded hamlets when they were in a
similar position; that is, when they were resting in a corner of
the aquarium.

This applies also to hamlets from which only one eye had
been removed; animals so prepared characteristically seek a
corner of the aquarium?—a dark corner, if such be available—
and for long periods remain in a fixed position with the side

° The aquarium used in most of these experiments was that already described
in Jordan’s paper (717). It had solid wooden ends and plane glass sides. In
working with hamlets having one or both eyes functional the arrangements were
such that the experimenter was screened from the fish, and the glass, or other,
rod was suspended from above and moved about by an appropriate arrangement
of strings.

TACTILE RESPONSES OF DE-EYED HAMLET 165

carrying the intact eye pressed against the confining wall. They
seldom, if ever, moved in any way as the result of a solid object
being brought near them on the blind side, although when actu-
ally touched on that side, however lightly, they made exceed-
ingly violent escaping movements—much more vigorous move-
ments, in fact, than are ordinarily evidenced by the normal
seeing fish.

Whether or not the delicate form of sensitivity described for
the completely blinded hamlet is present and actively functional
in the unblinded animal cannot be decided from the facts so far
given; but it can be shown that the responses in question are
not the result of special sensory alterations determined by or
during anaesthesia, since 1) different anaesthetics (chloroform,
ether, chloretone) and various degrees of narcosis could be used
for the de-eying operation without affecting the result in any way;
2) there is no discernible increase in sensitivity after a fish pre-
viously de-eyed has recovered from a second anaesthetization ;
3) a non-de-eyed fish does not give responses of the character
under discussion after recovery from (chloretone) anaesthesia;
4) several hamlets from which the eyes were removed without
anaesthesia, gave well-defined reactions of this nature.

Inasmuch as the reactions to the careful approximation of solid
bodies were secured very shortly after the operation, and were
evident almost to their maximal extent within twenty-four
hours, it is doubtful if the mere absence of the eyes has produced
this form of sensitivity; the following results, as well as the
studies upon normal individuals, support such a conclusion:

a) When the eyes of a medium-sized hamlet were covered by a
eap of black velvet, the fish became very restless (owing to me-
chanical irritation of the harness required to fasten the cap);
but after about ten hours, good ‘avoiding reactions’ were ob-
tained upon the careful approach of a glass rod, both at the
snout and at the caudal peduncle.

b) In several hamlets the cornea of either eye, or of both
eyes, was rendered opaque by searing with a hot iron. The
fishes so treated behaved respectively as did those with one or
both eyes removed.

166 W. J. CROZIER

The delicate sensitivity manifested in the responses of the
blind hamlet upon the near approach of foreign objects is there-
fore not induced by the absence of the eyes or by procedures in-
cidental to their removal; it is present in the normal seeing fish,
although reactions to which it might give rise are largely inhib-
ited through visual and coarse mechanical stimulations (touch).
It is obvious that this form of irritability, if present but unrecog-
nized, might lead to serious errors in the interpretation of differ-
ent phases of behavior not only in the hamlet, but also in other.
fishes where it may occur.

~2. De-eyed hamlets, stationary in mid-water or slowly swim-
ming, but not in contact with the bottom or walls of the aquarium,
were found to show the following regional distribution of sensi-
tivity to the gentle approach of the rounded end of a clean
glass rod (3 mm. diameter): tip of the snout, side of head, caudal
peduncle, top of head, side of body (especially in the region cov-
ered by the pectoral fin when it is folded back on to the body),
anterior edge of the erect spinous dorsal fin, soft dorsal fin,
caudal fin (except near its distal extremity).

The parts are arranged in the foregoing list according to the
vigor of the reactions induced. No well-defined responses could
be secured from the ventral surface of the animal nor from the
pectoral or pelvie fins. The nature of the response varies with
the different regions of the animal; thus, the spinous dorsal was
pulled down close to the body when its anterior edge was
approached, while the soft dorsal responded by vibratory
movements.

About twenty-five individuals were carefully studied to de-
termine the distribution of this sensitivity to ‘contact at a dis-
tance.’ The critical tests were made in filtered ‘outside’ sea-
water (the circulating water of the laboratory being less alkaline
than normal sea-water), and the conditions were so arranged
that no shadows from the body of the experimenter or from the
glass rod fell upon the surface of the fish. These tests were
made upon single isolated fishes in non-running water.

Rods or wires of a number of different materials were found to
induce reactions of this type. In all cases the rods were well

TACTILE RESPONSES OF DE-EYED HAMLET 167

cleaned; metal rods or wires were brightly polished and the
strips of wood were freshly planed. Tests were made with rods
immediately after cleaning and also when they had lain in sea-
water for an hour or more. ‘The substances used were:

Metals: copper, platinum, gold, zinc, cadmium, aluminum,
wrought iron, steel, galvanized iron, and brass.

Woods: ‘cedar,’ spruce, oak, elm and cypress.

Miscellaneous: glass, hard rubber, sealing-wax, soft rubber
(red, white, and black tubing), porcelain, hard paraffin, sand-
stone, and compressed carbon.

The great variety of materials which induced the same re-
sponse is sufficient to show that the process of stimulation did
not depend upon the diffusion of chemical excitants nor (in the ©
ease of the metals) upon any ‘action at a distance,’ either pri-
marily electrical or through the escape of charged atoms of
metal (cf. Mathews, 07). The cadmium stick and the wires of
platinum used in the tests were particularly pure, and no dif-
ference in the response they induced could be detected after they
had been covered with neutral paraffin. The reactions are some-
what variable, and it is conceivable that some substance may
stimulate in this fashion (i.e., ‘chemically’) more than others,
but I could find no evidence of it in the hamlet. This point
was tested with some care, because I had learned from Prof.
G. H. Parker of reactions found by him with the catfish when
approached by metal rods. Nor could I find anything of this
sort in Amphioxus, Balanoglossus, sea-anemones, crabs (blinded),
the ‘rhinophores’ of nudibranchs, or several teleosts that were
examined.

Rods of brass, iron, glass, or wood of different diameters and
shapes were then tried. Fishes of fairly uniform size (about 30
em. length) were used in comparative experiments. ‘To avoid,
as far as possible, communicating undesired trembling movements
to the rods, and thus to the water, the rods were in many tests
clamped firmly in the middle of the aquarium and the behavior
of the blinded hamlet when approaching them during slow swim-
ming movements was compared with the result when a rod was
earefully brought near a part of the body. The result was in

168 W. J. CROZIER

either case the same; when slowly swimming the de-eyed hamlet
will most often neatly avoid contact with a rod or wire situated in
its path, but more successfully if the end or edge of the rod pre-
sents a sharp corner. Similarly, in many cases, the fish is some-
what better stimulated by a thin wire (less than 1 mm. in diame-
ter) than by a thicker one and by a rod of square cross section
than by one of similar size (several centimeters in diameter)
but with a smoothly rounded end and circular cross section.

The inference from these tests is, unavoidably, that mechanical
deformations in the water, of a somewhat zrregular character, are
the means of stimulation. It was shown by appropriate elimi-
nation experiments that the nostrils and lateral-line organs could
not be concerned, and this is further made obvious from a con-
sideration of the local nature and manner of distribution of these
reactions over the body of the fish.’

The mode of excitation in these reactions is in certain par-
ticulars significantly different from that in some reactions which
have previously been attributed to tactile excitation of the skin
in teleosts (cf. Parker, ’04, pp. 61, 62; Jordan, 17). A current
from a pipette or ripples at the water surface frequently failed
to induce any perceptible reaction in a de-eyed hamlet, al-
though immediately after this, or immediately before, a slender
rod or wire slowly brought to within 5 em. of the snout or caudal
peduncle led to well-defined reactions. Moreover, it was often
possible to get good reactions to a thin rod in water much dis-
turbed by a current of relatively large volume.

The snout and lips of the hamlet were the most sensitive re-
gions of the animal’s surface. There is thus a general parallelism
between the distribution of this delicate tactile sensitivity and
that of skin sensitivity to currents, as described by Jordan (’17).
Whether or not this indicates the actvity of the tactile corpuscles
in the reactions herein discussed, I am not sure; but I suspect
that the tactile corpuscles may not be involved, although con-

It may be suggested that the reactions of Amoebae to insoluble substances,
as described by Schaeffer (’16), are possibly due to some such form of irritability
as that herein considered. Certain peculiar phenomena obtainable with human
erythrocytes (Oliver, ’14; Kite) are also suggestive in this connection.

TACTILE RESPONSES OF DE-EYED HAMLET 169

clusive evidence for this belief cannot be adduced. The higher
sensitivity of the anterior end of the de-eyed hamlet was not
occasioned by the presence of freshly exposed tissue surfaces in
the orbits or by other injuries, since in several cases the animals
were kept in aquaria for more than four months, long after the
orbit surfaces had cleanly healed, and their reactions were as
distinct as those of recently de-eyed fishes.

The relatively acute sensitivity of the region behind each
pectoral fin, as judged by the reactions obtained when it was
approached by a rod, is probably a secondary condition, due to
the fact that the pectoral fins are usually in slight motion, creat-
ing in the water waves which impinge upon thgse surfaces; any
disturbance of these wave fronts or fin currents would result
in a greater stimulus than that afforded by the near approach
of a rod or wire to a stationary part.

3. I have ventured to describe these tactile reactions of the
de-eyed hamlet at some length, because the fine, ‘epicritic’ nature
of the sensitivity evidenced toward minute mechanical disturb-
ances in the water is of particular use for the purposes of cer-
tain critical experiments regarding chemical stimulation of the
skin of fishes. It will be observed that crude tests made by
applying solutions from a pipette to the skin of Epinephelus
would be quite pointless, since the blinded fish reacts with pre-
cision to the presence of the undischarged pipette. The degree
of sensitivity in these delicate tactile reactions is nevertheless
rather definitely fixed at a uniform level, as seen in the more than
twenty-five individuals I have examined. The speed, vigor,
and amplitude of these reactions give them a perfectly definite
character. It is conceivable that this tactile sensitivity might
be enhanced or diminished under various conditions and that
such variations would be reflected in the behavior of the de-eyed
fishes, and that, in fact, a good opportunity would be offered
for discovering the way in which tactile terminals may be influenced
by such treatment of the skin as is involved in the local applica-
tion of chemical excitants. If, as is supposed by Coghill (14,
p. 197; ’16, p. 302), those responses of fishes and amphibians
usually regarded as being initiated through excitation of ter-

170 W. J. CROZIER

minals representing a ‘common chemical sense,’ are in reality
due to the heterologous activation of tactile and pain terminals,
owing to destruction of the epithelium, then it would be expected
that the local application of irritants to the skin of the hamlet
would produce one of two effects; either tactile sensitivity would
be noticeably increased immediately thereafter or, following
relatively severe treatment, it would be found more difficult to
bring about tactile activation. In the former case it might be
held that excitants for the ‘eommon chemical’ sense are capable
of acting upon tactile receptors in a sensory way. —

In testing this matter, my experiments dealt mainly with the
areas of skin on @ther side of the caudal peduncle, although other
regions were also examined, notably, the lips and gill-covers.

In different individuals these areas were treated with solutions
of cocaine hydrochloride in sea-water by painting the surface in
question (held out of water) with a brush. The dermal chromat-
opores in the region cocainized quickly contract and remain con-
tracted for some hours. The area treated is sharply outlined
by the blanching of the skin. The narcotized area is thus
clearly delimited for reference in stimulation trials.

Even slight cocainization causes a complete suppression of the
sensitivity to rods or wires, as well*as to water currents; slightly
stronger narcosis obliterates all responses to touch. Even then,
however, the anaesthetized surface is fully active in the reception
of stimulation from acid and alkaline solutions (HCl, NaOH,
NH,OH, n/20-n/40) or from dilute solutions of quinine. The
sensitivity to delicate mechanical stimulation in these experi-
ments returns with equal rapidity whether or not the narcotized
area has been stimulated chemically while under anaesthesia.

The hamlet, normal or de-eyed, reacts to local treatment with
n/20 NaOH or NH,OH on the caudal peduncle after the spinal
cord has been transected, but this operation obliterates the sen- |
sitivity to minute mechanical disturbances at all levels poste-
rior to the cut and decreases the amplitude of responses of this
nature in other regions.

+A view suggested also by Watson (714, pp. 419) and apparently accepted in
some degree by Herrick (’16, pp. 85).

TACTILE RESPONSES OF DE-EYED HAMLET ike al

By several stimulations in rapid succession the vigor of the
response elicited upon the near approach of a glass rod may be to
some extent heightened. Such reactions are never so vigorous as
those ealled forth by acid or alkali. If, however, tactile stimu-
lation by this means be induced immediately after relatively
severe chemical irritation (n/10 HCl from a pippette), it is found
either that the local irritability is quite unaffected or that it is
slightly decreased. With weaker acid, inducing, nevertheless,
very vigorous reactions, no effect could be detected upon subse-
quent excitability by the near presence of glass rods or wires.

The results of the test thus briefly outlined are uniformly in
agreement with the idea that (within physiological limits) the
excitation of the ‘common chemical sense’ has nothing to do
with tactile receptors or with the destruction of the epithelium,
since the delicate form of ‘touch at a distance’ employed in the
de-eyed hamlet shows no specifie effects of a sort otherwise to
be expected when the receptive areas of this sense are bathed with
chemical excitants. These results make it impossible to sup-
pose that acid, for example, could disorganize the skin (as sug-
gested by Coghill) sufficiently to induce violent painful excita-
tion and yet at the same time leave sensitivity to minute mechani-
cal disturbances practically unaffected.

And if acid acted directly upon tactile receptors, it would be
expected that organs of delicate tactile receptivity would behave
toward subsequent mechanical activation as if they had recently
been activated; as previously described, this is apparently not
the case. It might be objected that the source of stimulation
could not, in the ‘tactile’ experiments with wires and rods, be
localized with sufficient precision for critical use. Yet this would
be incorrect, as could very nicely be shown in tests made upon
small narcotized areas of the skin. Regions (on the caudal pe-
duncle) not more than 2 em. in diameter were painted with cocaine,
and when the pale anaesthetized part was approached with the
end of a thin rod, no reactions followed, although similar spots
3 cm. away were of fully normal sensitivity.

This result confirms the conclusion which I supported in a pre-
vious paper (716), to which Coghill (’?16) has made further and (it

172 W. J. CROZIER ;

seems to me) quite unwarranted objection. According to a
conception first formally advanced by Botezat (’10) and later
applied by Parker (712) to the general chemical irritability of
moist surfaces in vertebrates, the stimulation of epithelial free
nerve terminals is accomplished secondarily through the activity
of substances diffusing from the more external epithelial cells
(some of which may be supposed to be in a special receptive state,
although this is not necessary) to deeper parts. There is ob-
viously no necessity that the nerve terminals concerned be situ-
ated near the surface immediately exposed to the activating agent.
The cells primarily activated by acid or alkali in the ‘common
chemical sense’ experiments are undoubtedly those of the very
outermost layer of the skin. A study of the conditions of chemi-
cal activation in primary receptors (of the earthworm) shows,
or seems to show, that a chemical reaction occurs between the
activating agent and some receptor constituent.°

This means that the acid or other agent stimulates after union
with, or penetration of, the surface of the superficial cells. The
acid or other substance does not act directly upon deeper layers
of the skin, for the good and sufficient reason that the stimula-
tion time is utterly inadequate for any such process, even though
the changed condition in the cell primarily affected can obviously
be transmitted from cell to cell through the whole depth of the
epidermis in a very brief time. The fact that one small area
of the skin may be excited repeatedly by acid or by alkali shows
that no destructive action is wrought by these excitants (within
reasonable limits of concentration).

It is becoming more and more necessary to recognize that re-
ceptor organs depend for their differential irritability upon the
possession of specific substances which enter into excitation re-
actions. There is reason to suppose that in mechanical stimu-
lation surfaces (intracellular, intercellular, or both) are tempo-

5 Some of the results of this investigation are in course of publication.

6 This primary effect may or may not be an increase in cell permeability, but
it undoubtedly does involve an alteration in the relations between ions at the
surfaces of the stimulated cells; hence the violent stimulating effect of distilled
water under certain circumstances, as Loeb long ago found in the case of the
frog’s foot.

TACTILE RESPONSES OF DE-EYED HAMLET 73

rarily broken down, to a certain extent, so that substances nor-
mally kept apart are free to intermix and react. There is no
reason to expect that the products of the chemiéal activation of
epithelial cells should be able to bring about a specific action
upon tactile nerve endings or upon the specialized accessory end
organs of the tactile sense. ‘Tactile organs, ‘corpuscles,’ or what
not may obviously be (and in fact frequently are) situated at
some distance from the outer epithelial surface; it is probable,
however, that the ‘epicritic’ form of irritability described in the
hamlet depends upon very superficial structures; hence their
particular value for the present research.

These considerations may enable one to see why it would be
somewhat surprising to find tactile organs in fishes capable of
being normally excited by acids, for example.

It is easily seen that differential anaesthesia is, by itself, in
many cases a poor criterion of sensory differentiation; and yet, in
the case of cocaine, when the results obtained by this method
agree perfectly with other and quite independent methods of analy-
sis, the results must perforce be accepted. In the present case
it is rendered probable that the production of stimulation by
chemical irritants applied to the general surface of Epinephelus
has nothing to do with tactile receptors, and that the oblitera-
tion of tactile (‘epicritic’) sensitivity by cocaine is not an “arti-
fact’ due to the specifically more intense action of the chemical
irritants. Even in coelenterates there are indications that irri-
tant chemicals and mechanical agencies respectively act in a
sensory way upon differentiated receptors having diverse inter-
nal connections (Parker, ’17), and the present observations con-
firm the idea that these agencies have modes of action in lower
vertebrates as separate as they are in man.

4. Responses similar to those described for the de-eyed ham-
let are exhibited by the normally blind cave fishes, according to
- Eigenmann (cited by Whitman, ’99, p. 303). The parallelism
is striking, since in both cases the direction from which a rod is
being brought near is accurately located, while vibrations of a
coarser order may not be responded to. Inthe blind fishes, how-
ever, this form of sensitivity is said to be more active in younger
individuals than in adults.

THE JOURNAL OF COMPARATIVE NEUROLOGY, VOL. 29, NO. 2

174. W. J. CROZIER

Inasmuch as tactile sensitivity of a very highly developed
character is present in the hamlet possessing well-developed func-
tional eyes, there is no reason to believe that a similar superior
degree of tactile irritability has been developed in the blind cave
fishes as the result of their lack of vision.’

Concerning the function of this sense in Epinephelus, it may be
suggested that it is useful at night or when the fish is maneuver-
ing in darkened crannies of the ‘coral reefs.’

SUMMARY

The de-eyed hamlet (Epinephelus striatus) gives well-defined
reactions to the near approach of solid bodies. In the seeing
fish this form of sensitivity is present, but motor effects which it
might induce are almost completely inhibited. Mechanical de-
formations in the water of very minute amplitude and of a some-
what irregular nature are the source of stimulation in these re-
sponses, which cannot be attributed to chemical or to electrical
disturbances. The presence of this exceedingly delicate form of
sensitivity, generally distributed over the surface of the fish and
leading to deliberate reactions of a well-defined character, has
been used to discover any influence of chemical excitants, locally
applied, upon the end organs of tactile sensitivity. Although
the existence of this ‘epicritic’ form of irritability interferes with
any direct study of the mode of excitation in ‘common chemical
sense’ reactions, it can nevertheless be shown, with its aid, that
the generally distributed ‘common chemical’ irritability of this
fish does not involve tactile receptors. Since the hamlet with
well-developed eyes exhibits a high degree of tactile discrimina-
tion, such as has been described for blind cave fishes,—although
the existence of this sensitivity would be quite overlooked unless

71It should be added that after living in the laboratory for more than four
months after the removal of the eyes, three hamlets were carefully compared
with several others recently de-eyed as regards their comparative ‘tactile’
irritability; no differences could be detected. Hence continued lack of vision
does not lead to an increased development of the hamlet’s ‘epicritic’ tactile
irritability. i

TACTILE RESPONSES OF DE-EYED HAMLET ees

blinded animals were studied,—it is unnecessary to suppose that
sensory structures appropriate to this type of irritability have
been determined either by blindness or by life in caves.

AGAR’s ISLAND. BERMUDA.

LITERATURE CITED

Borrzat, KE. 1910 Uber Sinnesdriisenzellen und die Funktion von Sinnesap-
paraten. Anat. Anz., Bd. 37, pp. 513-5380.

Cocuitt, G. E. 1914 Correlated anatomical and physiological studies of the
growth of the nervous system of Amphibia. I. The afferent system
of the trunk of Amblystoma. Jour. Comp. Neur., vol. 24, pp. 161-
233.
1916 II. The afferent system of the head of Amblystoma. Ibid.,
vol. 26, pp. 247-340.

Crozier, W. J. 1916 Regarding the existence of the ‘common chemical sense’
in vertebrates. Ibid., vol. 26, pp. 1-8.

Herrick, C. J. 1916 An introduction to neurology. Phila., 355 pp.

JorpDaNn, H. 1917 Rheotropic responses of Epinephelus striatus Bloch. Amer.
Jour. Physiol., vol. 48, pp. 4388-454.

MartueEws, A. P. 1907 An apparent pharmacological ‘action at a distance’ by
metals and metalloids. Ibid., vol. 18, pp. 39-46.

Oxtiver, W. W. 1914 The crenation and flagellation’ of human erythrocytes.
Science, N. 8., vol. 40, pp. 645-648.

OstrrHOUT, W. J. V. 1916 The nature of mechanical stimulation. Proc. Nat.
Acad. Sci., vol. 2, pp. 237-239.

Parker, 8. H. 1904 Hearing and allied senses in fishes. Bull. U. S. Fish.
Comm., vol. 22 (for 1902), pp. 45-64.
1912 The relation of smell, taste, and the common chemical sense
in vertebrates. Jour. Acad. Nat. Sci., Phila., Ser. 2, vol. 15, pp. 221-

234.
1917 Nervous transmission in the actinians. Jour. Exp. Zodél., vol.
22, pp. 87-94.

ScHaEFFER, A. A. 1916 On the behavior of Ameba toward fragments of glass
and carbon and other indigestible substances, and toward some very
soluble substances. Biol. Bull., vol. 31, pp. 303-326.

Watson, J. B. 1914 Behavior: an introduction to comparative psychology.
New York, xii + 489 pp., ills.

WuitTman, C. O. 1899. Animal behavior. Biol. Lect., Mar. Biol. Lab., Woods
Hole (1898). Boston, pp. 285-338.

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AUTHOR’S ABSTRACT OF THIS PAPER ISSUED
BY THE BIBLIOGRAPHIC SERVICE, MARCH 30

COMPARATIVE STUDIES ON THE GROWTH OF THE
CEREBRAL CORTEX

Vil. ON THE INFLUENCE OF STARVATION AT AN EARLY AGE UPON
THE DEVELOPMENT OF THE CEREBRAL CORTEX. ALBINO RAT

NAOKI SUGITA
From The Wistar Institute of Anatomy and Biology

TWO CHARTS
1. INTRODUCTION

Investigations on the influence of partial or complete starva-
tion upon the growth of the body under various conditions have
been made by many authors, and it has long been known that of
all the organs the brain is least affected in weight by underfeeding
while, in younger animals in active growth, the brain weight may
even increase during severe underfeeding. ‘These facts were
early observed by Chossat (’48) in pigeons, Falck (’54) in dogs
and Voit (66) in cats, later by Bechterew (95) in kittens and
puppies and Lassarew (’97) in guinea-pigs, and recently by
Hatai (04, ’08, 715), Donaldson (’11), Jackson (15 a, 715 b), and
others working in the albino rat. Jackson made experiments
with complete and partial starvation on adult albino rats and
also held the young albino rats at constant body weight for a
considerable period by partial underfeeding, and in all his experi-
ments the brain was found to be only slightly affected in weight.
Hatai underfed young rats so as to cause a reduction of 30 per
cent in total body weight, while the average loss in brain weight
was only 5 per cent. According to Donaldson’s experiments on
the young albino rats (thirty days old) under moderate under-
feeding for three weeks, it was found that the underfed are on the
average 41.2 per cent less in body weight than the controls and
nevertheless only 7.7 per cent less in brain weight.

177

THE JOURNAL OF COMPARATIVE NEUROLOGY, VOL. 29, No. 3
JUNE, 1918

178 NAOKI SUGITA

According to my previous studies on the normal development
of the cerebral cortex during the period of most active growth
(Sugita, “17, “17 a, 718 a, “18 .b; 718 ¢), 1t was found that the
growth of the cortex is precocious and that its elementary organ-
ization (that is, the cortical thickness, the cortical cell number
and cell size, ete.) is nearly completed at the time of weaning,
when the albino rat is twenty days of age. The investigations
by the several authors cited above were, however, made mostly
on animals which were already weaned, because, of course, feeding
experiments necessitate a strict food control. But at this stage
(after weaning), the elementary organization of the cerebral
cortex is already completed. For my object, which was to
determine the effect of starvation on the early development of the
cerebral cortex, it was necessary to use animals in which the
growth of the cerebral cortex was still in active progress and to
note the influence upon the organization of the cortex of longer
and shorter periods of inadequate feeding.

For this it is necessary to use the very young animals, still de-
pendent on the mother. During this period the growth impulse
in the brain is especially strong and the results of underfeeding
are somewhat peculiar, as the brain weight may even increase
under severe underfeeding. In complete starvation, growth is
stopped and the brain weight remains constant. Thus, von
Bechterew (’95) studied on new-born kittens and puppies the
influence of complete starvation upon the brain weight. His
results were that the brain weight, at the time of death after three
or four days of starvation, was like the initial weight of the organ
at birth. The brain had not grown, but also it had not lost in
weight.

By applying severe starvation to the albino rat immediately
after birth, it has been my object in the present study to obtain
answers to the following questions:

1. How far will the growth of the body and of the brain be
arrested?

2. Will the normal relation between body weight, body length,
and tail length be modified?

GROWTH OF THE GEREBRAL CORTEX 179

3. What will be the relation between body weight and brain
weight in the underfed rats?

4. How far will the size and shape of the cerebrum be in-
fluenced?

5. Will the thickness of the cortex of the stunted rats be
different from that of the standard?

6. How far will the Volume of the cerebral cortex be modified?

7. Will the number of the cortical cells increase normally
according to age?

8. Will the development in the size of the nerve cells be influ-
enced by starvation?

9. What will be the effect of the starvation on the percentage
of water and on the alcohol extractives?

2. THE TEST ANIMALS

After several preliminary tests on producing underfed young, I
adopted the following three procedures, which are fairly reliable:

I, Separation of the young from the nursing mother for a
maximum period each day.

II. Entrusting one mother with an excessive number of young
and thus reducing the amount of milk available for each of the
young.

III. Underfeeding the nursing mother and thus reducing the
quantity of milk secreted.

I treated five litters by the first method (Series I),-two litters
by the second method (Series IT), and one litter by the third
method (Series III). The detailed records of these experiments
are on file at The Wistar Institute of Anatomy and Biology.
All the material, consisting of forty-six test individuals and four-
teen controls, from the above eight litters, was supplied from the
rat colony at The Wistar Institute. They are all from mothers of
standard size which were kept throughout the experiment under
good sanitary conditions.

This study was carried on from October, 1916 to July, 1917, at
The Wistar Institute of Anatomy and Biology.

180 NAOKI SUGITA

3. MATERIAL
Series I (Litters A, B, C, D, and E, table 1)

Procedure. In each litter, half of the young were selected for
the experiment and marked with hectograph ink on the back and
the remaining individuals were used as the controls. The young
under experiment were taken away from'the mother each day
and kept packed in cotton in a warm place, but without any food
or water, for the time which had been determined. Table 1
contains the records of the number of hours during which each
test individual in this series was isolated each day.

Litter A (born October 16, 1916) was composed of nine young.
Five (ce, a, d, f, and h) were subjected to experiment and were
separated from the mother daily beginning on the very day of
birth, the foodless interval being increased day by day, as recorded
in table 1. Sundays were excluded from any experimentation,
The duration of starvation, daily and total, and the age at which
the animals were killed is recorded also in table 1. Four controls
(b, e, g, and 1) were also killed one by one at the same’ages as the
test animals. The total hours of isolation, the average per day,
and the percentage of hours isolated during the total life of the
individual in hours, are given in the lower part of the table.
As the young are not fed continuously, even when they were
with the mother, this percentage will but roughly indicate the
grade of underfeeding to which the young were subjected. ‘They
were killed for examination at the ages of 3, 4, 9, 11, and 15 days
(see X in table 1).

Litter B (born October 15, 1916) consisted of ten young. Five
(a, ec, e, f and i) were separated daily from their mother, as in the
case of Litter A, and the remaining young (b, d, g, h, and j) were
used as controls. The experiment was begun at the age of one
day in Litter B, a day later than in the case of Litter A. They
were killed for examination at the ages of 4, 8, 11, 12, and 19 days.

Litter A and B represent groups in which mild starvation was
instituted from a very early age.

Litter C (born October 18, 1916) was composed of seven young,
of which four (a, c, d, and f) were used for experiment and three

GROWTH OF THE CEREBRAL CORTEX 181

(b, e, and g) for control. The experiment was begun five days
after birth. One test rat (f) and one control (g) were killed by
the mother. For the first three days mild starvation was tried,
and then, from the age of nine days, severe starvation was
instituted. They were killed for examination at the ages of 15,
17, and 28 days.

Litter D (born October 23, 1916) consisted initially of eight
young, of which five (a, c, d, e, and g) were used for experiment
and three (b, f, and h) for control. One underfed (g) and one
control (h) were killed by the mother. In this litter severe
starvation was begun at the age of three days. The animals
were killed at the ages of 9, 10, 16, and 18 days.

Litter E (born November 4, 1916) was composed of eight rats,
of which six (a, b, e, d, g, and h) were selected for experiment and
two (e and f) for control. Severe starvation with some intervals
of feeding was begun at the age of three days. In this litter pairs
of test rats of the same age were killed for examination (on the
7th, 10th, and 17th days of the experiment) to determine indi-
vidual variations.

Litters D and E represent groups in which relatively severe
starvation was begun at an early age.

Series II (Litters F and H)

Procedure. In this series one nursing mother was placed in
charge of an excessive number of young. The results were not
very good, because some relatively lucky or strong ones always
got more than their share of milk, while the others were in a con-
dition of severe underfeeding.

Litter F (born October 15, 1916). To a young small primipara,
which had just given birth to ten young, were entrusted ten more
young from two other litters which had been born on the same
day. Unhappily, the young from three different litters were
not separately marked. The rate of growth among them was
later found to be unequal, owing probably partly to litter char-
acteristics and partly to the inequality of the milk ration. Indi-
viduals were selected arbitrarily and killed for examjnation at
intervals of one to three days (at the ages of 11, 14, 17, 19,

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184 NAOKI SUGITA

20, 23, 24, 26, 30, and 40 days). Those killed were replaced
by individuals of like age from other litters, so as to keep the
number in this litter always above thirteen. After twenty days,
the mother was removed and the young fed with a small amount
of ordinary food. ‘The last eight young, which survived beyond
the age of forty days, were rejected as too old for the purpose of
this study.

Litter H (born January 2, 1917). A mother having just given
birth to eight young was entrusted with nine more young from
another litter which had been born on the same day. The
underfed young of this litter were all employed for the study on
the percentage of water and for the histological study of myelina-
tion in the brain and not included in the study of the cerebral
cortex.

Series IIT (Litter G)

Litter G (born October 23, 1916). In this series a nursing mother
was severely underfed immediately after the parturition. This
litter consisted of eleven young. Only a fraction (one-tenth to
one-twentieth) of the ordinary diet with unlimited water was
supplied daily to the mother. She was found to lose slowly
in body weight day by day. The amount of milk was conse-
quently much reduced, but not completely stopped, as could be
determined by examining daily the stomach contents of the
young. By this method I was able to get a series of young which
were very poorly developed. The young were killed for exam-
ination at the ages of 8, 10, 11, 12, 15, 16, 18, 22, and 25 days.

Table 2 contains the observed body weight and brain weight of
the young in Litters F, G, and H, when examined, for a com-
parison with table 1.

4. BODY WEIGHT, BODY LENGTH AND TAIL LENGTH

Table 3a (not published, because of its complexity, but on file
at The Wistar Institute).-gives for each individual in this study
the sex, age, observed body length, tail length, and brain weight.
The standard tail length and the standard brain weight for the
observed body length were also entered for comparison, the

GROWTH OF THE CEREBRAL CORTEX

TABLE 2

185

Showing for each test individual in Series II and III (Litters F, G, and H) the
sex, age, and body and brain weights, at time of examination

ety Gs SEX AGE OF KILLING BODY WEIGHT BRAIN WEIGHT
days grams « grams
Fa m 11 8.5 0.709
b f 14 9.8 *0.954
¢e f 17 13eo 1.106
d f 19 Bo3} 1.218
e m 20 12.4 1.148
f m 23 ieS2 1.230
g it 23 142 1.224
h m 24 1133.5) 70
1 f 26 17.0 1.197
j f 30 24.2 1.219
k m 30 18.7 1222.
] f 40 40.0 1.310
Ga m 8 Kok 0.679
b f 8 7.4 0.703
c f 10 10.3 0.864
d m 11 9.8 0.929
e f 12 8.8 0.907
f m 15 oe 0.881
g m 16 0.3) 0.948
h m 18 9.6 1.119
1 f 22 22 1.110
j m 25 Wise 1.234
Ha f 13 8.8 0.880
b f il) 10.8 1.024
c f 23 14.7 Ihe WSS}
d f 28 peo 1.166
e m 32 20.0 1.215
f ii 37 19.3 OH
g m 43 Pala il 1.295

’

values having been calculated for each individual by the use of
formulas given in ‘The Rat’ (Donaldson, ’15).
length was chosen as the basis for comparison, because the in-
crease in body length has proved less variable than body weight.
Table 3 was condensed from the original complete table (table
3a) by dividing the individuals, the tests, and controls within
each litter into two groups, according to the observed brain

Here the body

186 NAOKI SUGITA

weight and taking averages for each group. Group I consists
of those which have brains weighing less than 1.0 gram and pre-
sumably still in the first phases of cortical development (Sugita,
"17 a) and Group II those which have brains weighing more than
1.0 gram and probably in the second or third phase of cortical
development. So, one litter in Series I was divided into four
groups, the tests having brain weights less than 1.0 gram (T. I),
the tests having brain weights more than 1.0 gram (T. II), the
controls having brain weights less than 1.0 gram (C. I) and the
controls having brain weights more than 1.0 gram (C. II).
This grouping prevails throughout all condensed tables (tables
3 to 13, 16 and 17) published in this paper. The average values
were all obtained according to individual measurements, and the
average standard values were also obtained by averaging from the
full tables, which give the individual cases. As the standard
values were not based on the average measurements given in the
condensed tables, those standards given in the condensed tables
sometimes deviate slightly from the standard values which
would be directly obtained for the given average measurements.

On comparing, in table 3, the observed measurements with the
corresponding standards, no significant difference between them
has been detected, either in the underfed or in the controls,
Only the body weight in the underfed is slightly lower as com-
pared with the standard for the same body length, but it amounts
to no more than 8 per cent.

This comparison indicates that, though the underfed young
show a considerable retardation in total growth according to age
(see table 4), yet the relation between the body and the tail
lengths and the body weight is but little affected, at least during
the early period of active growth. So the only marked differ-
ence between the underfed and the controls of the same body
length or body weight would be the age, if their brain weights are
disregarded. The effect on the brain weight will be discussed
in the next chapter.

TABLE 3

GROWTH OF THE CEREBRAL CORTEX

187

Giving for each litter group in this study the average age, body length, tail length,
and body weight, the last two compared with the corresponding standard measure-
nents for the observed body length, calculated according to sex by the use of formulas

given in ‘The Rat’ (Donaldson, ’18).
trol groups are given at the foot of the table.

The general averages for the test and the con-
Ti ateSi a Ok—RCOninales

TAIL LENGTH BODY WEIGHT
SERIES, LITTER AND TEST * esi AVER- BODY Standard Standard
GROUP CONTROL ORS AGE AGE| LENGTH Ob- accord- Ob- accord-
+ served ibe te served he ae
length length
Series 1 days mm. mm. mm. grams grams
A ©, By Cui To IE ah samy 334% 7 06.3) |) 260255 26n3 One ell
h Ate ul lef 15 74.0 48.0 47 .0 13.9 13.9
b, e, g Cr 3m 8 66.7 BLS 7 37 .0 ILS 10.2
1 CeuL 1a 17 96.0 62.0 (lat) 30.1 26.3
Series I
B a, ¢, e, f Ate 3 met 9— 59.8 27.8 29.8 Tas hoe)
1 sleeeslili 1m 19 75.0 50.0 46.0 PASE 136
b, d (Gy I Dita 6 57.0 2580) CH es) ipl 7.0
Ces I} rat Bot 18— 86.3 53.3 C173 20.5 2013
Series I
Ca,ec,d ANS IM |) Bicone aT ae 20 82.0 Died O4.503 om Hip Ai
b,e Gy IL Dit 22— 98.5 leo) T3820 PM) 29.4
Series I
Da,c,d Ref ame Dat 12— 61.0 39.0 bulb 6.9 8.2
e ‘WS MM 1m 18 78.0 | 54.0} 49.0 IBROR el o.0
b (pt 1m 9 69.0 39.0 40.0 Ws TRO)
f Cem 1m B22; 91.0 65.0 63.0 24.0 21.9
Series I
awe cacd ale Sesomee let || 2 — GOESH | coe O! || sbn8 od 9.9
g,h at). Ju Dia 20 82.0 58.0 56.0 16.2 ae)
e, f (CAS Miami aletal al — SON 56250) 6OTOn e216 ‘0.4
Series II .
F a, b Ww 1m,1f 13— 63.5 33.0 84.6 9. 9.1
c-] A, OL Abia, Ge 25+ 83.9 61.5 Nf ol 18.1 19.4

188 NAOKI SUGITA

TABLE 3—Continued

TAIL LENGTH BODY WEIGHT
SERIES, LITTER AND TEST i AVER- BODY Standard Sta adard
GROUP CONTROL SES AGE AGE| LENGTH Obe accord- Ob- accord-
served is = s ¥ served ia ae

length length

days mm. mm. mm. grams grams

Series III |
G a-g ghee 4m, 3f 11+ 63.0 32.9 Bom 8.3 8.8
h-j AUS ME PPA roa, Tt 22— Ua) 48.7 46.7 13.0 Aaa
Series II y

Ha aT I i 13 63.0 33.0 34.7 8.8 OE

b-g AUS OE |) ysan, 2bral x0 81.7 64.0 53.8 Le oP TEP oll
Average } sega tS | GS | SR cy S22 8.6
«(Series I-II1) 4b; Ju 21+ 79.0 54.5 61.2 14.9 Gra
Average \ Cli S642 32 esa ORO 9.4
(Series I) (Oe) IO 19+ 91.8 61.7 65.8 24.8 yt,

‘

5. BODY WEIGHT AND BRAIN WEIGHT

Table 4 was condensed from table 4a (unpublished), which
gives data for each individual in this study, and shows for each
group, in the three series, the sexes, average age, average duration
of starvation (denoted by percentage value of the hours of iso-
lation), and the observed body and brain weights, accompanied
by the average values for the group of the individual standard
weights, for the same ages, and of the individual standard brain
weights for the same ages and for the same body weights. For
the calculation of the standard values for each individual the sex
was regarded, because in body and brain weights the sex differ-
ence is clear (‘The Rat,’ Donaldson, ’15). The average differ-
ences of the observed values from the standards are given for each
group in percentage, the standards being taken, respectively,
as the norms for comparison.

A glance at the table reveals three differences which are clearly
marked:

1. The underfed rats have, as a rule, body weights consider-
ably less than the standard values for the same age.

GROWTH OF THE CEREBRAL CORTEX 189

2. The underfed rats have brain weights somewhat less than the
standard values for the same age.

3. The underfed rats have brain weights mar edly higher than
the standard values for their observed body weight.

It was already noted in the introduction that the central
nervous system as represented by the brain suffers little or no
loss of initial weight even in the case of severe starvation. In
my series—-underfeeding of the albino rat at an early age—the
body weight of the rats stunted by starvation, as compared with
the standards for the same age, were deficient (on the average by
litters, table 4) by from 19 to 44 per cent. On the other hand,
the brain weights were less than the standards for the same age
by from 4 to 12 per cent (for litters, table 4, but by from 3 to 17
per cent for individuals, table 4 a), while for the same body weights
they were from 15 to 29 per cent (for litters, table 4, but up to 65
per cent for individuals, table 4 a) above the standard values.

Considering together all the five litters (A to E) of Series I,
in which the young were starved by separating them at an early
age from the mother daily, it appears that the underfed rats at
the end of the first twenty days after birth (during the suckling
period) are about 29 per cent (average of A, T. I and II, B, T.
handlinG 7k. la Iland hand; Ts T.and. il) behind
the standards in body weight, while they are only 8 per cent
(averge of the above-cited cases) behind in the brain weight.
In Series IT and III, in both of which the young were subjected to
early and continuous underfeeding, increasing in intensity, by
the method of reducing the ration of milk, but without removal
from the nest, the underfed young have shown a slightly better
development in brain weight (in relation to body weight), the
average being also 8 per cent (average of F, T. I and II, G, T.
I and IJ, and H, T. I and IJ) less than the standard for the same
age, while the body weight is on the average as much as 39 per
cent (average of the above-cited cases) below the standard value.
Whether removing the young from the nest increases the relative
effect of underfeeding on the brain, as these results suggest, can
be determined only by experiments with that question as the.
main point in view.

190 NAOKI SUGITA

In connection with the underfeeding, as practiced in Series I,
some interesting results of overfeeding have been noticed in the
control animals; overfeeding having taken place in the case of the
controls of Litters A to E on account of the periodic isolation of a
number of the members of the litter. The controls have shown
generally, as seen in table 4a (unpublished) and also in table 4,
some excess in body and brain weights, as compared with the
standard values for the same age. The excess in body weight is
on the average 19 per cent (average of A, C. I and II, B, C. I and
II, C, C. II, D, C. I and II, and E, C. II), while the brain weight
is on the average 6 per cent (average of the above-cited cases)
higher than the standard for the same age and 2 per cent higher
than the standard for the same body weight. Thus, by moderate
overfeeding, the growth in body weight is definitely accelerated
and, at the same time, the growth in brain weight is also acceler-
ated, nearly in proportion to the increase in body weight.

If the observed brain weights are compared with the standard
brain weights for the observed body weight, it is clearly seen
that the observed brain weights are higher than the standard by
24 per cent (average of all eight litters T. groups only). Of
course, the younger the individual, the higher is the percentage,
because the standard brain weight is smaller in the young animals
and they are not increasing in direct proportion to the body
weight, but nearly as the logarithm of the latter value. So it
may be roughly stated that the brain weights in the underfed
young albino rats have values below the standard weights for the
same age and above those for the same body weights, but always
falling nearer to the standard age values.

6. THE SIZE AND SHAPE OF THE CEREBRUM

The five diameters of the cerebrum of the underfed young were
measured and recorded according to the procedure already
described in my first paper of this series (Sugita, ’17, figs. 1 and
2). The measurement W.5, represents the greatest frontal
diameter; the measurement W.D, the frontal diameter passing
the middle point of the fissura sagittalis; the measurement
L.G, the greatest distance from the frontal pole to the occipital

GROWTH OF THE CEREBRAL CORTEX 191

TABLE 4

Show ng for each litter group in this study the average age, duration of isolation
denoted by the percentage of the life span, observed body weight, compared with the
standard body weight for the same age, and observed rain weight, compared with
the standard values for the same age and the observed body weight, respectively.
Standard values were all calculated by the use of the formulas given in ‘The Rat’
(Donaldson, '15). Within each litter the starved animals were divided nto two
groups, T I having brains weighing less than 1.0 gram and T. II having brains

_ weighing more than 1.0 gram. The contro! animals were also grouped in the same
way into two groups, C. I and C. II. Averages were taken within each group.
In lines designated ‘percentage difference’ (abbreviated ‘per. diff.’), the devia-
tions of the observed measuremonts from the standard values were given in per-
centage, the respective standard values being taken as standards of comparison.
At the foot of the table, the average as to the test and control groups are given and
the percentage differences from the standards are also ca'culated

Za
0% | BODY WEIGHT BRAIN WEIGHT
Fales|
ape
Mas Stand
1) otanda-
: TEST AVER-| Po»
Rise tetas ani cON- SEX AGE A a Stand- Stand- eee
TROL AGE Bo = Ob- _|ardac-| Ob- | ard ac- ees a
: = | served jcording | served |cording eeeced
Bo & o ee |t
Bias to age to age body
a weight

days |per cent| grams | grams | grams | grams | grams
Series I
IN Oils at mares fl 7 — 32 7.2 | .9.7 | 0.584) 0.644) 0.441

h 405 BG) bar 15 44 13.9 | 16.5 | 1.024) 1.048] 0.952
(per. diff.) (—19) (— 5)} (+15)
b, e, g Cra 3m 8 11.7 | 10.9 | 0.740) 0.750) 0.790
1 Cra iat 17 SOM Se W278i Ogg sO
(per. diff.) (+44) (+ 9)|(— 4)
Series I
1B) Be Gs al 3am 1h) 9 30 7.3 | 11.4 | 0.644) 0.775] 0.468
i ABs JUG) al seey |) Ae) 44 ee Siar Wl O52 SOL Gor
(per. diff.) . (—34) (—11)| (+24)
b, d Cask Dist 6 Woh 8.6 | 0.543] 0.559) 0.437
g, h, j Comet iris 20.5 | 18.7 | 1.144] 1.118] 1.148
(per. diff.) Gr) Gy DiGCe G6)
Serves I t
Cxaerrd As MANA som, a ail) 2X0) 44 15.1 | 20.4 | 1.105) 1.146) 0.946
(per. diff.) (— 26) (— 4)}(+17)
b,e CLIO Bi 22— PHL AD || FF | UpsxO| WU 2HGa)) LEY
(per. diff.) (+22) (+12))'+ 6)

NAOKI SUGITA

TABLE 4—Continued

SERIES, LITTER AND
GROUP

TEST
cON-
TROL

AVER-
AGE
AGE

SEX

Series I
Dia, cd
e .
(per. diff.)

b
f
(per. diff.)

Series I
Bia, b, c,d
g, h
(per. diff.)

e. f
(per. diff.)

Series IT
Fa, b
e-l
(per. diff.)

Series III
G a-g
h-j
(per. diff.)

Series IT
Jal 6)
b-g
(per. diff.)
Average }
(Series I-III)
(per. diff.)

Average
(Series I-III)
(per. diff.)

\ gfe? Elk

days

2
18

38m, 1 f} 12—
PA si 20

21+

(a)

weight

grams .

0.437
0.921
(+37)

0.782
1.287
(4)

0.664
1.042
(+15)

rhea
Gat)

0.631
1.046
(+21)

0.561
0.871
(+39)

0.600
1.045
(+24)

0.543
(+42)

0.966
(+15)

7 AB
° ef BODY WEIGHT BRAIN WEIGHT
ae eg
Sale
ARR Stand- Stand-
qaab Ob-_ |ardac-| Ob- | ard ac-
2 5 served |cording | served} cording
Bm & to age to age
SEO
per cent| grams | grams | grams | grams
57 6.9 | 14.0 | 0.778} 0.943
65 TSTOM PT SsOn Oso ieee
(—38) (=)
11.2 | 11.8 | 0.870} 0.840
24.0 | 91.7 | 1.220) 1.784
Gia (+ 3)
46 9.7 | 14.8 | 0.8385; 0.977
44 UG Pay) Oe | alee ah ae,
(—26) GES)
PAV GY i tl/face |) I WAS) al OVA
(+25) (+ 9)
9.2 | 14.9 | 0.832) 1.000
Sata e2oe6u| 204 1 Sear
(—33) (= 2)
8.3 | 13.6 | 0.844) 0.914
IS AON et on le Sameer
(—39) |(— 5)
8.8 | 15.1 | 0.880) 1.003
WPAN) GES || Wea eR
(—44) (—12)
EP alee Del Os
(—38) (—14)
V4 SOF 821 67) elas alos
(—31)

GROWTH OF THE CEREBRAL CORTEX 193

TABLE 4—Continwed

Zag
oO | BODY WEIGHT BRAIN WEIGHT
ies ‘
4&6,
pO Ste nd-
: ct ee x TEST AVER-| Pos : [esis ae
Sao enGne Ane CON- SEX AGE | o% & Stand- | Stand- he dae
‘ TROL AGE ARS Ob- |ardac-} Ob- | ard ac- rs abe
8 = | served|cording | served |cording served
B aS to age to age body
5 weight
days |\per cent| grams | grams | grams | grams | grams
Average | =
cee Cal SS 10.0 | 10.4 | 0.718! 0.716] 0.670
(Series 1) f
(per. diff.) (— 4) (+ 0)|(+ 7)
Average
ee 6 \ (Oy I 19+ PU | OMS |) WAZA Tl aleoid| df kes
(Series I) J
(per. diff.) (+27) (+ 9)}(4+ 1)

pole; the measurement L.F’, the sagittal diameter from the frontal
to the occipital pole running parallel to the sagittal fissure, and
the measurement Ht. is the greatest vertical height at. the stalk
of the hypophysis. In table 5, which was condensed from
table 5a (unpublished) for each individual, the average brain
weight, the average measurements W.B, L.G and Ht. are given for
each group, both test and control, compared with the corresponding
standard measurements for the brains of the same weight, which
were originally calculated for each individual using the formulas
formerly presented by me (Sugita, 717), and then condensed.
The measurements L.f and W.D are given, also condensed for
each group, in table 9.

On examining table 5, it appears that the measurement W.B
of the underfed is smaller on the average by 2 per cent (average
of all eight litters, T. groups only) than standard for the brains
of the same weight, while the measurement L.G of the underfed
is greater on the average by 2 per cent (average of all eight litters,
T. groups only). The height in the underfed seems to be slightly
less, by about 1 per cent on the average. On the other hand, if
the controls be considered in the same way, they show also slight
deviations from the calculated standard values, thus, on the
average (Litters A to E, C. groups only), W.£ is smaller by 1 per
cent, L.G greater by 0.8 per cent and Ht. smaller by about 3 per

THE JOURNAL OF COMPARATIVE NEUROLOGY, VOL. 29, NO. 3

194 NAOKI SUGITA

cent in the controls. As a matter of fact, the measurement of
Ht. could not be so accurate on’ account of difficulty in fixing the
dorsal limit, so that these slight differences in Ht. should not be
taken too seriously. The measurement of L.G and W.G can be
made accurately so that these results are trustworthy.

Taking these deviations in the controls into account, the
general statement may be made that underfeeding alters the
shape of the cerebrum, ‘so that it becomes slightly elongated,
when compared with the normal cerebrum of the same weight.
This difference is probably due to the fact that, although the
underfed cerebrum is arrested in growth, it nevertheless tends to
enlarge normally and, as already determined (Sugita, ’17) be-
comes more and more elongated as the age advances.

If, for the brains of like weight, the width-length indices

W.D x 100

obtained by the formula TT aaah eee compared between
the underfed and the controls (compare table 9) or the standard
values (based on table 3, Sugita, 717), it will be seen that the
index value tends to be lower in the underfed, especially in the
members of Litters F and G which were underfed continuously
and rather severely. In the latter litters the index values for
each individual are smaller by 2 to 7 points than the index values
for the standard brains of like weights (the data for these calcu-
lations are contained in table 9a, not here published). The
average index values in Litters F and G are 102 (for T. I groups)
and 97 (for T. II groups), while the corresponding standard
values are, respectively, 106 and 103 (Sugita, 717).

7. THICKNESS OF THE CEREBRAL CORTEX

Tables 6 a, 6 b, and 6c (all unpublished) were originally pre-
pared to give the cortical thickness for each individual as measured
at the localities I to VIII in the sagittal and frontal sections and
to give theaverage cortical thickness in each section and the general
average thickness, to be compared with the respective standards
presented in a former paper (Sugita, 17a). Table 6, which fol-
lows, contains in condensed form the corrected data for the thick- »
ness of the cerebral cortex of the underfed Albinos and that of

TABLE

5

Giving for each litter group in this study the average brain weight and the average
measurements L.G, W.B and Ht. of the cerebrum, each compared with the corre-
sponding standard values for the same brain weight, calculated by the use of the

formulas given by me (Sugita, ’17).

are given at the foot of the table.

The averages for the test and control groups

AVER-— W. B. E.G: Ht.
SERIES, LITTER AND TEST AGE
GROUP CONTROL BRAIN
WEIGHT |Observed|Standard |Observed| Standard |Observed| Standard
grams num. mm. mm. mm. mm. mm. :
Series I
IN G5 fein (oly at aol 0.584 | 10.79 | 10.94 9.69 9.20 6.99 7.06
h eS IE O24s SRO ae MeaGO | D2eSOn|e12e30. 8.45 §.70
b, e, g (Goal OR74 05 63) |e SOF NON | 1On6S oO 7.68
1 CH M2785 MBE Soe |e AOG alse lone sabi 8.95 9.30
Series [
Bya, cent ‘veal OGLE | EE 11 28 |) 10. Zo 9.96 7.36 7.38
1 SUS UE PDO WIS 2I0) || hos Ths PA ested AE AO) 8.50 SEuo:
b, d Cr 0.543 | 10.50 | 10.78 ORS 9.18 6.90 6.95
(x lal Cee AA SRA ele Sull boron elonaas 8.68 9.00
Sertes I
Cran @ Gl ARS EOS RTO TS AON ea 8.70 §.88
b, e CH SISO eles ON TS 63e ese 33 8.83 9.40
Series I
DD Fancy. Alert OR Sr EO er ee i725 10280 7.98 7.92
e ADEIUE | TSO CLO GO) |) PA ray |) TAR 8.60 8.86
b Cra OLSON 2 25a et2260.\) 140) | tt 66: 8.00 8.20
f Cholla 2200 Soon eisesO)| 13230) 13.05 8.80 9.20
Series I
Ka, b, ¢, d plat Once || WACS |) wk /Al | Maes |) POL KG 8.29 8.10
g, h AR OL |) We MAPS) asta os AO PISA GE iO) 8.98 8.95
e, f (Oj, JOE | Te 835 Bs TSAO De CASI ARCs) 8.88 9.05
Series II
F a, b ALi OFSSZe eUZR00N i eroSn pile 50 a3 7.95 8.05
e-l AU, JE |) POE | UBIO Ges) ey bl 2.98 9.30 ils
Series III
G a-g alee: 0.844 | 12.22 | 12.46 | 11.46 | 11.32 8.13 §.69
h-j WW, WE | ab aE) aes Pare dh aless ates |) May UBS |) G0) 8.95 9.00
Average Baal 0.753 | 11.65 | 11.98 | 10.92 | 10.60 7.78 7.87
(Ser. I-III) AGMA OF elise leaner oncom| tel 2 equ ZeG 2, 8.78 §.90
Average } (Opa ORS AG ee 76N) TOR62 5 OEZS 7.47 7.61
(Ser. I) ©, IW) UPR) WB SEO 183.1) Tes 0s 8.83 9.19

196 NAOKI SUGITA

the controls from the same litter, and it gives for each group,
underfed and controls, the average brain weight and the cor-
rected cortical thickness in the sagittal and frontal sections of
the brain, together with the average thickness. The data for
obtaining the correction-coefficient are given in the full table for
each individual, but in the condensed table 6 only the average
values of the correction-coefficients for each group appear.
The application of the correction-coefficient was made in the
way formerly described (Sugita, 17a). The horizontal sections
of underfed brains were not prepared for this study.

Table 6 shows also a comparison of the average thickness of
the cortex in the underfed young with that for the standard
Albino of the same brain weights. As the present study was not
extended to the horizontal sections, the average thickness of the
cortex was determined from only the two kinds of sections from
the same individual and it was compared with the corresponding
average for the standards. In the standards, these values
proved to be within 0.5 per cent of the general average thickness
of the cortex based on the three kinds of sections. Here, in table
6, the standard values were obtained from the somewhat smoothed
curve based on the data formerly presented (table 9 and chart
9, Sugita, ’17a).

Table 6 a (unpublished) for the sagittal section showed for the
underfed that the cortical thickness at the frontal pole (locality
I) is evidently very much greater than that of the controls or
the corresponding standard value for the same brain weight,
comparison having been made on the basis of the data given
formerly (table 6 and chart 4, Sugita, ’17 a). Locality IT was
the next which exceeds in the cortical thickness on the side of the
underfed. Localities III and IV stand in general slightly in
favor of the underfed, but at locality V, the occipital pole, there
was found no notable difference in the cortical thickness between
the underfed and the standard. Asa rule, the cortical thickness
of the normal Albino diminishes from the frontal to the occipital
pole—from locality I to locality V—and the cortex at the frontal
pole increases most rapidly in the early age. This is also just the
order of the excesses in the cortical thickness of the underfed

GROWTH OF THE CEREBRAL CORTEX 197

when compared with the standard values for the brains weighing
the same. The cortical thickness at each locality of the controls
was on the average fairly in accord with the standard (the detailed
evidence for these conclusions is contained in table 6 a, not here
published).

In table 6 b (unpublished), in which the cortical thickness at
localities VI, VII, and VIII of the frontal section was given, it
was also clearly seen that the localities VI and VII are much
greater in the cortical thickness, compared with those of the
controls or the standard values of the same brain weight. The
excess amounts on the average to more than 10 per cent. The
locality VIII, at which the cortex is heterogeneous in laminar
structure, did not show any significant difference in the cortical
thickness, compared with the normal, though in some cases here
and there it was found somewhat thicker in the underfed (the evi-
dence for these determinations is contained in table 6 b, not here
published).

One more notable thing found in the cerebral cortex of the
underfed was that, while in the controls and standards the
locality VII is always somewhat greater in thickness than the
locality VI, the relation has, in many cases (18 out of 44) of the
underfed, proved to be reversed (A a, h; Bi; C a, ec; D d, e;
Pew tks, ect hy G,a,.¢;-2,e andvh)),

Generally considered, the localities which are situated nearer
to the ventricular wall, the locus of the cell division, seem to have
gained much more in the cortical thickness in the case of the
underfed, while the localities remote from the matrix (for ex-
ample, locality V) or the part constructed heterogeneously (for
example, locality VIII) appear to be modified but little by under-
feeding.

As is to be seen in table 6, the average thickness of the cortex
is in favor of the underfed Albinos. If compared with the stand-
ard values for the same brain weight, the average cortical thick-
ness in the underfed young (table 6) is greater than the standard
on the average by 7 per cent (average of all eight litters, T. groups
only), while the controls are greater on the average by only 1.8
per cent (average of Litters A to E; C. groups only). According

198 NAOKI SUGITA

TABLE 6

Giving for each litter group in this study the average age, brain weight, and the
average cortical thickness in the sagittal and frontal sections. The general average
cortical thickness was obtained and compared with the standard value for the same
brain weight, quoted from a previous paper (Sugita, ’17a). The data for each
individual and for each locality of the cortex were originally tabulated in three full
tables (tables 6a, 6b and 6c) which are on file at The Wistar Institute and from which
this table 6 was condensed. The correction-coefficients are given in averages for
each litter group for each kind of section. The averages for the test and control
groups are given at the end of the table.

GaEriON? par oe AVERAGE
SERIES, LITTER AND oes ie cea GE Dae iehian) (Galak oe 7 sens
GROUP on AGP | srarn |Correc-| Corti- | Correc-| Corti- | Corti- | ard for
Bioke AGE |weicHt| tion cal tion cal cal the
coeffi- | thick- | coeffi- | thick-| thick- | same
cient ness cient ness ness brain
weight
days grams mm. ety mm Rae a
Series I
ING, Ba Cl di av, I US Meese) UGG |) Ze ales | aA |p lees || oe @)
h 40. JOU) a5 1.024 Pal | ibaa ibs} || P25) |) WL Sts. |) il 53
\ ley Cyl 8— | 0.688} 1.09 | 1.384 | 1.14 | 1.46 | 1.40 | 1.38
1 (Oe OU) ike 12278) 123) | aie 26) |e 200s Som ees:
Series I
B a, ¢c, e, f APR OS ORC Ni ass ales | al ee al ete a4} | if 4)
1 40 U0) We) T2O52| 20M IRGC R Mas i(alie2 Lon) leo) llerned
b, d C.I] 6 | 0.543] 1.08 | 1.18 | 1.09 | 1.32 | 1.25 | 1.28
fe lol 7 ©. Wi as— | 1.744) 15240) 1 s74 4 2-31 |) 2014) LesSsiees8o0
Series I
@rancrd A 20) DOS) ae 74s 2 oa Ze OS eles O Gs erie taa
b, e Ce 22 SO Ti ei7 al alata inferno
Series I
Da,ec,d ee L2— | On77S| Teale ee O48 abe 24 |e CON eile 2 leon
e Ih JE ke 1.089 IA Wika ciety PSO al Seal a ery
b Cr 9 OersvAO}) eels |) vbatiay beer) al tei |) aleAal |) il @y
f CF 22 1220 A leis = = = 1.82
8 EE | (eee Pose Pies Peat ae ee AS ; Jae
Series I
13) [oy Gy Cl AMS EAE ie COS{oyAy baal WP abesshq) Ibo 283 |) iL @sy | Ae Wes
g, h 4h JN) AO PPA) OA aber Pea) | Pan aksy |] al iss | ile)
e, f Oe IN) TS OH TO) TESS |p algal || Lee | aL ih |)

GROWTH OF THE CEREBRAL CORTEX 199

TABLE 6—Continued

Be eee | amet
SERIES, LITTER AND | (Ge. | “vor ee __ | Stand-
GROUP Teo age | BRAIN Correc- | Corti- |Correc- | Corti- | Corti- | ard for
WEIGHT| tion cal tion cal cal the
coeffi- | thick- | coeffl- | thick- | thick- | same
cient ness cient ness ness brain
weight
days grams mm. mm. mm. mm,
Series IT
F a, b Abe J |) UBS |) OSA) wa ilze ale) ea TLS Le |) GE
c-l eh e25 ela 2O4 ele 24 le Si eles 2a eel one OSm else:
Series IIT
Gag T. 1,| 11+ | 0.844] 1.14 | 1.55 | 1.24 | 1.89 | 1.72 | 1.63
h-] QUE OG) PR | a a) AL | ISAS MES OAsy | Ae ISS | LON HE
Average } Dals| ti— | (ON768| teas | 1467) L2t eae ae Gleliiand
(Ser. I-III) 4M IG) P= |) Oe) PO ae TEP) I 2 TL BY I) a ery
Average } C.1y |) °S=" FO. 7001. 10) | 1.36 | 115 | 255.) 14a, ees
(Ser. I) C. IT} 19+ es TANS |) heey || the ZS es TLS | a see

to table 6 ¢ (unpublished), which gives comparisons of cortical
thickness of the underfed with the standard in each section, the
average cortical thickness in the sagittal section of the underfed
exceeds the standard on the average by 5.3 per cent and that in
the frontal section of the underfed on the average by 8.7 per cent.

8. AREA OF THE CORTEX IN THE SAGITTAL AND FRONTAL SECTIONS

Following the procedures which have been described earlier
for the measurement of the area of the cortex in the sagittal and
frontal sections of the Albino brains (Sugita, 718 b), the data
for the underfed Albinos were obtained. ‘Table 7 presents in
condensed form for each group the averaged data on the corrected
area of the cortex together with the average correction-coefficient
for each group, in the sagittal and frontal sections, respectively.
The observed data, as measured on the slides, and the data for
correction-coefficient for each individual were tabulated in tables
7a and 7b (unpublished), on the basis of which table 7 was
made. In table 7 (and in table 7b) the total areas of the
frontal sections (one hemicerebrum) and the percentage of the
cortical area to the total area of the section are also entered.

200

NAOKI SUGITA

TABLE 7

Giving for each litter group in this study the average brain weight. the corrected areas
of the cortex in the sagittal and frontal sect'ons, and the total area of the frontal
section and the average correction-coefficients for each group for each kind of sec-

tion.

The percentage values of the cortical area to the area of the total section in the

frontal section are also given for each group. This table was condensed from two

detailed tables for individual observed data and the data for the correction-coeffi-

cients. The averages for the test and control growps are given at the foot of the table
SAGITTAL SECTION FRONTAL SECTION
SERIES, LITTER AND Tasie, |p Percent-
’ 3 + f
CHOOE CONnKOM aaa Cone Area of Sore Area of oe conical
efficient Rorcex efficient cortex section Heel
area
grams mm .2 mm.” mm.* per cent
Series I
IN (Op By Cloak os ll 0.584 1.16 14.6 1.18 13.4 | 28.8 45
h TEE | 1024 2 22.2 P28 e22nS) ORO 51
b, g Gra 0.688 1.09 17.4 1.14 L5e2 ip voled 46
1 Cepia ee 27S iL 28} 27.4 IAD Ale al 2 35(0) 50
Series I
Beanie wenat We 0.644 ey 16.9 Iie SPOR eS le6 47
i 405 INE || db: LAO: || ~ Baie iLoeiy/ 2a. 44) 452.7 51
b, d Cr 0.548 1.08 9.1 1.09 GR eZ orl 46
g, h, j C. II | 1.144 1.24) 24.6 Sil 2M | 4ae3 47
Series I
Cra cud ST LOS 1 24.5 1225 2220) e43e6 50
b, e Ce 18307 a 27.8 AG, 222255 AoR0 48
Series I
ID el ‘Ted 0.778 mS 19.4 1,24 79 SOR 50
e She WUE), WeWssy The ay 24.2 28h 2OkOn Peale 49
b Gall 870 tke? 20.6 iil MeieCe | Bisets: 48
f Cree le 220) 1.14) 26.7 =
Series I :
13) lo, ©, Cl re 867 pelo 19.9 123 19.8 | 38.4 52
g,h MD JOE |) Te ees 1.20 | 25.9 1.26 | 23.4] 45.9 51
e, f Cale 79 We |p Pee 1h Al 22.2 | 45.2 49
Series II
F a, b TT 02832 air 20.8 1.21 18.6] 38.0 50
e—| Tea AS 204 1.24 | 26.0 IS 2ale 2a tu eas 50

GROWTH OF THE CEREBRAL CORTEX 201

TABLE 7—Continued

SAGITTAL SECTION FRONTAL SECTION
| lavE RAGE| Percent-
SERIES, LITTER AND TEST
, é : BRAIN eee r age of
SROUE CONTROL | WRIGHT HOC Area of Comer Area of aes cortical
efficient | “TX | efficient | Cortex section fe ae
area
| grams mm 2 mm. mm. per cent
Series ITT |
G asg ral: 0.844 1.14 20.1 1.24 19.2 38.5 50
h-} es | ASA: 1.19 25.6 1.26 22.9 46.2 50
Average | Als (ose) pala 18-6 | 1-20) 17.30) 35:2") 49
(Ser. LeIaW Off ADS ARE aaa Oy 1.20) 24.5 1.29 | 22.6) 45.0 50
Average | Cuil ZOOL Peon =athe7 | 1205) 15s") S319 48
(Ser. I) f Coy 2260) eS) 260 | 1.244 99.04! 45.011)» 249
| |

The above-mentioned corrected data for each individual were
separately paired with the corresponding standard values for the
same brain weight, quoted from my previous study (Sugita, ’18 b)
in table 8 a (unpublished) and from this latter table 8 was con-
densed, giving only the averages for each group.

Briefly stated, the area of the cortex in the sagittal section of
the underfed is on the average greater by 1.4 per cent (average
of all eight litters, T. groups only) than in the standard, while
the controls are on the average about 1.9 per cent less than the
standard.

The average area of the total frontal section is in the underfed
ereater than that of the standard by 2.4 per cent (average of all
eight litters, T. groups only), while the controls are less by 3.8
per cent (average of Litters A to E, C. groups only) than the
standard, and the area of the cortex in the frontal section is in the.
underfed greater on the average by 5.0 per cent, while in the con-
trols less by 2.1 per cent, than the standard (table 8). From
these observations, it may be easily concluded that in the under-
fed the proportion of the cortex to the total section is higher than
in the standard or control, as shown by the percentage values
directly calculated for each brain (table 7 b) and given in a con-
densed form in the last column of table 7, where the values are

202 NAOKI SUGITA

TABLE 8

Giving for each litter group in this study the average brain weight, the corrected areas
of the cortex in the sagittal and frontal sections, and the area of the entire frontal
section, respectively, compared with the corresponding standard values for the
same brain weight. The standard values are all entered according to my previous
presentation (Sugita, ’18b). This table was condensed from an original complete
table 8a for each individual. The averages for the test and control groups are given
at the end of the table.

SAGITTAL SECTION FRONTAL SECTION
AVER- Area of cortex Total area Area ot cortex
SERIES, LITTER AND AGE
GROUP BRAIN <
WEIGHT Area Area
Cor- | Stand- Cor- | Stand-| Cor- | Stand-
rected | ard | ppicg-| rected | ard | rected} ard | pick.
ness ness
grams | mm.2 | mm.? mm. mm.2 | mm.2 |~mm.2 | mm.2 | mm.
Series I
Ac) a, det 0.584] 14.6 | 13.8 | 11.4 | 28.8 | 28.3 | 13.4 | 12.9| 8.9
h OPA PPA?) || P23) | eiety | eNOS) ABO | PS ogy || aC I
b, g OF688) ie | 16.10) || 12061) 3195312851525) 15 0N|) On
1 SPARS Pe Ta WP Uy eID, || AS Al Se) LBRO | 1(0)@
Series I
Bvasic ent OVG44/ MGZON 1oeZ 1225) | 306) 304) 15x08) 48. 9.6
1 1052102323) | 2326540) 45.430) || 2oe4al OI On LOS
b, d 05543) 13.1 | 78500) VON 250 12828.) 16a 1194) este
fe, | 4 AA ANG 2a 2h AINA asi eons |i nero? ale OR es
Series I
Ca,c,d 105) 2455) 2249) 14205) 43565) 447822200 921s b LONG
b, e MESOMN 21281) Sieve Moesnl 4 GeOnl ee 9eeale22e2mle como meal ees
Series I
1D) By Gaal (De CCeel Whee | APA || akon tk Wl GyASSh | ky Ot it, 0) 9.5
ec 1.089] 24.2 | 24.6 | 14.0 |} 41.0} 44.0 | 20.0 | 21.3 9.5
OF870)2056" | 2005=)" V3k3") 28828 | 788.0 She s2 ea LOO
it 1.220) 26.7 | 26.0 | 15.0 = 47 .0 = 22.6 =
Series I
E b, c, d 0.867) 19.9 | 20.3 | 13.0 | 38.4 | 37.6 | 19.8 | 78.7 | 10.1
g, h 1222529) | 2o-ON 14534) 45290 eso | 2324 oie oe ORS
e, f 1.179) 24.2 | 25.3 VARA A522) 46RO Ne 22e2ulecomom melee

GROWTH OF THE CEREBRAL CORTEX 203

TABLE 8—Continued

SAGITTAL SECTION FRONTAL SECTION
AVER- Area of cortex Total area Area of cortex
SERIES, LITTER AND AGE |_ Ramrekt es
GROUP BRAIN
WEIGHT Area Area
Cor- | Stand- Cor- | Stand-| Cor- | Stand-
rected | ard | yigx-| rected | ard | rected) ard | pick.
ness ness
grams mm.2 mm.2 mm. mm.2 mm.2 mm.2 mm.* mm.
Series IT
F a, b OF832) 2078 19E4 |) 32") 38-0) |) Sb25) 186) | 729 9.9
c-l 1.204) 26.0 | 25.9 | 14.4 | 47.3 | 46.7 | 23.4 | 22.3 | 10.9
Series IIT
G a-g OFS44) 20S S9SS 30) 3815 (S6E9 192) San OrZ
h-j 15425 Gale Zon vero 46).2 le4onoe | e22n9) ees ml Ong,
Average } (ks ID) Oe ast SG || aA) || WO BPA eyAa Tl | Ale ees|) a6 9.7
(Sere l=] ERD) | WOT 24s an 246 MAT 45 10) | 4252 2256" 20 on LOR,
Average | (C. I) 0.700| 15.7 | 16.5 | 12.3 | 31.9 | 32.7 | 15.2'| 15.2 | 986
(Ser. I) J (Cy 1) 12226826215 (E261 eld. ON) 45.08 4722 | 2220N eo nce mise

higher on the average by 3 per cent (1 to 4 per cent in individual
cases) than the standard or controls. These results fit with the
observation that in the underfed the cortical thickness in the
frontal section is 8.7 per cent greater than for the standard
(chapter 7).

9. COMPUTED VOLUME OF THE CORTEX

In a former paper (Sugita, ’18 b), it was assumed that, as the
form of the cerebrum of the albino rat is relatively simple and
nearly constant, the relative volumes occupied by the cortical
cells could be computed, and compared among themselves, by
reducing the data obtained by measurement to a simple geo-
metrical form, since the cortical areas in the sagittal and frontal
sections stand in fixed relations to the respective diameters
L.F and W.D and to the cortical thickness of the sections from
the same brain. These relations have been expressed as follows
(Sugita, 718 b):

204 NAOKI SUGITA

Cortical area (mm.’) in sagittal section
Cortical thickness (mm.) in the same
Cortical area (mm.”) in frontal section
Cortical thickness (mm.) in the same

And the computed volume of the cortex should be obtained
simply by the following formula:

L.F x W.D X T (all in millimeters), (3)
where T gives the general average thickness of the cerebral cortex
of the same brain.

As shown in table 9, which has been condensed from table 9 a
(unpublished) for each individual, the constant ratios obtained
by the above formulas (1) and (2) fall between 1.10 and 1.29 for
the sagittal sections and between 0.80 and 0.95 for the frontal
sections, throughout both the underfed and the control groups.
The averages of the ratios for the sagittal and frontal sections of
the underfed are, respectively, 1.18 and 0.88, and those of the
controls are, respectively, 1.20 and 0.88. I have previously
given the figures 1.22 and 0.91, respectively, as these ratios of the
standard albino rat brains weighing more than 0.5 gram. So
it may be assumed that the ratios are nearly the same in both the
underfed and the controls; slight differences in the underfed
from the standard may be regarded as due to the facts that the
cerebrum of the underfed is sightly more elongated and the cor-
tical thickness is somewhat greater than in the standard. As
the product of the coefficients in the underfed (1.18 x 0.88) falls
somewhat lower than that in the standard (1.22 x 0.91), the
results of L.F x W.D x T should be about 5 per cent higher in
the underfed than in the standard.

The relative volumes of the cortex, obtained by the formula (3),
are computed and given in table 11 (without any special cor-
rection), compared with the corresponding standard values for
brains of the same age, instead of for brains of the same weight.
The relative volume of the cortex in the underfed brains, which
are considerably retarded in total weight development, is greater
than for the standard brains of the same weight, which are neces-
sarily younger and less developed as regards the cortical elements
than the underfed brains of like weight.

+ L.F (mm.) = constant (1)

+W.D(mm.) =constant (2)

GROWTH OF THE CEREBRAL CORTEX 205

Since in the underfed the average cortical thickness in the
sagittal and frontal sections was used in place of the standard 7’,
based on the thickness of the sagittal, frontal and horizontal
sections (compare Sugita, 717 a), therefore corresponding values
of T have been used in calculating the standard values for the
present comparison.

For this comparison, the test animals may be considered in two
groups, T.Il and T. II. In T. I groups, in which all test rats have
a brain weight less than 1.0 gram, the average computed volume
of the cortex is less than the standard by 16 per cent, while in
T. II groups, which contain the test rats with brains weighing
above 1.0 gram, it is more than the standard on the averagé by 1
per cent. On the other hand, the cortical volume in C, I groups,
which embraces the controls having brain weights less than 1.0
gram, is on the average 2.4 per cent less, and in C. II groups, the
controls with brain weights above 1.0 gram, it is on the average
7.5 per cent more than the standard for the same age (table 11,
last lines). As these comparisons are based on the numbers
obtained by calculation and not on the direct measurement, slight
discrepancies cannot be regarded as significant, and, as already
noted, the results in the underfed are open to special correction of
a few per cent for an accurate comparison.

The underfed brains are much retarded in the weight develop-
ment and the brains weighing up to 1.0 gram include those of
ages up to sixteen days, at which age the normal rats have a brain
weight 10 per cent heavier than the test rats (chapter V). We
conclude, therefore, that, calculated by the formula L.F x W.D
x T, the relative volumes of the cortex in the underfed are
nearly the same as in the standard in the brains weighing more
than 1.0 gram (T. II groups), while, on the contrary, they are
considerably smaller than the standard in the case of the brains
weighing under 1.0 gram or under the age of sixteen days, if the
age be taken as the standard of comparison.

It appears, therefore, that in rats underfed severely the cortical
volume is considerably retarded in growth during the early period
of development, but this is probably fairly compensated later
when the brain attains a weight of more than 1.0 gram or an age

206

NAOKI SUGITA

TABLE 9

Giving for each litter group in this study the average brain weight, the measurements
L.F and W.D, the quotient of the cortical area divided by the cortical thickness
(given also in table 8), and the ratio of the latter to the measurement L.F or W.D,

for the sagittal and frontal sections.
by (W.D X 100)/L.F is also given.
published table 9a for each individual.

are given at the foot of the table.

The width-length index which is obtained
This table was condensed from an un-
The averages for the test and control groups

The ratios given in this table 9 are based on the
average of the individual ratios and not on those obtained directly from the average
L.F or W.D and the average quotients

{<2} cORT. CORT &
g : AREA AREA 2
Be fowsr| 23 ANE CORT CORT a
pea way ta AND aoe E eae (GsTe THICKN RATIO| W. D| pHickn. | RATIO 7 f
@ |WEHIGHT UX IN Ha
. 2} SAGITTAL FRONTAL azd
B SECTION SECTION S
days grams mm, mm. mm. mm. hew
Series I
Ae ar idee T. I | 7—| 0.584) 9.28) 11.4 1.23) 9.88 8.9 0.89) 106
h 'T. I0}15 1.024)11.85). 13.5 14200 leat 0.93} 101
b, g C. I | 8—| 0.688) 9.90) 12.6 .27/10.60} 10.1 0.95} 107
1 Oh YT 27812295) bed 1.20)12.85|) 10.9 0.84) 99
Series I
Brac sent T. I | 9—| 0.644! 9.70) 12.5 1.29)10.46 9.6 0.92) 108
1 4h WOH) 1.052/12.10} 14.0 1.16)12.45) 10.9 0.88) 103
b, d Ca sit6 0.543] 8.78), 11.0 1.24) 9.85 8.6 0.88} 112
fag Mos C. IT/18—| 1.144)12.28} 14.1 1.16/12.40; 10.8 0.87} 101
Series I
Ca,e,d Av. UO LE LOS 27321 1450: 1. 14)12.17) 10.6 .| 0:87) 99
b, e C. II}22—] 1.307|13.30} 15.8 1.19)12.98) 11.3 0.87) 98
Series I
D¥aruced T. I |12—| 0.778/10.90} 12.6 UES OSH 9.5 0.88} 99
e AU, ENC 1.089)12.25}) 14.0 1.14/11.85 9.5 0.80} 97
b Casing 0.870)10.95| 13.3 1.21/11.45) 10.0 0.82} 104
f ; @. 1122 S220 12-40)" 1520 1.21/12.80 — — | 1038
Series I ; f
12), Joy, 1, Gl Ihe Ue 0.867|10.65) 13.0 22130 eek O eel 0.90) 106
g, bh E20 1.122)12.10) 14.3 1.19)12.35) 10.9 0.88} 102
e, f C. IL}17—| 1.179]/12.23) 14.4 1.18)/12.48) 11.4 0.92) 102

GROWTH OF THE CEREBRAL CORTEX 207

TABLE 9—Continued

a cORT. CORT. z
cS AREA | AREA eo
eo) ager (OR eae eg CORT CORT A
Berg ee ANP | con-| & | prain| 2: F | varcxn. | RATI0|W.D| varckn. |RATIO| 7
TROL | = |wrIGHT EN LN Ba
3 SAGITTAL FRONTAL Ee,
7 SECTION SECTION S y
oJ
daus grams mm, mm. mm. mm.
Series II
F a, b T. I |138—| 0.832)11.18) 13.2 1.19)11.23 9.9 0.88} 101
c-l T. [1/25+] 1.204)12.66) 14.4 1.14)/12.30) 10.9 0.88) 97
Series III
B a-g T. I |11+] 0.844)10.99; 13.0 L TSiiie22\ Oe? 0.90) 102
h-] T. I1j22—| 1.154)12.58) 14.3 L. T41027-20) 10 N4 0.87| 97
Average T. I |11—| 0.758/10.45| 12.6 1.21)10.81 9.7 0.90) 104
(Ser. I-III) T. IT/20—| 1.107|12.27| 14.1 PHILO ORG 0.87) 99
Average } C. I | 8—|.0.700) 9.88} 12.3 1.24/10.63 9.6 0.88) 108
(Ser. I) C. I)19+] 1.226)12.63} 15.0 LSLO 270 eile 0.88) 101

of more than sixteen days, so that after this period there is no
longer any significant difference in the cortical volumes between
the test and the standard animals.

10. NUMBER OF NERVE CELLS IN THE CEREBRAL CORTEX

The actual number of nerve cells in the frontal cortex in a
unit volume of 0.001 mm.’, or 0.1 mm.? in area on the slide by
10 micra in thickness, was counted in the lamina pyramidalis and
in the lamina ganglionaris at locality VII, the middle part of the
cortical band of the frontal section. The procedure for counting
the cell number, adopted by me for the standard values and
described in my previous paper (Sugita, ’18 b), has been strictly
followed here also. The number of cells in the lamina pyramidalis
and the lamina ganglionaris and the number of the ganglion cells
in a unit volume have been recorded and then converted into the
number of cells in the same unit volume in the fresh condition
of the brain by the use of the correction-coefficients based on
observations. All the data have been tabulated in table 10a
(unpublished) and condensed in table 10 for each group. The

208

NAOKI SUGITA

TABLE 10

Giving for each litter group in this study the average age, brain weight, correction-
coefficient, and the corrected number of nerve cells in a unit volume (0.001 mm.*)
in the lamina pyramidalis and the lamina ganglionaris and the corrected number
of ganglion cells only in the same volume, measured at locality VIT.
was condensed from a detailed table, table 10a (wnpublished), which gives the same

data for the individual cases.

given at the foot of the table.

This table

The averages for the test and gontrol groups are

NUMBER OF CELLS IN 0.001 mm.?

SERIES, LITTER AND TEST AVERAGE! | eRoGE Om |
GROUP CONTROL AGE EARNS) COEFFI- Lamina Lamina | Ganglion
WARNE CIENT pyrami- | ganglio- cells in
dalis naris jlam.gangl.
days grams
Series I :
Mexacdet tial Te | 0:58 eis 271 167 47
h WW. Jil 15 1.024 1.28 120 86 DAl
bine: Cal 8— 0.688 1.14 224 131 40
i Cm 17, L278 ale 26 107 75 20
Series I
Ba, ¢, e, f feel |e ee 644 | 1.17 232 132 39
i IU, MU 19 1.052 I B¥/ Lily 77 19
b, d Cai 6 0.5438 1.09 268 177 58
g, h, i Calls RS ele 440 ee st 109 76 21
Series I
Ca,ec,d Dead ||) 326 1.105 | 1.25 109 73 20
b, e CMs 222 | eso met 109 79 26
Series
Da,e,d Ae een | L735 le2A 152 90 21
e 405 Ul 18 1.089 1.28 118 81 18
b Oe IE 9 .870 122 152 93 PH
f Cau 22 1.220 1.14 111 5 22,
Series I ‘
IBLE, oy 5 Cl 4u, Il 12— 835 2 144 101 25
g,h ar, JUL 20 eal22 1.26 116 79 Alt
e, f Ce 17— 1.179 Al 116 79 23
Series II
Fa, b Arayl 13— .832 IPA 162 98 29
c-l is 10 25+ 1.204 1.32 105 74 19

GROWTH OF THE CEREBRAL CORTEX 209

TABLE 10—Continued

Connie. ||| NUMBEE OF CELLS IN 0.001 mm.#
SERIES, LITTER AND TEST AVERAGE serra TION
GROUP CONTROL AGE far coBFFiI- | Lamina | Lamina | Ganglion
VsGRRRCEE Mt CIENT pyrami- | ganglio- cells in
dalis naris jlam.gangl
days grams
Series [II
G a-g [eAuT, 11+ 0.844 1.24 149 94 24
h-j 40S ML 22— 1.154 1.26 108 80 20
Average APs 11— 0.753 1.21 185 |, 114 3
(Ser. I-III) AP, JO 20— 1.107 1.29 113 79 20
Average C.I 8— ORL00R | tots 215 134 42
(Ser. I) Coit 19+ 1.226 1.24 110 77 22

sum of the cell numbers in the lamina pyramidalis and the lamina
ganglionaris, which may be regarded as representing the average
cell density in the cerebral cortex, are also given in table 11, as
N, and compared with the corresponding standard values for the
brains of the same age, taken from a former paper (Sugita, 18 b).

When compared in this way, it is seen that the observed cell
number in a unit volume is generally higher than the standard in
brains which weigh less than 1.0 gram (T. I groups). The excess
in cell number in underfed brains weighing less than 1.0 gram
(T. I groups) is on the average 17 per cent, and that of the con-
trol brains weighing less than 1.0 gram (C. I groups) is on the
average about 7 per cent. On the other hand, the average cell
number of the underfed brains weighing more than 1.0 gram
(T. II groups) is almost equal to, while that of the control brains
weighing more than 1.0 gram (C. II groups) is less by 4 per cent
than, the standard for the same age. The underfed brains are
underdeveloped in weight and the brains weighing less than 1.0
gram (T. I groups) contain those of ages up to sixteen days.
These relations lead me to conclude that, in the underfed brains
weighing less than 1.0 gram or under sixteen days in age, the cell
density denoted by N (the average cell number in two unit
volumes) is distinctly high, when compared with the normal
brains of the same age, probably because the brain size or weight

THE JOURNAL OF COMPARATIVE NEUROLOGY, VOL. 29, NO. 3

210 NAOKI SUGITA

or the cortical volume is relatively undeveloped in comparison
with the cell number (see above). In older brains weighing more
than 1.0 gram or of ages above sixteen days, these discrepancies
have been somewhat balanced, but, when compared with the
controls, the underfed brains remain generally slightly higher in
the cell density even in rats of sixteen days or older.

Considered in relation to the facts presented in the previous
chapter showing that the computed volume of the cortex is
below the standard in the underfed brains weighing less than 1.0
gram, it may inferred that the underfed brains, underdeveloped
in weight and size, have a relatively higher cell density, because
the normal number of cells is crowded into a cortex of smaller
total volume.

11. RELATIVE VALUE OF THE COMPUTED NUMBER OF CELLS IN
THE ENTIRE CORTEX ‘

As previously shown (Sugita, 718 b), the computed number of
nerve cells in the entire cortex may be obtained and the values
compared among themselves by the use of the following formula:

N XL XWDXT (LF) WD and 1, in ‘millimeters

where N means the relative cell density represented by the sum
of the cell numbers in the unit volume in the lamina pyramidalis
and in the lamina ganglionaris (that is,-the number in two unit
volumes), given in table 11, based on table 9, and L.F x W.D xT
is the computed volume of the cortex, as already given in the
foregoing chapter.

In table 11, these relative values for the volume of the cortex
and for the cell number in the cortex in the underfed Albinos
are given for each group, each paired with the corresponding
standard values for brains of the same age, all condensed from
table 11 a (unpublished), which gives the corresponding data for
each individual. Every standard value was taken from my
previous presentation (Sugita, 718 b). Throughout the underfed .
and the controls, these pairs of figures seem to be nearly in
accord, showing on the average only 1.7 per cent excess in the
underfed and 3.4 per cent excess in the control brains (average

GROWTH OF THE CEREBRAL CORTEX Dat.

of all groups), as compared with the standards. As already
noted in chapter 9, the results obtained by the use of formulas
are open to some error, and in addition the results in the underfed
are subject to special correction of a few per cent for a fair com-
parison, so that the differences recorded may be regarded as
probably insignificant and the computed cell number in the entire
cortex of the underfed may presumably be considered as equal
to the standard number for brains of the sameage. If this is so,
the process of the cell division in the cerebrum during early life
must have been going on undisturbed even by the severe un-
derfeeding, though both the size and the weight of the brain
have been arrested in development by this, in some cases very
considerably.

12. SIZE OF NERVE CELLS

The standard size of the pyramids (in the lamina pyramidalis)
and the ganglion cells (in the lamina ganglionaris) in the cerebral
cortex of the albino rats at different ages was presented in my
sixth paper (Sugita, 718 ¢). In the present study on the influence
of the severe underfeeding upon the growth of the cerebral cortex,
the size of the nerve cells in the cortex was also determined by
the measurement of the transverse and longitudinal diameters
of the cell body and the nucleus in the pyramids (in the lamina
pyramidalis) and in the ganglion cells (in the lamina ganglionaris)
at locality VII in the frontal section, in the same manner as for
the standard determinations (Sugita, ’18c¢). The results have
been tabulated in table 12a (unpublished) and condensed in
table 12 for each group. The average diameters of the cell body
and of the nucleus are obtained by extracting the square roots
of the respective products of the transverse by the longitudinal
diameters, and these have been corrected, by applying the cor-
rection-coefficient, to the fresh condition of the brain. The
corrected average diameters have been tabulated in table 13 a
(unpublished), compared respectively with the corresponding
standard values for the brains of the same age, and condensed
in table 13. The correction-coefficients which were used are
given in table 12.

212

NAOKI SUGITA

TABLE 11

Giving for each litter group in this study the average brain weight, the age, the com-
puted cortical volume, the cell density and the computed number of cells in the entire
cortex, as based on the observed measurements presented in this paper, each com-

pared with the corresponding standard values for the same age.
were taken from my previous presentation (Sugita, ’18b).

Standard values
This table was con-

densed from an original full table 11a (unpublished), which gives the data for each

individual.

given.

CORTICAL VOL-

CELL DENSITY:

At the end of the table the averages for the test and control groups are

CELL NUMBER:

UME: NXLFX
ewe TE OWED XE WED x<er:
SERIES, LITTER AND TEST | AVER-| ,gE |——————
GROUP es pee BRAIN Stand- Stand- Stand-
- WEIGHT/Starved| ard (|Starved| ard |Starved| ard
and |forthe} and |forthe| and _ | for the
controls} same |controls| same |controls} same
age age age
days grams | mm. | mm.
Series I
Ac,a,d,f T.1| 7— | 0.584] 134.4] 157.8] 437 | 375 | 482.9] 450.8
h 4hs 100) 155 1.024] 263.1) 265.0) 206 202 | 542.0) 535.0
b, g Ct 8— | 0.688} 159.9} 165.0) 355 854 | 452.4) 467.6
1 (Ge U0) al 1.278] 314.5} 275.0} 182 198 | 572.4| 545.0
Series I
Ba,c,e,f T.I| 9— | 0.644] 151.6] 187.0] 364] 298 | 489.1) 479.2
1 AU, Uh) ake) 1.052) 287.7} 285.0} 194 191 | 558.1) 544.0
b, d Cal 6 0.543) 112.4] 126.5) 445 888 | 457.8) 443.6
g, h, j C. Il] 18— | 1.144] 285.5] 278.3] 184| 195 | 526.2) 543.3
Series I
Clan c, a at, JU) 29 1.105] 287.3] 284.7) 182 191 | 521.6) 542.0
b,e C. II} 22— | 1.307} 320.9) 289.5) 188 188 | 603.4) 540.6
Series I
Dia, c,d T. LI | 12— | 0.778) 201.1) 238.3) 242 213 | 486.4| 505.3
e 405 JUN aks 1.089) 278.7} 280.0} 199 195 | 554.6) 546.0
b (Ge 1 9 0.870) 214.4) 207.0} 245 230 | 525.3] 476.0
Series I
Eb; c¢;, d Ate 12 0.867} 210.3) 249.3) 238 207 | 497.1] 516.7
g, h Te 20 1.122) 295.9} 290.0} 194 188 | 574.0) 545.0
ual Co 7 ae 79) 278-0 27225) 195 197 | 535.9) 535.0

GROWTH OF THE CEREBRAL CORTEX 213

TABLE 11—Continued

connie VOLS Were DENSITY: Se tae
jee L.FXW.DX T WAD SST:
SERIES, LITTER AND aon: ea AGE Aiea rae Bare
r t, loa - -
etoee wore Nee cant Starved ad Starved Fe | Starved ard
and |forthe} and | forthe} and _ | for the
controls} same |controls| same |controls} same
age age age
days | grams | mm. | mm.3
Series II
F a, b sb 13— | 0.832) 218.7) 252.5) 260 206 | 550.4) 520.0
e-l T. II} 25+ | 1.204) 307.9) 303.4) 178 180 | 548.7| 545.7
Series III
G a-g T. [| 11+ | 0.844) 213.2) 229.1) 248 225 | 520.4] 604.1
h-j T. IT] 22— | 1.154) 302.2) 294.7) 189 186 | 570.3) 546.7
Average Ay 11— | 0.758) 188.2} 218.0) 298 254 | 504.4) 496.0
(Ser. I-III) T. II} 20— | 1.107) 289.0) 286.1; 192 190 | 552.8) 543.6
Average (Ceol 8— | 0.700} 162.2) 166.2) 348 324 | 478.5) 462.3
(Ser. I) C. II} 19— | 1.227) 299.7) 278.8] 187 195 | 559.5) 641.0

By comparing the corrected values in the underfed with the
standard values, the average diameters of the cell body and of
the nucleus in the underfed brains are found to be generally
smaller, on the average, by 9.8 per cent (cell body by 8.6 per cent
and nucleus by 11.0 per cent) than the standard value. At the
end of the following table 13 appears a summary of the compari-
sons, arranged as in the earlier tables in this study.

As seen in this summary, both the pyramids and the ganglion
cells are much retarded in development in size of the cell body in
the underfed brains weighing less than 1.0 gram or of ages
under sixteen days, the average diameters of the cell body being
11.5 per cent (in the pyramids 11.2 per cent and in the ganglion
cells 11.8 per cent) smaller than the standard for the same age.
But in the underfed brains weighing more than 1.0 gram, this
arrest in size-development of nerve cells is no longer so notable,
the average diameters of the cell body being smaller than the
standard by only 5.7 per cent (in the pyramids by 8.3 per cent
and in the ganglion cells by 3.1 per cent). The size of the

214 NAOKI SUGITA

TABLE 12

Giving for each litter group in this study the average brain weight, the correction-
coefficient, and the observed (not corrected) diameters (transverse and longitudinal)
of the cell body and the nucleus of the pyramids (in the lamina pyramidalis) and of
the ganglion cells (in the lamina ganglionaris), measured at locality VII in the
frontal section. This table was condensed from table 12a (unpublished) for indi-
vidual cases. The averages for the test and control groups are given at the foot
of the table

g f LAMINA PYRAMIDALIS LAMINA GANGLIONARIS
ial a
g Cell body Nucleus Cell body Nucleus
SERIES, LITTER AND g z diameters diameters diameters diameters
GROUP 2 oe °
SURO Ca ee eee bee petals iee tere I<
go [ie ee |e ee Se | See
a “ g eae las =I 4 = 4 = S
grams B M M mn mm HM Me m
Series I
Ac, a, d, f ee OF5841 1 18) oie 2) LORS 2) 14 S122 24 Se OlaloaG
h Te MO24 1 28) 1422/1950 1383) toe) LORS 29.2 7 eZee
’ b, g © 0268Si el 14 4s YO FOO Aes IS 2 Zone lel Gellmnsee
i OE D0 2) AG Gs 2270) 4 Soe olecOetiesOLS el SseOlm20et
Series I
B a, ¢, e, f T. I \0.644) 1.17) 13.3) 18.8) 12:0) 18.5) 17.2) 25.3) 16 1S
i TS THT F052) WS Tie4 0 20K M8r4 oat) 19S 2873) elie
b, d C. I |0.543) 1.09) 13.9) 18.0) 12.4) 138.6) 18.6] 24.1] 15.6] 17.0
g, h, j Cont 44a 3) 4a 20e8) 144) be 4 19) 9 S0ks Ses elORG
Series I
Cra. cd Ree 105) U25) 1456) 23s) 13).9)) 1423) 1858) 2959 ees
b,e C. II/1.307| 1.16) 16.0) 21.1) 14.4) 15.3) 19.9) 30.4) 17.8) 19.6
Series I |
Dra- cs. a IR IE Os 77s PHN) TEE Sy 1) aN PL IBA SH MeO) a/c 0) Ts) il 5 2
e T. I1/1.089] 1.28) 14.0} 20.0) 12.2) 14.0)-18.3) 28.8} 16.2) 19.4
b Cel OLS 70) 1a Gt) iO sS) 4s 5 SS ees 72 eel See
li C. I1/1.220) 1.14) 14.9} 21.5) 14.2; 14.8) 19.2) 28.6) 17.2) 18.0
Series I
1B; 2h lon @5 G! T. I 10.835) 1-23) 13.5) 19.8! 12.8) 14.3) 17.9) 28.3) 16.0) 18
g,h Te e122) 1. 26) 1420120) 7) 1225 142 OR 7 S07 el Grams
ect G@, WDA 179) £20) P51) Qe 13.9) 15.4! 19/2) S0L6/aleG 192

GROWTH OF THE CEREBRAL CORTEX 25

TABLE 12—Continued

é m LAMINA PYRAMIDALIS LAMINA GANGLIONARIS
&
& a
PS Cellbody | Nucleus | Cell body | Nucleus
SERIES, LITTER AND io z diameters diameters diameters diameters
GROUP a me £
Erin SVEN eee by Bees IN ued | Boy’) Geshu MAISON SEA gst
= < is) ical 4 ical 4] Sal 4 HB 4
grams Be Me B A B B Me Me
Series IT
Fa, b Te OKSSZ ileal ISSO Te USGA MOL Sle 2esOlleolmloes
c-l ee M204 Pes? | ASO SZ Ol els7ip 1428) 1920 F300 73! 19a
Series III
G a-g T. I |0.844| 1.24) 14.0) 19.8] 13.1] 14.3] 17.9] 28.4) 16.8) 18.4
h-j TUT 54126) s13s9) 19e8iF 1226) 1329) 18.3) 28) 7 1622) Tse
Average \ Ab. IO. 74s} 1.21) 13.6 OR e265) Ss eOleliiao|e2Oes|ellomsl mele
(Ser. I-IIT) if T. IL}1.107|) 1.29) 14.2) 20.4) 13.1) 14.6} 19.1] 29.4) 16.9] 19.1
Average i C. I 10.700) 1.15) 14.7] 18.9) 13.3) 14.6) 19.3) 25.7) 16.6) 18.3
(Ser. I) \ Cem 226 |e 22| Sb 2 O44 2 53 19e Al oOeh lites oes

nucleus is much more affected by the underfeeding than that of
the cell body. In the underfed brains of T. I groups the average
diameter of the nucleus is smaller by 13.9 per cent (in the pyra-
mids by 15.8 per cent and in the ganglion cells by 12.5 per cent)
and in those of T. II groups it is smaller by 8.0 per cent (in the
pyramids by 11.0 per cent and in the ganglion cells by 5.1 per
cent) than the standard for the same age. The deficiency in the
average diameter of the cell body by 6 to 12 per cent and that
of the nucleus by 8 to 14 per cent correspond to the inferior-
ity in volume of about 20 to 45 per cent and 25 to 50 per cent,
respectively.

On the other hand, in the control brains of all weights, the size
of the cell body and of the nucleus have proved to be also some-
what smaller than the standards, but the deviations are not so
much in comparison with the underfed, the deficiency in the
average diameters of the cell body and the nucleus being on the
average 5.3 per cent (table 13).

216

from table 18a (unpublished) for individual cases.
trol groups and their percentage relations are given at the end of the table.

= percentage difference

NAOKI SUGITA

TABLE 13
Giving for each litter group in this study the average age, brain weight, the corrected aver-
age diameters of the cell body and the nucleus of the pyramids (in the lamina pyrami-
dalis) and the ganglion cells (in the lamina ganglionaris), based on the condensed
data in table 12, each compared with the corresponding standard values for the same
age, taken from my former presentation (Sugita, ’18c.)

This table was condensed

The averages for the test and con-

(per. diff.)

5 LAMINA Rae LAMINA*GANGLIONARIS
i=]
. Cell body Nucleus Cell body Nucleus
PIs el ae oT a = | Aver. diameter | Aver. diameter | Aver. diameter | Aver. diameter
GROUP Coen 2 a 7
S| a | 2 e 3 z E a 3 z
< < 3) S 3) 3 > 8 5 3
pe x © cs} ry) as} rs) as} ® ns}
g ] bs 2 a iS ba S Sy iB
> > ° ~ ° po) 9° Pe) 9 ~
< a (S) mM ie) NM 6) mM eo) nM
days | grams) Me Me be Me Be Ke Me
Series I
Ac, a, d,f | T. 1 | 7—|0.584/16.6] 19.4 |18.3) 16.6 |21.6) 25.9 [16.8] 20.7
h LES ME OZA2T H 2857e ISE WOES |S086|" Wiles) WasKG 24.4
b, g C. I | 8—|0.688118.7) 19.6 |15.4| 16.9 |24.7| 96.7 |19.5} 91.2
i CHIME WE2 A235 1 22358 Sele 2O20) S12 S132) ara 24.4
Series I
Ba,c,e,f | T. I | 9—|0.644/18.4| 20.7 114.8) 17.8 [24.3] 27.9 |19.4| 22.1
i T. THIS >113052/23. 2 22 70" 1978) 20r0" 132 al S1ee 258 Qh 6
bind C. £16 \0.543)7-4) -18.6 \14.3) 216.8) |23)3|| 9429. iL7e8!) 1988
oauhey CC, W180. 144123. 1) 93.9 \19.7| 2010 \32-4) 31.3) 2510) o7ey
Series I
Ca,c,d AR. JUUPAOY (MSs OF) en = 2s oy ely ZOKO | 29a) OL 48/229] ae
b, e C. 10/22—/1.307/21.4, 94.0 |17.4| 20.0 |29.1) 31.5 (|21.8 24.5
Series I
Dracd TL 12—)0.778|20.6|) 22.9 \16.6) 19.6 \27-4) BO 2082) 9328
e DTS) NV EOS9i21. 4) 23.9 16.8) 2050 |29r5|) B43) 22 28i eee:
b C. 1] 9 |0.870)21.8) 22.1 |18.4) 18.8 |29.3) 28.4 |23.2) 28:0
f CRON BONN) DUAN Te AMES PROG VAL Bul OB 24.6
Series I
By 2), sbync; T. I |12—|0.835)19.8) 23.0 |16.4) 19.8 |27.1) 30.9 |20.7| 24.2
g,h PAT 20) | 222125) VEO SGESi= 2OLOR | SIO: a ml ergo ano
e, f C. TTj17=|1.179,22.0| 23.7 |17.7/ 19.9 |29.5| 87.8 |22.4| 22.5

GROWTH OF THE CEREBRAL CORTEX A

TABLE 13—Continued

5 LAMINA PYRAMIDALIS ie LAMINA GANGLIONARIS
a Cell body Nucleus Cell body { Nucleus
Eaten Sees TEST 8 ms Aver. diameter | Aver. diameter | Aver. diameter | Aver. diameter
AND GROUP oe = 3 ;
c Q se} as} z 3 z as} z og
y g 2 Es £ & oe q 2 z
Bee | eel og, | et | MECN dares ee Leni ig
< = 1S) MD .S) 7) oO MQ 1@) oD)
daus|grams| uw a bu MU ia a u
Series IT
F a, b Ty. I 13 =)0..832/20.8), 238.2 07.1) 19.8 128.5) 87.7" |22.3) 2404
* cl T. [0)25+)1.204)22.9) 23.9 |18.6) 20.0 |31.0) 37.5 |23.6) 24.4
Series III
F a-g T. I /11+)0.844/20.6| 22.5 |17.0) 19.2 |27.9| 29.9 |21.9) 23.5
h-j TW. U22—)1 154/21 0) 24.2 \16:7) 20.1 |29:0) 3i.6 121.7) 24.5
Average
(Ser. I-III) Te MT =|\0.7538\19 25) 12220) 15.9) 18.8 126.1) 9928. |20 2923.7
(per. diff.) |. (—11.2) (—15.3) (—11.8) (—12.5)
Average
(Ser. I-IIT) T. I1/20—|1.107/21.9| 23.9 |17.8} 20.0 |30.4) 31.4 |23.1) 24.4
(per. diff.) - (= 8.3) (—11.0) (— 3.1) (— 5.1)
Average
- (Ser. I) C. I | 8—|0.700}19.3) 20.1 16.0) 17.2 |25.8) 26.7 |20.2) 21.38
(per. diff.) (29378) (37) | en coe) CAB)
Average)
(Ser. I) CMOS 2262204) 289 ASS 20.0! \20c8|) Sips N23cAs 8oe
(per. diff.) (— 6.2) (— 8.5)! (— 3.3) (— 5.5)

It is also seen that by underfeeding the nucleus is more affected
than the entire cell body both in the pyramids (deficiency in
diameters; T. I groups: cell body 11.2 per cent and nucleus 15.3
per cent, T. II groups: cell body 8.3 per cent and nucleus 11.0
per cent) and in the ganglion cells (deficiency in diameters; T. I
groups: cell body 11.8 per cent and nucleus 12.5 per cent, T. II
groups: cell body 3.1 per cent and nucleus 5.1 per cent) of brains
of all weights, while the pyramids are more markedly affected
than the ganglion cells both in the cell body (deficiency in diam-
eters on the average of T. I and T. II groups: pyramids 9.8 per
cent and ganglion cells 7.5 per cent) and in the nucleus (deficiency

218 NAOKI SUGITA

in diameters on the average of T. I and T. II groups: pyramids
13.2 per cent and ganglion cells 8.8 per cent). In young brains
which weigh less than 1.0 gram, the influence of the underfeeding
is considerable, while in brains weighing more than 1.0 gram or of
ages more than sixteen days we can not detect any large arrest
in the size-development, especially of the ganglion cells (the sizes
of the cell body and the nucleus of the ganglion cells in the
T. II groups are quite equal to the corresponding sizes in C. II
groups) (tables 12 and 13). These observations are in agreement
with the conclusions reached by Morgulis (’11).

13. PERCENTAGE OF WATER IN BRAIN

As stated earlier (in chapter III), Litter H in Series II, in which
a young primipara mother was entrused with seventeen young in
order to produce a series of underfed young, was used partly
for the investigation of the percentage of water in the underfed
brain and partly for a histological study of myelination fae con-
sidered at this time).

In this Series II the development in brain weight is not so
greatly arrested, as compared with the arrest in body growth, as
in Series I. As already shown, in Litter F, which was treated in
a similar manner, the brain weight is on the average 9 per cent
low, but in this Litter H it has been possible to arrest the brain-
weight growth on the average by about 12 per cent, compared
with the standard of the same age (compare table 4).

Table 14 gives for each individual examined in this litter the
sex, the age, the brain weight, and percentage of water in the
brain, each accompanied by the standard percentage of water
contained in the brains of the same age and sex and also of the
same weight and sex. The differences are given in special
columns.

By obtaining averages, it is found that the underfed brain
contains slightly (0.48 per cent) more water, when compared
with the normal brain of the same age and somewhat (1.4 per
cent) less water, when compared with the normal brain of the
same weight. This means in terms of the percentage of water,

GROWTH OF THE CEREBRAL CORTEX 219

TABLE 14

Showing for each brain in litter H the sex, the age, the brain weight, and the percent-
age value of water in the brain, accompanied with the standard values of percentage
of water in brain for the same age and for the same brain weight. The differences
between the observed percentages and the corresponding standard values are given

in special columns, with their averages. °
| PERCENTAGE OF i PERCENTAGE OF
a hee _ WATER ____ WATER
a a oan Seer on WATER STANDARD FOR THE STANDARD FOR THE
gaap | saracane | eee [eo vars oo
grams
Ha f 13 0.880 86.39 | 85.40 +0.99 | 86.82 —0.43
b f 17 1.024 84.15 83.82 +0.33 | 85.08 —0.93
Cc f 23 1.135 2.00 81.93 +0.07 83.21 —— el
d f 28 1.166 80.83 80.74 +0.09 | 82.70 — 1°87
e m 32 1.215 80.31 80.04 +0227 81.70 —1.39
f ay ff Thal 80.12 79.55 +-Okot | 838.78 —3.66
g m 43 1.295 80.24 | 79.32 +0.92 80.56 =(0.32
AVeTage ls) 2) hn: +0.48 —1.40

that the underfed brain is slightly underdeveloped for its age,
but somewhat overdeveloped for its weight. Similar relations
have been revealed by the comparisons already made. Normally
about 0.5 per cent excess in percentage of water in the brain would
mean at the early ages approximately one or two days’ retarda-
tion in development (compare table 74 in ‘The Rat,’ Donaldson,
Zo)

From the same litter (Litter H) I took with each of the above
individuals a second rat for the study of the myelination, because
it is known that the percentage of water in the brain is correlated
with its myelination. The brains under seventeen days of. age
showed no fibers in the frontal sections, as stained with Pal-
Kultschitzky method. The twenty-eight-day brain showed
only a few faintly stained fibers in the cortex, the fibers in the
corona radiata (designated C. E. by Watson, ’03) being already
myelinated. Material above thirty-seven days was not exam-
ined. This passing examination of a small number of cases
roughly indicates, therefore, that the first appearance of myelina-

220 NAOKI SUGITA

tion in somewhat retarded, because, according to the investiga-
tion of Watson (’03), myelination in the corona radiata should
have begun at eleven days and radiations into the cortex should
have been recognized at twenty-four days. But a more detailed
test for this process is required before any special use can be
made of the results.

14. RELATIVE QUANTITIES OF THE ALCOHOL EXTRACTIVES

In my former paper (Sugita, ’17 a) a chart, based on the data
given in ‘The Rat’ (Donaldson, ’15), was presented to show the
absolute quantity of solids contained in the Albino brain accord-
ing to the brain weight. For comparison with this, I calculated
also the relative quantity of alcohol-extractive substances in the
Albino brains, as shown by comparing the initial weight of the
brain with its weight after extraction by 80 per cent alcohol
(for twenty-four hours) and 90 per cent alcohol (for twenty-four
hours) according to a uniform procedure. As the brains were
treated uniformly throughout the investigation, the results are
comparable among themselves.

The results from 120 normal albino rat brains, grouped in
twenty brain-weight groups (Groups I to XX), are given here in
table 15 and plotted also in chart 1, in which the smooth curve
(in a dotted line) represents the percentage weight of the ex-
tracted brain on the fresh brain weight. In chart 1, the graph
which presents the absolute amounts of solids (in grams) accord-
ing to the brain weight is also given in a solid line based on the
chart in my former paper (chart 12, Sugita, *17a). It was
remarked previously (Sugita, ’17 a) that in the Albino brains
weighing between 0.95 gram and 1.4 grams, that is, between ten
and thirty-five days of age, the rate of increase in solids is some-
what higher than in the periods before and after that phase,
and this fact was formerly interpreted as indicating that, during
this phase, the myelination in the brain had been proceeding
very actively. This interpretation is now supported by the
graph which gives the percentage weight of the brain. This
graph varies inversely to the amount of the alcohol-extractives

GROWTH OF THE CEREBRAL CORTEX 221 .

and, as it decreases relatively rapidly in the phase during which
the brain grows in weight from 0.9 gram to 1.35 grams, or in the
ages between nine and thirty-three days, it shows that during
that phase the alcohol-extractives increased.

The turning points in the both graphs marked with crosses
x and XxX) and asterisks (* and **), respectively, are in fair

% ff : mgms.

68 + 1 | a : ss aay ee =
| | | | | | =
66 4 - + | 4 + alba — ~_ les fe

Sy Tt
|

64|—_| 2) Bee ae ne ad ee —— 100

Sees te | 4 | :
60|_ i | | | | t

| Hes PRA Sele OD ih Leet
O20 03) 1047 (05) 06 FOr 0S 0910 Sse by LT AS oe gms

Chart 1 The dotted line shows the ratio between the initial brain weight and
the weight after its dehydration and extraction in 80 per cent alcohol (for twenty-
four hours) and 90 per cent alcohol (for twenty-four hours) according to a uniform
procedure, plotted on the brain weight. The data were taken from table 15.
The graph was drawn connecting the middle points of each pair of entries.
* and ** indicate the turning points in the graph.

The solid line shows the absolute weight of the solids in the brain according to
the brain weight. The data were taken from table 74 in ‘The Rat’ (Donaldson,
15) and calculated by me. * and ** indicate the turning points in the graph.

For the ratios of brain weight the scale is given on the left side of the chart and
for the absolute weight of the solids the scale is given on the right side.

coincidence, so that it may be concluded that the mass of the
aleohol-extractives would be in proportion to the grade of myeli-
nation in the brain, and by following the former the progress in
myelination could be estimated roughly.

It must be emphatically stated that my figures given in table
15 do not represent the total quantity of the alcohol-extractives,

Zee NAOKI SUGITA

TABLE 15

Giving for each brain-weight group of the normal albino rat the average initial
brain-weight in the fresh condition and the brain weight after dehydration and
extraction in 80 per cent alcohol (for twenty-four hours) and 90 per cent (for twenty-
four hours) by a uniform procedure. The ratio of the final brain weight to the
initial weight is given in the last column as a percentage value. Based on observa-
tions on 120 albino rats, sexes combined.

| BRAIN WEIGHT
pl a aaa | NUMBER OF CASES aspen a es DEHYDRATION IN ANIMAL
PER CENT ALCOHOL
grams grams per cent
II (birth) 6 0.271 0.213 78.6
Itt 8 0.343 0.267 77.8
IV 9) 0.428 0.332 77.5
V 14 0.543 0.416 76.7
VI 5 0.636 0.479 75.4
VII 4 0.755 0.571 75.7
VIII 10 0.844 0.630 74.7
IX (10 days) 5 0.954 - 0.714 74.8
x 6 1.047 0.757 72.3
XI (20 days) 5 pelo 0.820 70.6
XII 5 1.245 0.874 70.2
XIII 8 1.341 0.921 68.6
XIV 5 1.449 0.989 68.2
XV a 1.558 1.074 68.9
XVI 8 1.667 1.131 67.9
XVII 6 1.721 1.170 68.0
XVIII (90 days) 5 1.832 1.222 66.7
XIX 1 1.924 Leoili(eauy 68.4
XX 3 2.037 1.369 67.2

because the extraction was not complete. My figures are only
by-products in a study on histological technique, and to obtain
the total quantity of the extractives the brain must have stayed
much longer in alcohol of a higher concentration. My data
therefore give merely the relative values for the quantity of the
alcohol-extractives, but are comparable among themselves and
with the values from the underfed brains treated in the same
manner.

In giving the ratio of the brain weight after extraction in aleohol
(by this method) to its initial weight, no correction was made for
the weight of water replaced by alcohol, because my object was

GROWTH OF THE CEREBRAL CORTEX 223

only to compare the results among themselves and not to de-
termined the exact quantity of the extractive substances.

Table 16 gives for each group in this study the ratio of the
brain weight after dehydration in 80 per cent alcohol (for twenty-
four hours) and in 90 per cent alcohol (for twenty-four hours) to.
its initial weight in the fresh condition, calculated in the same
way as in table 15 and each paired with the standard ratio for
the same age, quoted from table 15. Thus compared, the under-
fed brains show in general a higher ratio, the difference amounts
to 1.0-4.3 per cent, on the average 1.9 per cent, while the differ-
ence in the control brains is generally low, on the average
+ 0.4 per cent.

This examination tells us roughly that in the underfed brains
the alcohol-extractives are somewhat less in quantity than in
‘the normal brain, if the age be taken as the standard of compari-
son, and, therefore, it may be concluded that they are somewhat
retarded in the formation of alcohol-extractive substances and
therefore in myelination. Reviewing tables 14 and 16 together,
we see that during underfeeding the myelination process or the
increase in the alcohol-extractives is retarded slightly, but is
going on, not greatly affected by the outside influence, regularly
according to its age. It is fair to say, however, that the differ-
ences thus determined by extraction are seemingly less than those
shown by the histological tests.

15. A DISCUSSION ON THE RELATION BETWEEN THE BODY
WEIGHT AND THE BRAIN WEIGHT IN THE UNDERFED
ALBINO RATS

By examining table 4 it will be readily seen that under severe
underfeeding at an early age, the increase in the body weight and
the brain weight, according to the age, is notably reduced, and, as
a consequence, the acutely underfed (Series I, chapter 5 and
table 1) have lost, in the course of first twenty days after birth
(during suckling period), about 29 per cent in body weight, but
only 8 per cent in brain weight, when compared with the corre-
sponding standard values for the same age. By chronic starva-
tion, during which the young (excessive in number) were left

224 NAOKI SUGITA

TABLE 16

Giving for each litter group in this study the average age, the initial brain weight in
the fresh condition and the brain weight after extraction in 80 per cent alcohol
(for twenty-four hours) and 90 per cent alcohol (for twenty-four hours) by a uniform
procedure, and the ratio of the latter to the initial weight. The corresponding
standard values for the same age were calculated on the basis of the data in table
15 and compared with each and the difference between them given as an average for
each group. This table was condensed from table 16a (unpublished) for individual
cases. The averages for the test andcontrol growps are given at the end of the table.

AFTER EXTRACTION
IN 80 PER CENT AND
90 PER CENT Standard See
SERIES, LITTER AND TEST AyeRaGn.| “VEEAGE steers fie fOr, ENCE
GROUP CONTROL AGE Hehe oan of hee FROM THE
mal Ratio to same age | STANDARD
arn the initial
weight | brain,
a days grams grams per cent per cent per cent
Series I :

Ac, a, d, f Ny JE T= 15025848) 40.4501 77: 25)| 757 epi

h 40S IU 15 1.024 0.779 76.0 72.8 +3.2

b, g rai 8— 0.688 0.517 Deo 75 4 +0.3

i (G5 JUL 17 1.278 0.928 (P00 72.3 +0.4
Series I

inate cena AR sclt 9— 0.644 0.488 dor 74.9 +1.2

i 405 IL 19 1.052 | 0.799 | 76.0 (fibatt +4.3

b, d Cali 6 0.548 0.414 76.4 UWGio Al +0.3

g, h, j (Ge JU 18— 1.144 0.826 (22 72.1 +0.1
Series I

Crane PTO 20 1.105 0.816 73.9 729 1.0

b, e Cyn 22— 130% 0.934 TANS 71.8 —0.3
Series I

D a,c, d 19 12=- || 0.778) (O2584 | (75.0) | 78-7 eee

e Ghee Ul 18 1.089 0.795 Jal) 72.0 +1.0

C. 1 9 0.870 0.656 75.4 74.6 +0.9

f Ch ul 22 1.220 0.863 70.8 LEO +0.2
Series I

Ea, b, c, d Tesal! 12— 0.835 0.626 75.0 UBall +1.3

e Go Ti 13 1.024 0.760 74.1 73.4 +0.7
Series II

F a, b altel: 13— 0.832 | 0.636) 76.7 73.4 +3.3

e-k IS IH 25-- 1.198 0.862 U8) 70.7 +1.6

GROWTH OF THE CEREBRAL CORTEX 225

TABLE 16—Contin wed

AFTER EXTRACTON
IN 80 PER CENT AND
90 PER CENT Standard DInT RS
SERIES, LITTER AND TEST ASV. ETRIAG TD) |e ALCOHOU ay ENCE
GROUP CONTROL AGE | eee a ; ofthe. FROM THE
| Final lt} ete? Je, same age SEAS UENO
Deane jue initial
weight brain
| oo weight
days grams grams per cent per cent per cent
Series III
G a-g aS: 11+ 0.844 0.641 76.0 UOae, aioe
h-j AUS JU 22— . 1.154 0.833 72.2 (2 1.0
Average | Tl i+ | 0.753 | O.571| 76.0 | 74.2 | +1.8
(Ser. I-III) f T. IT | 20+ ft OAS]. OLS814) |) "45298 |) S708 +2.0
Average Cr 8— 0.700 | 0.529 | 75.8 75.3 +0.5
(Ser. I) Cyr 18+ 1.195 0.862 (253 72.1 +0.2

continuously with the mothers (Series IJ and III, chapter 2 and
table 2), the loss in the brain weight is relatively less, in some
individual cases nothing, while the body weight suffers much
more, compared with the acutely underfed groups (Series I).
The observed body weight and the brain weight of each indi-
vidual in this study are plotted separately for each litter in chart
2, A to H, according to the advancing age. Comparing the set
of graphs both for the body weight and the brain weight within
every litter, it is clearly seen at a glance that the courses of the
graphs are similar, so that one, which advanced in age but has a
smaller body weight, has also a relatively smaller brain weight,
and vice versa. From this it is concluded that, though the
brain, with a strong impulse to grow, regularly increases in weight
with age and is only slightly affected by outside influence, yet
it is controlled somewhat by the growth in the entire body.
Thus, within certain limits, the brain weight may be said to be a
function of the body weight: a rat reduced in body weight by
starvation has a brain also reduced in weight and, on the other
hand, a rat excessive in body weight for its age, through overfeed-
ing, has an excess of brain weight for its age, as seen in the control
groups shown in table 4. In the interrupted starvation tests
(Series I), an average reduction of 29 per cent in the body weight

THE JOURNAL OF COMPARATIVE NEUROLOGY, VOL. 29. NO. 3

226 NAOKI SUGITA

25 days ©

Chart 2 Giving for each litter in this study the relation between the body
weight and the brain weight of the individuals. The capital letters for each
small chart designate the litter. The data given in table 3 were plotted according
to the advancing age in days.
eamee=e (Observed body weight of the underfed, in grams. ,

o----0 Qbserved brain weight of the underfed, in grams.
Observed body weight of the controls, in grams.
------ Observed brain weight of the controls, in grams.
For the body weight the scale is given on the left side and for the brain weight

the scale is given on the right side of the chart.

GROWTH OF THE CEREBRAL CORTEX PPA

is accompanied by 8 per cent reduction in the brain weight in the
test rats, and an excess of 14 per cent in the body weight by an
excess of 6 per cent in the brain weight in the controls. These
relations indicate that the brain weight is affected in abnormal
conditions of nutrition during early life so that its percentage is
altered by about one-third the percentage of the change of the
body weight, either plus or minus, as compared with the standard
values. On the other hand, in chronic inanition (Series II and
III) where the young rat is not disturbed, the brain-weight loss
was also 8 per cent against a body weight loss of 39 per cent.
It appears, therefore, that during the early helpless period the
brain development is highly disturbed by the changes in the
environmental conditions represented by removal from the nest,
but that when the rats are not disturbed it is much less affected
even by severe underfeeding.

Table 17 gives for each group in this study the brain weight—
body weight ratio, in percentage value, paired with the ratio
obtained from the corresponding standard values for the same
age and sex, calculated on the data given in table 4. The com-
plete data for each individual are contained in table 17a (un-
published) from which table 17 was condensed. In the underfed
the above ratios are all higher than the standard, as was to be
expected, while in the controls lower ratios are sometimes seen,
which, in turn, means an overgrowth of the body. The average
differences for each litter and group are given and the values are
indicative of the severity of starvation combined with the special
characteristics of the litter. Within each litter the range of the
differences is narrow but the evidence for this statement is fur-
nished by the unpublished detailed table 17 a.

16. A DISCUSSION ON THE CHANGE IN SHAPE OF THE CEREBRUM

In my first paper (Sugita, 717) it was stated that the Albino
cerebrum becomes relatively longer as the age advances. During
starvation, the rate of increase in every dimension diminishes
considerably, but the relations between the three dimensions re-
mains nearly unchanged, so that, as a result, the underfed brain
is somewhat elongated in shape in comparison with the standard

TABLE 17
Giving for each litter group in this study the average age, the sex, the brain weight—
body weight ratio, compared with the same ratio for the standard rat of the same
age and sex. The difference of the ratio for each group is given in the last column
of the table. This table was condensed from table 17a (unpublished) for the indi-
vidual cases. At the foot of the table the averages for the test and control groups
are given.

terete (The same | pIFFER-
Se GLone: AND tae state al SEX aneen TO par eed pret cs
WEIGHT same age STANDARD
days per cent per cent per cent
Series I ;
AY ed asd, at A eel ee See 7.9 6.5 1.4
h 405 JU 15 AL Gi 7.4 (iss +1.1
b, e, g OFM 8 3m 6.4 6. —0.4
i (On JUL 17 ii Am? Qxil —1.9
Series I
Bare, est Ai, | ato, We 8.7 Gad, +2.0
1 40 iu! 19 1m 8.3 Oe i
b, d Cr 6 Pent 7.6 6.5 +1.1
oe hy 1 Cr it 18— ont One 6.0 —0.3
Series I
Ca, c,d 4u5 JU 20 Demeter Cath 5.8 +1.9
b,e Car 22 2f one B58 —0.2
Series I
Da,c,d Ts i 12— |1m, 2f 183 6.8 +4.5
aLe 4Ue Us 18 lm 8.4 6.2 +2.2
b Cm 9 1m 7.8 (fel +0.7
f Cail 22 lm bal 5 —0.5
Series I
Ea, b, c,d ARE 12— |}3m,1f 8.6 6.8 +1.8
g, h ahs 08 20 Det 7.0 5.6 +1.4
emt Cy Ju 17— tim, i O26 6.4 —0.8
Series II
F a, b Basle 13— IL sons 1 i 9.1 6 +2.3
c-] 405 JU 25+ |4m, 6f as Sil. +2.4
Series III
G a-g 4A dE 11+ |4m, 3f 10.3 6.9 +3.4
h-j ahs 1 22 |e tr lak 9.3 O20 +3.8
Average } Pl ere 9.3 6.8 +2.5
(Ser. I-IIT) AMS TUL 21+ vans) 5.8 +2.1
Average } Cor 8— 7.3 6.8 +0.5
(Ser. I) (Os 101 19+ One 5.9 —0.7

»

GROWTH OF THE CEREBRAL CORTEX 229

brain, which is the same in weight but younger. As shown in
table 5, in the underfed brains the measurement L.G (the sag-
ittal diameter) is on the average nearly 2 per cent (about 0.25
mm. in a brain weighing 1.0 gram) greater.than the standard,
while, on the other hand, as shown in table 6 a (unpublished),
in the underfed the cortical thickness at the frontal pole (locality
I) which was measured almost in the same direction with L.G
is also greater by 10 per cent (about 0.25 mm. in a brain weighing
1.0 gram) than the standard for the same brain weight, while the
cortex at the occipital pole (locality V) is nearly equal to the
standard in thickness. Considering together the above facts,
the sagittal length of the central nuclei only, if measured between
the frontal and occipital poles, would be supposedly about the
same in both the underfed and the standard brains weighing alike.
~ On the other hand, the width W.8 is, in the underfed, less by
nearly 2 per cent (about 0.3 mm. for 1.0 gram brain) than in the
standard, and the cortical thickness at locality VII, which was
measured at the side of the cerebrum, is thicker in the underfed
by nearly 10 per cent (about 0.4 mm. for the both hemispheres in
a 1.0 gram brain (based on the unpublished table 6b for each
locality), and therefore the central nuclei in the underfed are less
in width by about 0.7 mm. (for a 1.0 gram brain) than the stand-
ard for the same brain weight. In short the central nuclei are
notably elongated in shape in the underfed brain compared with
the normal brain of like weight.

17. A DISCUSSION ON THE THICKNESS OF THE CORTEX IN THE
UNDERFED

As described in Chapter 7, the cortical thickness in the
starved brain is on the average markedly greater than the stand-
ard for the same brain weight. In the sagittal sections, the local-
ity I surpasses the standard most, the localities II and III are
the next, while the localities IV and V are almost equal in thick-
ness to the standard (these statements are based on the unpub-
lished table 6a for each locality). This order in which the
localities surpass the standard in thickness is the same as the
order in rate of increase in the cortical thickness during the post-

230 NAOKI SUGITA

natal growth (Sugita, 17a). The same statement is true for
the localities VI, VII, and VIII in the frontal sections (based on
the unpublished table 6b). The order in the rate of increase in
the cortical thickness is an index of the grade of intensity in cell
migration to those localities and of the growth impulse of the
elements there. From previous studies (Sugita, 717 a), it was
found that, as a rule, the cortical thickness decreases from the
frontal to the occipital pole and from the dorsal to the ventral
aspect, and the nearer a locality is to the ventricular wall or the
matrix the more rapid the rate of increase in the thickness of the
cortex. In underfed brains, the localities which show normally
the higher rate of increase in thickness are also greater in the
cortical thickness when compared with the standard. So, in the
underfed, the cerebral cortex is generally thicker than the stand-
ard for the same brain weight and thicker in each locality in pro-
portion to the rate of increase in the thickness of that locality
under normal conditions.

In short, the growth in the cortical thickness in the case of the
underfed is more advanced than that of the normal brain of the
same weight, which is, of course, younger.

18. A DISCUSSION ON THE RELATION BETWEEN CELL DENSITY AND
THE COMPUTED VOLUME OF THE CEREBRAL CORTEX

As stated earlier, the cell density of the cerebral cortex, repre-
sented by the number of nerve cells in two unit volumes (NV), is,
in the underfed Albino brain, under sixteen days in age, consid-
erably higher than the standard for the same age, and accord-
ingly the cell size in the underfed must be smaller than the stand-
ard size and, by inference, the cell attachments also underde-
veloped for the age. The relations between these data will be
examined now according to my measurements as presented in this
paper.

The cortical area as measured in the sections from the under-
fed brains proves to be slightly greater than the standard values
for the same brain weight, but on the other hand, it is distinctly
less in brains under sixteen days of age than the standard values

GROWTH OF THE CEREBRAL CORTEX Ty |

for the same age, which belong to brain weights higher by about
10 per cent.

Let us take as an example an underfed brain which weighs less
than 1.0 gram for examination. ‘The computed volume of the
cerebral cortex is in the underfed smaller on the average by 16
per cent than the standard for the same age (chapter 9). As
shown by calculation, the computed number of nerve cells in the
entire cortex is almost the same in both the standard and the
underfed, throughout all ages, so that the process of cell division
appears to have been going on undisturbed by the condition of
underfeeding. The cell density, the cell size, and the cortical
volume must therefore be regulated so as to provide the cerebral
cortex with the number of cells fixed according to the age, regard-
less of the starvation.

To present the relation, the formula N x L.F x W.D x T
was used. The value.of N <x L.F x W.D x T has proved in
my present material from the underfed to have been 1.7 per cent
higher than the standard, but as this is open to some correction,
it may be regarded as approximately the same in both the under-
fed and the corresponding standard. ‘To be less in the cortical
volume, which was computed by the formula L.F x W.D x T,
by about 16 per cent or more, the cell density must be increased
by about 19 per cent or less theoretically. ° This latter figure is
fairly in accord with that obtained in my direct observation;
that is, 17 per cent excess in the number of cells in a unit volume
in the underfed brains (chapter 10). To be reduced in cortical
volume by 16 per cent or more, the individual cell must theoret-
ically be reduced in volume also in the same ratio, in order not to
be reduced in total number. My results in cell-size measurement
showed that the individual cells measured are reduced in average
diameter by about 12 per cent, and accordingly in average volume
by about 30 per cent or more. These figures appear somewhat
higher than was to be expected, but it must be recalled that these
figures apply only to the largest cells found in the measured
locality, and this class of cells may suffer a disproportionate
arrest, so that the figures do not indicate what has taken place in
the small cells and those of average size. Furthermore, in the

Zon NAOKI SUGITA

cerebral cortex the neuroglia, the intercellular tissue and the
blood-vessels occupy considerable space and these may not be
reduced in volume in the same proportion as the large nerve cells.
These facts combined seem to furnish an explanation why the
largest nerve cells, which have been here studied, deviate some-
what in size from the figures theoretically to be expected.

The data here presented show, I think, that the relations
between the cell density and the cortica! volume in the underfed
fit with the formulas presented earlier and which represent the
relations in the normal Albino brains.

19. A DISCUSSION ON THE PROCESS OF MYELINATION

Tables 14 and 16 supply the data on which the myelination
process in the underfed Albino brain may be tentatively dis-
cussed. s

In Donaldson’s series (11), which consisted of twenty-two
litters of albino rats in which the underfeeding was begun at 30
days of age and in which all were killed after three weeks and
compared with the controls from the same litter, the average
brain weight of the underfed was 1.402 grams and the percentage
of water 79.28, while the average brain weight of the controls
was 1.519 grams and the percentage of water 79.39. Here the
underfed had 0.11 per cent less water. By examining the sec-
tions from the underfed and the controls, the author could not
discover any recognizable difference in myelination between them.
Hatai (’04) made a partial starvation experiment, extending over
three weeks, using the albino rats in the growing stage, about
thirty days old. In this series, the final average brain weight was
1.341 grams and the percentage of water 79.15 or 0.21 per cent
less than in the controls from the same litter and killed at the
same age and in which the final brain weight was 1.508 grams
and the percentage of water 79.36. In the same series, the
solids extracted with alcohol and ether were determined. ‘The
average amount cf the extractives in the test brains was 46.7 per
cent, or 0.9 per cent more than in the controls, in which it was
45.8 per cent. Though higher in percentage in the underfed,

GROWTH OF THE CEREBRAL CORTEX j Zoo

the absolute mass of the extractive substances is 0.065 gram
(about 5 per cent of the brain weight) less than in the controls
of the same age. The absolute weights were in the underfed
0.626 gram and in the controls 0.691 gram. These extractives
represent mainly the myelin which is contained in the sheaths of
the nerve fibers, and the above results mean that the extractive
substances are increasing at the same rate or slightly slower in
the underfed than in the controls.

In my material as seen in table 14, the underfed brains contain
slightly more water (by 0.48 per cent on the average) than the
standard of like age, and, as presented above (chapter 13), the
frontal section showed a higher percentage in area of the cortex
against the area of the central nuclei, which latter contain the
bulk of the myelin sheaths. On the other hand, the underfed
brains contain less water (by 1.4 per cent on the average) than
the standards of the same brain weight. Comparisons of the
absolute weight of the solids in the underfed brain with the corre-
sponding standard value for the same brain weight and for the
same age, based on data in ‘The Rat’ (Donaldson, 15), are given
‘in table 18. The underfed has shown as a rule considerably less
in total solids than the standard for the same age, though it
proved to be only slightly higher in percentage of water than the
standard (also table 14).

From the above, the absolute mass of the solids in the underfed
brain seems to be more than in the standard for the same brain
weight, but less than in the standard for the same age. So the
increase in solid mass is somewhat retarded by starvation. It will
be noted that in my series of rats the percentage of water in the
underfed was 0.48 per cent above that in the standards of like
age and this is the reverse of the results reported by Donaldson
and by Hatai in the studies just cited. This discrepancy prob-
ably depends on the fact that my rats are absolutely much
younger than those studied by the other authors, but the ex-
planation must await further study.

Since, as shown in chart 1, the relative values of the quantity
of the alcohol-extractives has a fixed relation to the absolute
weight of the solids in the brain, the above statement may be also

234 NAOKI SUGITA

TABLE 18
Giving for each individual in Litter H (Series IT) the sex, the age, the observed brain
weight, percentage of water, and the calculated absolute weight of the solids in the
brain, compared with the standards for the percentage of water and the mass of
solids for the brains of the same weight and of the same age. Averages are given
in the last line. .

STARVED STANDARD
hase xe the She For the same age
: Brain “| Mass of

No. Sex A : f ’ -
: = Ee | weight aia solids | Percent- Mase on | Benin Percent-| ass of
age of | “solids | weight | 22¢°f | ‘solids
grams | percent| grams | percent| grams | grams | percent| grams
Ha f 13 0.880} 86.39 | 0.120 | 87.45 | 0.110 |} 1.003 | 85.40 | 0.146
b f 17 1.024) 84.15 | 0.162 | 85.08 | 0.153 | 1.099 | 83.82 | 0.178
c f 23 1.135) 82.00 | 0.204 | 83.21 | 0.191 | 1.208 | 81.93 | 0.218
d f 28 1.166) 80.83 | 0.224 | 82.60 | 0.203 | 1.282 | 80.74 | 0.247
e m 32 1.215) 80.31 | 0.289 | 81.70 | 0.222 | 1.338 | 80.04 | 0.267
f f 33 1 101 8O0M2" 70. 219) | 83578") Oel79F | 139) | Or oo | On28a
g m 43 1.295) 80.24 | 0.256 | 80.51 | 0.252 | 1.468 | 79.32 | 0.304
Average ..... 28—| 1.117| 82.01 0.203 83.48 | 0.187 | 1.256 | 81.54 | 0.235

confirmed by the data given in table 16, in which it is clearly
shown that in the underfed the alcohol-extractives are slightly

less developed as compared with the standards for the same age.
‘

20. SUMMARY

1. Young albino rats were experimentally starved throughout
the suckling period, by one of the following methods:

Series I. Separation of the young from the nursing mother for
the maximum time each day.

Series II. Entrusting one mother with an excessive number of
young (over seventeen) at the same time and thus reducing the
amount of milk for each young one.

Series III. Starving the nursing mother and thus reducing the
quantity of milk secreted.

I employed five litters for Series I, two litters for Series I,
and one litter for Series III; in all forty-six individuals were sub-
jected to experiment and there were fourteen controls.

GROWTH OF THE CEREBRAL CORTEX 239

2. The underfed and the controls were killed at different ages
(between three and forty days) and the body measurements and
the brain weights recorded. The brain was fixed, sectioned,
stained, and examined according to the standard procedure pre-
viously adopted for these studies (Sugita, 717, 717 a, 718 b, ’18 ¢)
and the size of the cerebrum, the thickness of the cerebral cortex,
the area of the cortex in the sections, the number of nerve cells in
a unit volume of the cortex, and the size of the pyramidal and the
ganglion cells, were all determined and then corrected to the
values for the fresh condition of the material, by the use of the
correction-coefficients devised for these purposes.

Using these data, the relative volume of the cerebral cortex
and the number of nerve cells in the entire cerebral cortex were
computed, employing the formulas already devised by me
(Sugita, 718 b). All the observed and computed data were com-
pared with the corresponding respective standard values for the
normal Albino brain of the same weight or of the same age, as
given in my previous papers (tables 3, 4, 5, 6, 8, 11 and 13).

3. In Series I the underfed rats were found to be 29 per cent
less in the body weight and 8 per cent less in the brain weight, than
the standards for the same ages (between three and forty days).
In Series II and III the underfed rats were 39 per cent less in the
body weight while 8 per cent less in the brain weight. It appears ~
from this that starvation without removal from the nest, and the
corresponding disturbance to the young, retards the growth of
the brain relatively less, despite the greater arrest in the body
growth.

The underfed brain weight was found on the average 24 per
cent higher than the standard for the same body weight. ‘The
brain weights in the underfed have values between the standards
for the same age and those for the same body weight, but generally
fall nearer to the former.

The brain weight is a function of the body weight: a rat which
is more reduced in body weight by starvation has a more reduced
brain weight. The brain weight—body weight ratio is always
higher in the underfed than in the standard for the same age, and
the difference between the ratios roughly indicates the severity of

236 NAOKI SUGITA

the starvation. Thus in those severely underfed the difference is
higher than in those less severely underfed.

4. The shape of the cerebrum in the underfed is slightly elon-
gated as compared with that of the standard with the same brain
weight and approximates that for the same age. As the result of
underfeeding, the growth of the central nuclei seems to be more
arrested in width than in length and the changes in the growth
in the cortex in thickness matter little for the shape of the
cerebrum.

5. The thickness of the cortex is on the average 10 per cent
greater in the underfed in the localities I, II, VI, and VII than
in the standards for the same brain weight. By averaging accord-
ing to the entire section, the average thickness in the sagittal
section of the underfed exceeds that of the standard by 5.3 per
cent and in the frontal section by 8.7 per cent. The general
average thickness of the cortex in the underfed is consequently
greater by about 7 per cent than the standard for the brain of the
same weight. The localities which normally show the higher
rate of increase in thickness during the postnatal growth are
those which are notably greater in the cortical thickness in the
underfed brains.

6. The relative volume of the cerebral cortex, computed by the
- formula L.F x W.D x T, is generally smaller in the underfed
than in the standard for the same age. In the underfed brains
weighing up to 1.0 gram (that is, under sixteen days of age), it is
on the average less by 16 per cent or more, while in the underfed
brains weighing more than 1.0 gram it is 6 per cent greater than
the standard. So it may be said that, in rats underfed severely,
the cortical volume is considerably retarded in growth in early
period of development, but this is somewhat compensated or
overcompensated later when the brains attain the weight of more
than 1.0 gram or in age of more than sixteen days.

7. The cell density in the cerebral cortex, represented by the
sum of the number of pyramids in the lamina pyramidalis and
the number of nerve cells in the lamina ganglionaris in two unit
volumes of 0.001 mm.’, is considerably higher in the underfed
than in the standard rat for the same age. The excess in cell

GROWTH OF THE CEREBRAL CORTEX Dol

density in underfed brains weighing less than 1.0 gram is on the
_ average 17 per cent, and that in underfed brains weighing more
than 1.0 gram is almost equal to the standard for the same age.
As in the underfed brains weighing less than 1.0 gram, the relative
volume of the cortex-is smaller than in the standard, it follows
that the underfed brains, if they contain the same number of cells,
must have a relatively higher cell density in a unit volume to
balance the smaller total volume of the cortex.

8. The relative value of the computed number of the nerve
cells in the entire cortex, calculated by the formula N x L.F x
W.D x T, in the underfed was compared with the corresponding
standard value for the same age and the former was found to be
only slightly higher than the latter, so that they may be regarded
as practically the same. If so, the process of the cell division
in the cerebrum must have progressed according to the advancing
age, in spite of the starvation.

9. The size of the nerve cells was studied on the pyramids in the
lamina pyramidalis and on the ganglion cells in the lamina gang-
lionaris. The cell body of the pyramids in the underfed brains
weighing less than 1.0 gram is smaller by 11.2 per cent in average
diameter and that in brains weighing more than 1.0 gram smaller
by 8.3 per cent than the standards for the same age. The corre-
sponding figures for the nuclei of the pyramids are 15.3 per cent
and 11.0 per cent.

The cell body of the ganglion cells in the underfed brains
weighing less than 1.0 gram is smaller in average diameter by
11.8 per cent, and that in the underfed brains weighing more than
1.0 gram is smaller by 3.1 per cent than the standards for the
same age. The corresponding values for the nuclei of the gang-
lion cells are less by 12.5 per cent and 5.1 per cent, respectively.
So, on the average, the nerve cells in the cortex of the underfed of
all weights are smaller in average diameter by about 9 per cent
(for the underfed brains weighing less than 1.0 gram by about
12 per cent and for those weighing more than 1.0 gram only
by about 6 per cent), and consequently smaller in volume by
about 25 per cent than the standard cells of the same age. These
determinations apply only to the largest cells found at the
measured locality.

238 NAOKI SUGITA

10. The underfed brains (Series II) contain on the average
slightly (0.48 per cent) more water, if compared with the normal
brain of the same age, and somewhat (1.4 per cent) less water, if
compared with the normal brain of the same weight. This means
probably that, in terms of the percentage of water, the underfed
brain is slightly underdeveloped for its age and somewhat over-
developed for its weight. If the absolute weight of the solid
mass be calculated and compared with the standard for the same
brain weight and sex, the solids are found to be somewhat more
in the underfed and if the same compared with the standard for
the same age and sex the solids are always less in the underfed.
The relative value of the alcohol-extractives, obtained by com-
paring the initial brain weight with its weight after dehydration
and extraction in 80 per cent alcohol (for twenty-four hours)
and 90 per cent alcohol (for twenty-four hours) according to a
uniform procedure, shows that in the underfed brains the amount
of the aleohol-extractives is somewhat smaller than in the normal
of the same age.

The above observations indicate that in the underfed the mye-
lination process in the brain is somewhat retarded for the age.
This assumption was supported in a general way by the direct
examination on the sections obtained from the underfed brains.

11. Briefly, we conclude that by starvation in the early days
the brain suffers much in its development in toto, but the cell
division is going on quite normally according to its age. The
growth of the cells in size is retarded and the formation of mye-
linated fibers somewhat diminished by inanition. So the smaller
weight and size of the underfed brain is due to an arrest in the
growth and development of the constituent neurons and not to a
decrease in their number.

GROWTH OF THE CEREBRAL CORTEX 239

LITERATURE CITED

Brecuterew, W.von 1895 Uberden Hinfluss des Hungerns auf die neugeborenen
Tiere, insbesondere auf das Gewicht und die Entwicklung des Gehirns.
Neurol. Centralbl., Bd. 14, pp. 810-817.

CuHossaT, CHARLES 1843 Recherches experimentales sur l’inanition. Mémoire
auquel |’ Académie des Sciences a décerné en 1841 le prix de physiologie
experimentale. Extrait des mémoires de l|’academie royale des sciences.
Tome 8 des savants é6trangers. Paris, Imprimiere Royal.

Donaupson, H.H. 1911 The effect of underfeeding on the percentage of water,
on the ether-alcohol extract, and on medullation in the central nervous
system of the albino rat. Jour. Comp. Neur., vol. 21, no. 2. 1915
The Rat. Memoirs of The Wistar Institute of Anatomy and Biology
no. 6.

Faucx, C. P. 1854 Beitraige zur Kenntnis der Wachstumsgeschichte des Tier-
k6érpers. Virchow’s Archiv, Bd. 7.

Harar, 8S. 1904 The effect of partial starvation on the brain of the white rat.
Amer. Jour. Physiol., vol. 12, no. 1.

1908 Preliminary note on the size and condition of the central nervous
system in albino rats experimentally stunted. Jour. Comp. Neur.,
vol. 18, no. 2.

1915 Growth of the body and organs in albino rats fed with a lipoid-
freeration. Anat. Record, vol. 9, pp. 1-20.

Jackson, C. M. 1915a Effect of acute and chronic inanition upon the rela-

tive weights of the various organs and systems of adult albino rats.
: Amer. Jour. Anat., vol. 18, pp. 75-116.

1915 b Changes in the relative weights of the various parts, systems

and organs of young albino rats held at constant body weight by under-

feeding for various periods. Jour. Exp. Zodél., vol. 19, pp. 99-156.

LasarEw, N. 1895 Zur Lehre von der Verinderung des Gewichts und der
zelligen Elemente einiger Organe und Gewebe in verschiedenen Perio-
den des vollstindigen Hungerns. Dissertation, Wasschau (cited by
MiihImann, 799). é

Moreuuis, 8S. 1911 Studies of inanition in its bearing upon the problem of
growth. I. Archiv f. Entw., Bd. 32, Heft 2.

Miuuimann, M. 1899 Russische Literatur iiber die Pathologie des Hungerns
(der Inanition). Sammelreferat. Centralbl. f. allg. Pathologie, Bd.
10, pp. 160-220; 240-242.

Sueira, Naokr 1917 Comparative studies on the growth of the cerebral cortex.

I. On the changes in the size and shape of the cerebrum during the
postnatal growth of the brain. Albino rat. Jour. Comp. Neur., vol.
28, no. 3.
1917 a Comparative studies on the growth of the cerebral cortex.
II. On the increase in the thickness of the cerebral cortex during the
postnatal growth of the brain. Albino rat. Jour. Comp. Neur., vol.
28, no. 3.

240 NAOKI SUGITA

1918 a Comparative studies on the growth of the cerebral cortex.
IV. On the thickness of the cerebral cortex of the Norway rat (Mus
norvegicus) and a comparison of the same with the cortical thickness
in the albino rat. Jour. Comp. Neur., vol. 29, no. 1.
1918 b Comparative studies on the growth of the cerebral cortex.
V. Part I. On the area of the cortex and on the number of cells in a
unit volume, measured on the frontal and sagittal sections, of the albino
rat brain, together with the changes in these characters according to
the growth of the brain. PartII. Onthe area of the cortex and on the
number of cells in a unit volume, measured on the frontal and sagittal
sections of the brain of the Norway rat (Mus norvegicus), compared
with the corresponding data for the albino rat. Jour. Comp. Neur.,
vol. 29, no. 2.
1918¢ Comparative studies on the growth of the cerebral cortex.
VI. Part I. On the increase in size and on the developmental changes
of some nerve cells in the cerebral cortex of the albino rat during the
growth of the brain. Part II. On the increase in size of some nerve
cells in the cerebral cortex of the Norway rat (Mus norvegicus), com-
pared with the corresponding changes in the albino rat. Jour. Comp.
Neur., vol. 29, no. 2. :

Voir, Cart 1866 Uber die Verschiedenheiten der Hiweisszersetzung beim
Hungern. Zeitschrift fiir Biologie, Bd. 2.

Watson, JoHn B. 1903 Animal education. Con. from the Psychol. Lab.
Univ. of Chicago, vol. 4, no. 2, pp. 5-122.

,AUTHOR’S ABSTRACT OF THIS PAPER ISSUED
BY THE BIBLIOGRAPHIC SERVICE, MARCH 30

COMPARATIVE STUDIES ON THE GROWTH OF THE
CEREBRAL CORTEX

VIII. GENERAL REVIEW OF DATA FOR THE THICKNESS OF THE
CEREBRAL CORTEX AND THE SIZE OF THE CORTICAL CELLS IN
SEVERAL MAMMALS, TOGETHER WITH SOME PGSTNATAL GROWTH
CHANGES IN THESE STRUCTURES

NAOKI SUGITA
From The Wistar Institute of Anatomy and Biology

THREE FIGURES AND TWO CHARTS

‘I. INTRODUCTION

Years ago Schwalbe (’81) pointed out as characteristic somatic
expressions, which might be taken to indicate the grade of in-
telligence of a species of animals, the following four measure-
ments on the brain: 1) total weight of the brain; 2) total num-
ber of nerve cells in the brain; 3) total area of the surface of the
hemispheres of the brain, and 4) the thickness of the cerebral
cortex. Since then he and many other neurologists have en-
deavored to gather data on the morphological evidence for the
development of mental ability. Donaldson and Hatai (‘The
Rat,’ Donaldson, ’15) have made systematic observations on
the growth changes in the central nervous system as well as in
other organs and systems, using exclusively the albino rat. As
a result of their investigations, the postnatal growth of the brain
and the spinal cord, in gross measurements, and the relations of
these to the other systems during growth have been deter-
mined. In line with these studies, I also made further re-
searches on the growth in the thickness of the cerebral cortex,
the size and shape of the cortical nerve cells and the relative
number of the cortical cells in both the Norway and albino rats.
The results of these researches have been already presented
(Sugita, 717, 717 a, 718, 718 a, ’18b, 718 c¢, ’18 d), with references

241

THE JOURNAL OF COMPARATIVE NEUROLOGY, VOL. 29, NO. 3

242 NAOKI SUGITA

to some similar studies by other authors. These data give us a
general idea of the postnatal development of the cerebral cortex
in a representative mammal (albino rat), and we may fairly
infer that similar changes occur in other mammals during the
growth of the brain. To test how far my conclusions on the
mode of the development of the cerebral elements during post-
natal life may be extended, I shall review and summarize in the
present paper the results obtained by several authors on the
development of the cortex in other mammals and make a com-
parison of their results with the data obtained by me.

II. THICKNESS OF THE CEREBRAL CORTEX IN THE ALBINO RAT

The results obtained by me regarding the cortical thickness
in the brain of the albino rat may be summar zed as follows
(Sugita, 717 a):

1. The cortex at the frontal pole of the hemisphere is the
thickest and that at the occipital pole is the thinnest. Speaking
in general terms, the cortex diminishes in thickness from the
frontal to the occipital pole and from the dorsal to the ventral
aspect.

2. After birth, the general average of the cortical thickness
increases very rapidly during the first ten days, thickening from
0.74 mm. at birth to 1.73 mm. at ten days, more than twice the
thickness at birth, while the brain weight increases from 0.25
gram to 0.95 gram during the same period. ‘This is designated
by me the first phase of the cortical development.

3. Between the tenth and the twentieth day after birth, the
cortical thickness increases more slowly, attaining at twenty
days to within 4 per cent of the full thickness of the cortex,
namely, 1.84 mm., or about 2.5 times the thickness at birth,
while the brain weight increases to 1.15 grams. This is desig-
nated the second phase of the cortical development.

4. From the twentieth to the ninetieth day, the cortical thick-
ness increases but little on the average, attaining at ninety days
the thickness of 1.93 mm., or 2.6 times the thickness at birth,
while the brain weight has increased to about 1.80 grams. This
is designated the third phase of the cortical development.

GROWTH OF THE CEREBRAL CORTEX 243

After the ninetieth day, there is no significant change in the
thickness of the cortex, but the area of the cortex increases as the
brain weight rises and at 2.0 grams is greater than at 1.15 grams_
(20 days) by about 45 per cent.

5. In the first phase the cortex increases its thickness by re-
ceiving some newly formed cells from the matrix and many
already formed from the transitional layers and at the same time
by the general enlargement of the neurons, especialy the cell
bodies; in the second phase, however, it grows main'y by the
enlargement of the cell bodies and the growth of the axons and
dendrites; while during the third phase it thickens only slightly,
but extends in area as the result of the ingrowing axons and the
formation of the myelin sheaths and non-nervous structures.

6. The cortex at the frontal pole increases its thickness very
rapidly and steadily, continuing to do this even after the end
of the second phase, while at all the other localities the cortex
thickens in the same proportion, so that at the end of the second
phase all the localities reach nearly the full thickness, but main-
tain their initial relations. The localities heterogeneous in their
cell lamination show in the course of thickening some deviation
from the localities which are typical.

7. The cortex generally attains nearly its full thickness before
myelination, as shown by the Weigert staining method, occurs
in it. In the Albino, the cortex has nearly its mature thickness
at twenty days, just before the young rat is weaned and when
the brain has attained only a trifle more than half its final
weight. The growth of the cortex in thickness is therefore
precocious.

III. INCREASE IN CORTICAL THICKNESS DURING GROWTH OF THE
BRAINS OF THE MOUSE AND THE GUINEA-PIG

Mouse. Isenschmid (711) has made a study of the cortical
cell lamination in the brain of the mouse and given a map of the
topographic localization in the hemisphere, which is repro-
duced here as figure 1. De Vries (712) and Rose (712) have also
presented a brain map of the mouse according to their studies
on the cell architecture of the cortex; a map which resembles that

244 NAOKI SUGITA

Fig. 1 Cortical area of the mouse (Mus musculus)—reproduced from the
original by Isenschmid (’11); the thickness of the cortex at each area desig-
nated on the map is tabulated in table 1 of this paper. Double lines
show borders of three—the dorsolateral, the frontomedial, and the suboccipital—
regions of the neopallium. Shaded parts (areas t, s, and h) do not le in the same
(median) plane as the other areas. A = Dorsal view of the right hemisphere;
B = Lateral view of the right hemisphere; C = Medial view of the right hemi-
sphere. B.olf. = Bulbus olfactorius; C = Corpus callosum; c.A. = Cornu Am-
monis; cl. = Claustrum; s.p. = Septum pellucidum. s—s’ = the level cor-
responding to that from which the sagittal sections of the Albino brain were
taken by me; f—f’ = the evel corresponding to that from which the frontal
sections of the Albino brain were taken by me; h—h’ = the level corresponding
to that from which the horizontal sections of the Albino were taken by me.

GROWTH OF THE CEREBRAL CORTEX 245

TABLE 1
Giving for each locality of the brain of the adult mouse the characteristics of the
cell lamination, the thickness of the cortex on the slide as determined from the
photograms given by Isenschmid (’11), and the relative thickness of the outer and
inner layers as presented by the same author. For the localities consult figure 1
in this paper, which was reproduced from the original of Isenschmid (711)

RELATIVE
THICKNESS OF
THE OUTER AND

ees CHARACTERISTICS OF. THE AREA IN CELL-LAMINATION THICKNESS OF | INNER LAYERS
(FIG. 1) THE CORTEX
OF THE
CORTEX

OUTER: INNER?

mm
a) Largest ganglion cells contained (18 X 204)... 0.73 48: 52
alam Notsomanrgencelll sen. 4.08. oiiccsa stern: cog ekewene
Des lV alan erktlitekesnshe Sr cree sae ot ey roe ds eee cies 0.86 45: 55
CER eRe leery «ry WAR ee ks aha deg, MR'e Tbe 8 0.50 45: 55
CUM Ese ctsicrc hac tae Sete Chat a ee ACER ch af ¢ 0.53 45: 55

Gin lmicansitionalqart pygon tases a hi aertriele cms alee as).
hin ie aleopallaims 2: s 48 send cee seer ticks eect ad 2
e IV layer not so well developed................ 42: 58
f Adjoins to fovea limbica, cell lamination not

CLES pb trea re. Meee eis hae 0.62
THe 3] eked tienes aed Cee eC Aa at AAR MRM aie 8 UA OO og 0.44
k Transitional part (ganglion cells: 13 & 15 n).. 0.81 34: 66
] At the corner (ganglion cells: 12 X 14y)...... 0.78 P32 TC
100: 4 nd Beco eR Meroe: Ok Satie blew kown co hikck Bese Drie ck ea ere aS 0.71-0.61
Tema Pe ren eA ee EEN: cae satol esters Ph estde cvs hee 1.201 22:78
q (Gangliontcellsissb) <8 jp) ners se res ett ha 2 0.56 28: 72
s Similiar: GOraVe BaGlie chin ny ierte aye ycuatpe seine vee aches 0.26
Be Aa RS 2 AMES Re (CEE Ae Rare Pe On WO) Se ee 0.34

' Section cut obliquely.

2 The outer layer = the lamina granularis externa plus the lamina pyra-
midalis plus the lamina granularis interna. The inner layer = the lamina
ganglionaris plus the lamina multiformis.

of Isenschmid. Isenschmid (711) has recorded the thickness
of the cerebral cortex of the mouse on the slide at every locality
mapped in his figure (fig. 1). But the actual thickness not being
given explicitly for each locality, I calculated the values from
the direct measurements made on the photograms. The brain
was fixed in alcohol, imbedded in paraffine and cut in 10-micra
sections and stained with kresyl-violet. The thicknesses of the
- cortex on the slide as thus obtained are given for each locality
in table 1 and also are condensed in table 2, in which the data

246 NAOKI SUGITA

TABLE 2

A comparison of the thicknesses Of the cerebral cortex at several corresponding
localities in the albino rat and in the mouse. The data for the albino rat were taken
from table 11 in my previous paper (Sugita, ’17 a, p. 578) and the data for the
mouse were taken from a paper by Isenschmid (11). The order of increasing
thickness is the same in both animals

ALBINO RAT MOUSE

Average Average

Locality _| thickness of ICorresponding locality | Thigkness of cortes at | thickness of

locality locality

mm. mm. mm.

V and XIII 24. c 0.50 0.50
IV 1.42 d 0.53 0.53

XIT and VIII 1.67 e and i 0.65 and 0.44 0.55
III and XI 1.91 aande 0.73 and 0.65 0.69
VI 2.01 1 (corner) 0.78 0.78

II and X 2.03 k and b 0.81 and 0.86 0.84
VII 2.29 b 0.86 0.86

I and IX 2.99 frontal pole 1.00 1.00
IAVELAP Cs se la 1.94 IANET AR Cb acm Ree eT eee 0.72

for the Albino are so entered that the cortical thicknesses at the
corresponding localities in the two forms may be compared.
The order of the localities is arranged according to the increasing
thickness in the Albino (taken from table 11, Sugita, 717 a, p.
578). The average value of the cortical thickness in the mouse
is, on the slide, 0.72 mm., and if corrected to the fresh condition
would probably be somewhat thinner than one-half the average
thickness of the Albino cortex. The order of the thickness ac-
cording to localities is quite the same, so that in both forms the
cortical thickness decreases from the frontal to the occipital
pole and from the dorsal to the ventral aspect. Moreover, the
cortex at the frontal pole is the thickest and has double the thick-
ness of that at the occipital pole.

As seen in figure 1, the cerebral hemisphere is divided by Isen-
schmid into three main regions—the dorsolateral, frontomedial
and suboccipital regions—separated by the double line in figure 1.

The average cortical thickness in the dorsolateral region
(fig. 1 a) is 0.56 mm. at its hinder-medial part and 0.90 mm.

GROWTH OF THE CEREBRAL CORTEX 247

at its fore-lateral part, and in this region the lamina zonalis is
about one-twelfth, the main outer layers (the lamina granularis
externa plus the lamina pyramidalis plus the lamina granularis
interna) about two-fifths and the main inner layers (the lamina
ganglionaris plus the lamina multiformis) about one-half the
total thickness of the cortex. In the frontomedial region (fig.
1c) the cortical thickness at the frontal pole is 1.00 mm. and
that at the caudal part is 0.35 mm., while in the suboccipital
region the cortical thickness ranges between 0.2 and 0.3 mm.

Ww

i

bf
nN)

be
/ MN)

TT

0°20

B 34 6 74 94 {24:11 M

Fig. 2 Showing diagrammatically the thickness of the cerebral cortex at lo-
cality a in the mouse at different ages. Reproduced from the original given by
Isenschmid (11). B= at birth. M = at maturity. The other arabic num-
bers show the age in days. = lamina zonalis; II = lamina granularis externa;
III = lamina pyramidalis; [V = lamina granularis interna; V = lamina gan-
glionaris; VI = lamina multiformis. The cell outlines found between the last
two diagrams indicate the relative size and shape of the cells in each cortical
layer.

Isenschmid has given also diagrams illustrating the growth in
cortical thickness at locality ‘a’ (fig. 1 a, corresponding approxi-
mately to locality III in my study, fig. 2, Sugita, "17 a, p. 525),
sampled from material at several different ages and magnified
uniformly. These are also reproduced here as figure 2. The
diagrams show that as age advances the lamina pyramidalis
(II and III) thickens steadily and continuously while the lamina

248 NAOKI SUGITA

ganglionaris (V) and especially the lamina multiformis (VI)
grow much less rapidly. Chart 1 gives a comparison of the in-
crease in the cortical thickness at corresponding localities (lo-
cality ‘a’ of the mouse and locality III of the albino rat) in the
albino rat and the mouse, the data being from Isenschmid (’11)
and Sugita (’17 a). In the Albino the cortex attains nearly its
full thickness at twenty days (weaning time), while in the
mouse this stage was reached between twelve and seventeen
days of age, very closely corresponding to the weaning time of

m.

m
2.0 [
18

B24 6 8 10 12 14 16 18 20 22 24 26 28 30 Ageindays.

Chart 1 Giving the cortical thickness of the albino rat and of the mouse ac-
cording to age. The data for the albino rat are taken from Sugita (717 a) at
locality III measured on the sagittal section and the data for the mouse are
taken from Isenschmid (’11) at locality ‘a.’ These two localities approximately
correspond.

the mouse, which is fifteen days. The remarkable phase during
which the rapid increase in cortical thickness takes place in the
Albino (first ten days after birth) cannot be clearly identified
on the graph for the mouse cortex. It must be recalled, how-
ever, that data on the mouse cortex have not been corrected for
the action of the reagents, while the data for the rat have been so
corrected. The outstanding fact, however, is that the cerebral
cortex in both forms attains nearly its full thickness just before
the weaning time.

GROWTH OF THE CEREBRAL CORTEX 249

Guinea-pig. I have had the opportunity at The Wistar In-
stitute to examine the sections of the guinea-pig brains prepared
by Allen (04) for her study on the myelination of the nervous
system of that animal. The sections were cut in series in the
frontal plane from material fixed in Miiller’s fluid, imbedded in
celloidin and stained by Weigert’s method for the myelin sheaths.
The thickness of the cerebral cortex in the adult guinea-pig
(body weight, 618 grams; brain weight not recorded) is on the
average 1.90 mm. (1.80 mm., 1.88 mm., and 2.01 mm., respec-
tively, at the localities corresponding to localities VI, VII, and
VIII examined by me on the frontal section of the Albino brain
at the level of the commissura anterior). The corresponding
measurements at birth (body weight, 108 grams) are 1.71 mm.
(and 1.51 mm., 1.75 mm., and 1.86 mm., respectively) and those
at thirty-five days (body weight, 250 grams) are 1.85 mm. (and
1.77 mm., 1.86 mm., and 1.92 mm., respectively). So, from
birth on to the maturity, the cortical thickness has on the aver-
age increased only 11 per cent. According to Allen, the guinea-
pig at birth is covered with hair, has complete muscular devel-
opment, and is almost independent of the mother, the central
nervous system being practically completely myelinated, whereas,
by contrast, the albino rat is born quite naked, extremely help-
less and undeveloped, and myelination in the brain has not be-
gun. The guinea-pig is psychically mature soon after birth
(three days after birth); the degree of development of the cen-
tral nervous system of the new-born guinea-pig corresponds to
that of the albino rat at twenty-three to twenty-seven days or
its period of first psychical maturity. A new-born guinea-pig
is found to have a cerebral cortex in which the myelination is
going on.

Comparing the sections from the guinea-pig brain with those
from the albino rat brain, it appears that the new-born guinea-pig
corresponds to the albino rat of about ten days in cortical thick-
ness, but seems to be older when judged by the myelination of
the cortex. This coincides with observation that the guinea-
pig is, almost from the start, relatively independent of the
mother.

250 NAOKI SUGITA

IV. THE CORTICAL THICKNESS AT SEVERAL LOCALITIES IN THE
BRAINS OF SOME MAMMALS OTHER THAN THE RAT

Few papers have been published regarding the differences in
the thickness of the cerebral cortex at given localities of the brain
in mammals other than the rat, except for man. Yet even in
these cases, the techniques of hardening, imbedding, and staining
used by the different authors are dissimilar and their results are
accordingly not precisely comparable. Despite this, however, it
has seemed worth while to make a survey of the data at hand.

Rabbit. Bevan Lewis (’81) has given as the natural thickness!
of the cerebral cortex of the adult rabbit the following figures
(table 3) according to localities. For the localities, the map
made by him and reproduced by me in a previous paper (Sugita,
17 a, fig. 10, p. 544) should be here consulted. He has pre-
sented the thicknesses of every layer of the cortex separately,
but here only the total cortical thicknesses, as computed by me
from his data, are given in round numbers.

Pig. Lewis (’79) has also determined the cortical thickness
at several localities in the pig brain (the names of the localities

TABLE 3
The thickness of the cerebral cortex of the rabbit, quoted from Bevan Lewis (’81)
Depth of cortex on a plane with genu of corpus callosum:

mm.
Gyrus LOGMICAtUS «rect wea o0 6 og te Sk nba ene ye eee tae iz,
Sagittalvangle: 2.ccrpre +22 ees who ah Sakl Shand sends eet chee ote areola 2.23
BE ctra-lam biryani oe. & he sis Gane nae oe) eae ee eee ee ee 2.81
INearilimbiteysmlicnsie heh icy) cauacha ee er ocean eer eee 2.31
Depth of cortex on a plane with posterior border of corpus callosum:
Gyrus LOrnVea Lusher rns eo. oe ne ee aoe eee ee ee Rene) eee eee 1.70
Sapittalianigletss 97 ea. Ua. Me PASO ores Meee es oe eee 1.91
Txtraslurnioicne 4.4 eae tend cones une: soaked seco ees Ae ae nen a eee 2.46
Depth of cortex of the modified lower limbic type................. 2.23 to 2.47
Depth of cortex in the cornu Ammonis:
Amterlon TEgIONS:. mare tae ian. Soar oe A nr ao ee eee ere PD OA
Average: atisix differentisites:).|. sehen. a. 3) Loeb aete aotearoa 2a2e

1 Lewis measured the cortical thickness on sections cut by the freezing micro-
tome from fresh material and then hardened by osmic acid, stained by aniline
black and mounted in Canada balsam. According to his statement we obtain,
by this method, the natural depth of the cortex, no shrinkage occurring if the
preparations have been carefully made (Lewis, ’78).

GROWTH OF THE CEREBRAL CORTEX 251

TABLE 4
The thickness of the cerebral cortex of the pig, quoted from Bevan Lewis (779)
Depth of cortex from before backward:

mm.
(4.97
4.48
3.70
4.98
3.58
erik
PAV CT AD Claw) Ae gel gine Demand A KEEN cov al. fi antece #4 6 areraloer se Reon eee tes 4.22
(3.28
2.65
3.08
3.91

4.23
3.44

sia vCal O be yes. 3 re ee OTe ese tele ben, oe Eo eer

Upper parietal convolutions.......... BA Seach AEN USE a et

3.50
3.44
3.91
3.95

HAVEL ACR EST ke OTA, Aen Ee yo ota. cyory es ces
Gowersparietaleconvolutlonsseer eee eer. oor nice eeenre

JNA GTIE ZOE & & Rear diy BEw-0 PERIENCE Gee 5 BTS ER TG Os oe emer notte core a oc cole 3.64

are analogous to those given for the rabbit brain, loe. cit.). His
results are summarized in table 4. These values are distinctly
high compared with those for other mammals, as shown in the
various tables in this paper. These results taken together with
those for the rabbit just given, which are also noticeably high,
suggest that the determination by Lewis are for some reason
systematically too high.

Marsupials to man. Table 5 is quoted (slightly modified)
from Brodmann (’09) and gives for several species of mammals,
including man, the cortical thickness at six localities (areae
precentralis, frontalis, parietalis, occipitalis, hippocampica et
retrosplenialis) in the brain of each animal. The sections were
made by hardening the material in 4 per cent formaldehyde,
imbedding in paraffine, and staining by the modified Nissl’s
method, and the cortical thickness was measured by the microme-
ter directly on the slide. The average thickness was calculated
by me for the four areas, excluding the areae hippocampica et
retrosplenialis which are heterogeneous in cell lamination.

252 NAOKI SUGITA

TABLE 5

The cortical thickness at the corresponding parts of the cerebral hemisphere in dif-
ferent mammals, quoted from Brodmann (’09). According to his nomenclature,
area precentralis = type 4, area frontalis agranularis = type 6, area parietalis =
type 7, area occipitalis = type 17, area hippocampica = type 28, and area retro-
splenialis = type 29, as given in his ‘Hirnkarte’ (Brodmann, ’09)

mn 1 1S]
a m e Zz a
mn 4
fod est eee ie ees |) ae eee
SPECIES 3 a a o< a Py 8 5 a
al a iS) gr Ls im o8
A 3 B Be 3 5 Sy Ee ay
5 eS A a A ° x <n om
» 5 < <% < < < ag ab
a < a gQ < Q a Q 2 x Re
° fon] & fof (ot <i & >
Q 4 < < < < < < <
; grams grams mm. mm. « mm. mm. mm. mm. mm.
Homo sapiens (man)} 60,000} 1,400/3.0-4.5/3.0-3.8/3.08/2.3-2.6/2.5 | 2.3 |3.0
Cercopithecus (long-
tailed ape)....... 2,500} 85 3.0 De NDQsOL Pe Ga ee eo
eMuUry eect ees 1,800} 23 2.3 203) MGrl Abba soy 11S adie ie
Hapale(marmoset). 200 8 Weis || alee inlay Ibe Le alee [fil a)
Pteropus edwardsii

(vampire bat).... 375 Gols Lag LaG (flee 1.76 |1.52)1.4-1.76)1.66
Erinaceus euro-
paeus (hedgehog) AO! S385 |) TAYE) ok eH ES LO), Math fl Gil

Cercoleptes caudi-

FOU) ce peepee one 2,000 DAZ: 1 2.0 se | AS) ESOS Tes, HESo
Lepus _cuniculus
(nabs bith’. “ioe 2,200} 10 Pall 25331252)| 18° 1122>|0.8-1.5 1509
Spermophilus citil-
lus (ground
SQUisrel)'. -...4e 200); 92225)" 221 DAS NWS) dicot eo Onvome lees

Macropus- gigan-
teus (kangaroo)..| 5,000} 25 |2.8-3.1 PAP NO lar Il Tbe ees

Reviewing this table, it is readily seen that, within each
order, the animal which has a greater brain weight shows also a
greater cortical thickness, but a fixed relation between the
brain weight and the cortical thickness has not been here re-
vealed. In different orders, this relation is not true; the lemur
and the kangaroo have a similar brain weight (23 to 25 grams),

GROWTH OF THE CEREBRAL CORTEX 253

while the cortical thickness in the latter is much greater (by
about 25 per cent).

Prosimiae and primates. The following table (table 6) is
summarized from a paper by Marburg (’12) and shows for some
species of the prosimiae and primates the total cortical thickness
measured at four representative localities (gyri centralis, fron-
talis, temporalis et occipitalis). The average values were taken

by me.
TABLE 6
Thickness of the cerebral cortex at several localities in monkeys, as presented by
Marburg (12). Averages are calculated by me

AVERAGE

CEN- FRON- TEM- occi- <a ae a Tir
SPECIES TRAL TAL PORAL | PrTaL | Of the | Of the

GYRUS | GYRUS | GYRUS | GYRUS four three
locali- | locali-

ties ties

mm. mm. | mm. mm. mn. mm.

SUMMIa SAV TUS Ae ood aan bream koh cles aoe Bolu | Bose | B23} 2.84
iv lobatesn(Sps))eenern melee ae SMM lS ||| Seon mlerioe eae som|memultes
Semnopithecus masicus...........-4.... B03) | as I DB ahaa) |) oO: || Beis}
IMPVCOGUE TANTS a6 a bade ne Gaswoeeosonuek PAL | DITO) |) PTGS |W) ah 288) |) A BXO) | BE
Cynocephalus hamadryas...............| 2.97 | 2.70 | 2.03 | 1.35 | 2.26 | 2.57
Abeleshmilo erie ame, tae ck a noe totus ae ee 2.97 | 2.84 | 2.48 21D)
Remiunevianiisn7e sss ots ee ee ee SON Onl le 1Oy ele Oden ele G2 ele oll

This table also suggests that, in the order of monkeys, the
average thickness of the cortex varies so that those which have
the greater brain weight have also the greater thickness of the
cerebral cortex, but the brain weights are not available for
comparison.

V. THE THICKNESS OF THE CEREBRAL CORTEX IN MAN

Man. There are scores of papers giving the measurements of
the thickness of the cerebral cortex in man, but they are diverse
in the techniques used for preparing the material, in the locali-
ties selected for measurement, and also in the manner of meas-
urement. The results published before 1891 were all summa-
rized by Donaldson (’91), but the table is not reproduced here as,
- owing to the lack of the information necessary for the interpre-
tation of the values found, it has mainly an historical interest.

254. NAOKI SUGITA

Donaldson (’91) measured also the thickness of the cerebral
cortex at fourteen. localities from each hemisphere of nine nor-
mal brains (six males and three females), as shown in figure 3
reproduced from his original paper, in order to obtain control

A

Fig. 3. This figure shows the localities on the hemispheres from which the
samples of cortex were taken by Donaldson (91). Kor the thickness of cortex
at each locality see table 8 and chart 2. A = Lateral aspect. 3 is used to desig-
nate the insula, here not exposed. B = Ventral aspect; C = Mesial aspect.

values for the study of the brain of a blind deaf-mute, Laura
Bridgeman. The technique employed by Donaldson was fixa-
tion in bichromate and alcohol (potassium bichromate 23 per

cent plus % its volume of 95 per cent alcohol) for six to eight

GROWTH OF THE CEREBRAL CORTEX 255

TABLE 7

Giving the average cortical thickness of man, arranged according to age and sex,
together with the brain weight. Quoted from Donaldson (’91)

AGE BRAIN WEIGHT AVERAGE CORTICAL THICKNESS
Males
years | grams mm.
35 1419 2.81
35 1443 2.98
39 1393 2.82
45 1367 | 2nO2
57 1464 2.94
1 1210 Beli
Females
40 1196 2.74
45 iil} 2.90
uy 1312 3.07
Average
1331 2.92

weeks, washing in water for twenty-four hours, 95 per cent alco-
hol for two days, final preservation in 80 per cent alcohol, and
imbedding in celloidin. The sections were cut about 100 micra
thick and measured unstained under a low magnifying power
with a micrometer eyepiece, at the summit of the gyrus and at
the side, midway between the summit and the bottom of the
bounding suleus. To obtain the average thickness at the lo-
cality, the smaller figure was multiplied by 2, added to the larger
figure, and the sum divided by 3

Table 7 shows the average pnbh aes of the cortex (taken from
the fourteen localities) arranged according to sex and age,
quoted from Donaldson (’91). If we take the nine cases in this
table as the basis for computation, we find the mean thickness
of the cortex to be 2.92 mm., with a probable error of the mean
equal to +0.026 mm.

I wish to cite also the average thickness of the cortex, as thus
obtained by Donaldson (’91), according to locality (table 8).
These localities are shown in figure 3 and the relative thickness

256 NAOKI SUGITA

of the cortex at each is graphically presented in chart 2. Gen-
erally summarized, the average thicknes of the cortex of the adult
man is 2.92 mm.; females have a slightly thinner cortex than
males (differences less than 1 per cent, or 0.02 mm.) and the
right hemisphere usually has a cortex a few per cent less thick
than the left (maximum difference 7 per cent).

With the foregoing determinations are to be compared the
measurements by three other observers.

mm

376425 101 131211 8 9 14

Chart 2. -The curve was plotted according to table 8 to show the cortical
thickness at each locality as measured by Donaldson (’91. |. The numbers placed
by the ordinates indicate the thickness of the cortex in millimeters. The num-
bers for the localities are given below, and correspond to those in figure 3, A.
B and C.

In accordance with this plan, the results obtained in a careful
study by Hammarberg (’95) are tabulated in table 8. The
material used for this study was a brain of a male, twenty-eight
years old, mentally normal, and who died of typhoid fever.
The technique employed was fixation in 95 per cent alcohol,
imbedding in paraffine by means of xylol, sections 10 micra in

TABLE 8
Giving for several localities on the hemisphere of the adult human brain the thick-
ness of the cortex, as measured by different authors. The general average thick-
ness was taken, averaging all measurements presented by each author. For
reasons given in the text, these averages as they stand are by no means compara-
ble with each other. The data were taken from Donaldson (’91), Hammarberg
(95), Campbell ('05), and Brodmann (’08)

” |
Author Donel Haag Camp bell Brodmann
Cell | Cell [| Celt | Fiber | Cell | Fiber
rm. | wm | mm | mm | wm | min
| | ares centialis pmterior —_J | 2.97 | 2.50 | 262] 3.9% | 405
4, : oral side LER CN EGS
2 ae intermediate part | 308 | 2.70 ol 21S ERGs AWG
= caudal side AON IFO NN QezRS|| ou Sat:
} Lower end of sulcus Rolandi aes a 2.53 }
8 Lobulus paracentralis 2.86 Pe aaiee lh A, Bll es |
| : hinder part 3.82 3.84 |
Ss sl ia len paeE SONG \\ 52: Estes
ie) fore part 2.60 3.45
& | Gyrus frontalis medius 340 | 240 | 2.70] 357 |
=: Gyrus frontalis Pars opercularig 2.50 | Bh 25
a inferior Pars Iriamgularis 2.98 3.00 tas 34 }
at Pars orbitalis 38610
| a Gyrus rectus 2.53 es Sa
| Frontal pole 2a Sia oral OTe
iS Gyrus parietalis superior 263% 2525) || SOS | siat0
=. ea extreme fore part ose 2.93 | 23:5
B% | Gyrus pariefalis [Gyrus angwlaris 243 (250 | 200 | a35 [317
| a inferior __|Gyrus supramarginalis| _ j =e eS
S Wi} Gyrus occipifalis | fore part 2.68 | 2.83
|: lateralis polar part 2.64 | 1.80 | 2.50 ee 2.34 | 2.33 |
ke Cringe PREP A) Pett) ETE red FOO 2.38 | 247
US ceean| [Gyrus lingualis
= Gyrus Temporalis Superior
i lin fissura Sylvii
) | do. external part : :
| S | Pole of femporal lobe Son eral
| - Gyrus Temporalis medius SUS | 352) 3.64
8 | Gyrus Temporalis mferior 268 | 225 | 347| 342 |
} a extreme hander part oS 2.97
Insuala 3.38 | 234 | 267 | 2.62 |
|
ectorhinal p
— posterior ventralis
— posterior dorsalis
retrosplemal part

Gemeral average

THE JOURNAL OF COMPARATIVE NEUROLOGY, VOL. 29, NO. 3

258 NAOKI SUGITA

thickness and staining with methyleneblue. Hammarberg claims
that after twenty-four hours in 95 per cent alcohol the brain
piece shrinks about 20.5 per cent in volume and the cortical
thickness diminishes by 0.1 to 0.2 mm., but that during the
subsequent procedures no significant size changes occur. Ac-
cording to his results, the gyri frontales have the thickest cortex
(about 3.0 mm.) and the lobus centralis or insula is the thinnest
among localities typical in cell lamination. This latter part as
measured by Donaldson shows the thickest cortex.

Campbell (’05) gave two series of determinations of the cortical
lamination of the human brain, after cell staining and after fiber
staining, represented by uniformly magnified illustrations of the
sections at the several localities. Making use of his iltustrations,
I obtained a series of cortical thicknesses at different localities
(table 8), reduced to the actual thickness on the slide, by divid-
ing the direct measurement on the illustration by the magnifi-
cation. His sections were taken from the material fixed in
Miiller’s or Orth’s fluid and imbedded in celloidin, cut at 25
micra, and stained with thionine. The general average thick-
ness thus obtained, the two series combined, is about 2.3 mm.

Brodmann (’08) also has measured the thickness of the cortex
on the human brains at forty-two different localities on sections
prepared by two different methods: one set was fixed in 4 per
cent formaldehyde, imbedded in paraffine, and stained by
Nissl’s method for cell study, and the other, fixed in Miiller’s
fluid, imbedded in celloidin, and stained by Weigert’s method
for the myelin sheaths. His results, which are the averages
from brains between seventeen and forty-five years in age, are
also tabulated in table 8 for a comparison. The general average
thickness given by Brodmann is about 3.09 mm.

Kaes (’07) also studied the growth in thickness of the human
cerebral cortex, measured at twelve different localities on the
hemisphere, using sections fixed in Miiller’s fluid and stained by
Weigert’s method. His results are remarkably high, giving 4.9
mm. on the general average. His method of measuring the cor-
tex is so arbitrary and peculiar, however, that his results are not
included in this table 8.

GROWTH OF THE CEREBRAL CORTEX 259

Bevan Lewis (79) has given as the average depth of the
human cortex the figures as high as 4.84 to 5.70 mm., a higher
value even than that of Kaes. His results for both the pig and
rabbit cortex were also very high, compared with those obtained
for other mammals. These results suggest that his technique,
which he claims gives the natural depth of the cortex, is likely
to produce very high values.

Reviewing the table (table 8), the values for the cortical thick-
ness given for a fixed part of the hemisphere by different authors
are by no means in accord; the results by Brodmann stand close
to the results by Donaldson, while those given by Campbell are
the lowest, less than one-half the values given by Lewis. These
differences are probably due mainly to differences in technique
and are not to be attributed to variations within the same species,
as the series of Donaldson (table 7) and my previous study
(Sugita, 717 a) both have shown that individual variations in
cortical thickness, obtained by the use of the same technique,
are low as compared with the variations for other body meas-

» urements.

On the average, the figures given by Donaldson and Brodmann
are fairly close and the former being somewhat lower, probably
because Donaldson took the average from the values at the
summit and at the sides of the gyrus, while Brodmann has meas-
ured the thickness at the summit only. The figures given by
Hammarberg and Campbell are low, probably owing to the
shrinkage of the material during preparation, as may be in-
ferred from the descriptions by the authors and from the studies
on the effects of fixing fluids by King (10) and by me (Sugita,
Aliza, 13° b, 718 'e)

Despite the apparent irregularity among the figures given for
the cortical thickness at different localities by the several au-
- thors, as shown in table 8, there are some general relations which
are fairly clear. If we examine table 9 in which has been en-
tered for each region the average thickness obtained by each
author, it may be safely said that this table (and also table 6
for the monkeys) shows that in man (and the primates) the
cerebral cortex differs normally according to locality. The

260

NAOKI

TABLE 9

SUGITA

Giving the average cortical thickness for several lobes and regions (with typical
cell lamination) of the cerebral hemisphere as given by different authors, and the
order of localities according to the cortical thickness, together with the difference
in thickness between the temporal and occipital regions.

R = regio Rolandica,

F = lobus frontalis, P = lobus parietalis, O = lobus occipitalis, T = lobus
temporalis. Based on table 8 in this paper
DONALDSON ee CAMPBELL CAMPBELL BRODMANN BRODMANN
EAS (791) (795) (705) (705) (’08) (708)
(Cell) (Cell) (Cell) (Fiber) (Cell) (Fiber)
mm. mm. mm. mm. mm. mm.
Regio Rolan-

GiCareer ers 2.92 2.34 2.48 Dy 2.74 2.93
Lobus frontalis 2EO2 2.92 2.46 D. 3.50 3.84
Lobus parieta-

las Aen vat cee: 2.43 2.44 Deals 3.17 3 le
Lobus occipita-

Listeners 2.59 2.09 2.16 1.96 2.47 2.54
Lobus tempora-

lise ease eee ce: Bi PAll 2.49 2.64 2.29 3.48 3508

Average...... 2.91 2.45 2.43 Drealiey 2.92 3.16
Order of the

above five

localities as

to the thick-

Meco ncdeuc TERO? || ETPRO. || TEPRO)| TREO} FLEEROo AREER
Difference be-

tween T and

OE RED IAS 0.62 0.40 0.48 0.33 1.01 LSPA

frontal and temporal regions have in all cases the thickest cortex
and the occipital region is the thinnest, while the position for
the cortex of the parietal and Rolandic regions is less fixed.
These thickness relations support the earlier statement made
by me for the rat cortex that the thickness diminishes from the
frontal to the occipital pole and from the dorsal to the ventral

aspect.

Brodmann (’08) has concluded from his careful study that
regional characteristics for the cortical thickness clearly exist.
‘Diese sind in allen normalen Gehirnen gesetzmissig und kon-

GROWTH OF THE CEREBRAL CORTEX 261

stant und bilden ein Hauptmerkmal der struktuellen Ver-
schiedenheiten der Gehirnoberfliche; jedes Strukturfeld besitzt
demnach eine bestimmte, mittlere Durchschnittsbreite, durch
welche es sich von den Nachbarfeldern auszeichnet.’? Onthe
other hand, local variations within a fixed area are small, while
individual differences between different brains for each locality
may run sometimes as high as 0.5 mm. or more.

VI. INCREASE IN CORTICAL THICKNESS DURING THE GROWTH OF
THE BRAIN OF THE MAN

From the point of view of the growth changes, there have been
only few studies on the human cerebral cortex ever published.’

Kaes (’05, ’07, 09), employing forty-one human brains (twenty-
eight males and thirteen females, normal and pathological com-
bined) of different ages and of different grades of intelligence,
studied the cerebral cortex for the purpose of following the
growth changes in it. He took his sections from twelve locaii-
ties in each hemisphere, stained the fibers by Weigert’s method
and measured the so-called cortical thickness from the ectal
border of the Meynert’s arcuate fibers (or fibrae propriae) to the
ectal border of the zonal layer. His conclusions on the growth

2 His (’04) has given the following values as the cortical thicknesses meas-
ured at different localities of the hemisphere of the human embryos in early
months, at different stages of intrauterine development—measured directly on
the sections imbedded in paraffine.

|
sonor | arconrus | AT LATERAL| “Slt'on | “warn or | ALMEDIAN |“ “opt”
SMBENOS | SESIANOM | THALAMUS | (Basar pant) | Gmrp Pann) | MEMISPHERE | cory
mm Ke B B H Be
weeks
1 50-55
2 65-75
4 150 130 110 60
5 360 160 120 50
6 800 300 130 90 40
7 1300 600 300 170 110 30
8 2000 900 400 200 130 30

262 NAOKI SUGITA

changes, briefly stated, are as follows: The average thickness of
the cortex diminishes rapidly from his first entry (three months
old, 5.58 mm.) to the twenty-third year (4.44 mm.) and is fol-
lowed by an increase up to the forty-fifth year (5.71 mm.), where
it is to be noted that the thickness attained is even greater
than that at birth. Then it undergoes a second thinning up
to the-old age (at ninety-seventh year, his last entry, 4.62 mm.).

These conclusions have been disputed by Donaldson (’08)
and by Brodmann (’09), and I am in agreement with these critics |
that Kaes’ results cannot be taken seriously.

Brodmann (’08), in his paper on the cortical measurement,
has noted only in a general way the average cortical thickness
at the lateral surface of the hemisphere at several ages, as shown
in table 10 (columns A and C). Nevertheless, these data can
be used for a comparison.

Donaldson (’08) has compared the albino rat with man in
respect to the growth of the brain and reached the conclusion
that man and the rat show growth curves for the brain which
are similar in form when the data are compared at equivalent
ages, and the condition of the brain of the rat at five days of
age is taken as like that of the human brain at birth. The rela-
tive growth rates of the rat and man are as 30 to 1 and the brain
of the child at one year corresponds to that of the albino rat at
seventeen days of age in its stage of development (Donaldson,
MS.). These statements are also confirmed by me for the cor-
tical thickness, as shown in table 10 (see below), and I have
already noted that the transitional cortical cell layers, which
are no longer to be seen in a new-born child, do not disappear
in the albino rat until after four days of age (Sugita, 717 a, p. 539).

From these relations, we conclude that the course of growth in
the thickness of the cerebral cortex in man and the albino rat
would probably be similar, if the brains were compared at the
equivalent ages. Such a comparison is attempted in table 10.
Here the increase in cortical thickness in man and in the albino
rat is compared, employing data given by Brodmann (’08) and
by me (Sugita, ’717a). From the age (column A) given by
Brodmann, the approximate brain weight (column B) was de-

GROWTH OF THE CEREBRAL CORTEX 263

TABLE 10
Giving a comparison in the course of increase in cortical thickness in man and in
the albino rat, according to data given by Brodmann (’08) and by Sugita (17 a).
Approximate brain weight in man and in the Albino for the equivalent ages were
assumed in round numbers according, respectively, to Vierordt (’90) and Don-
aldson (08)

A B (©: D E F G
MAN ALBINO RAT
| ; | Correspond-
Approximate ing cortical
Observed brain Thickness | thickness in
Approximate} thickness of |weight,atthe) Equivalent [of the cortex}human brain,
Age brain the cortex, | equivalent (observed) at ages when the
weight Brodmann | (observed) age given in adult values
(08) ages | Column E | inthe both
(Donaldson) are taken as
the standards
grams mm. grams days mm. mm,
Fetus
8-9 months 1.0-1.5 Birth 0.80 1.25
Birth 380 1.5-2.0 0.50 5 1.10 20s
1 year 950 2 .0-3.0 1.10 Ue Lets 256
Adult 1400 2.0-—4.0 1.90 Adult 1.90 3.00

termined according to Vierordt (’90) and then the final weight
(1400 grams) was entered corresponding to the adult brain weight
of the albino rat (1.9 grams). The other corresponding brain
weights of the Albino of the equivalent ages were entered also
according to Donaldson (’08) (column D). The cortical thick-
ness (column F) for the given brain weights of the Albino were
then entered according to my former determination (Sugita,
17 a). If the cortical thickness of the adult man be assumed
as 3.00 mm. (the mean value of 2.0 to 4.0 mm.) and the corre-
sponding thickness at each age be calculated on the basis of the
course of increase in cortical thickness in the Albino (given
in column F), the results given in column G—a mere inference,
to be sure—are fairly in accord with the figures presented by
Brodmann (column C).

In this connection, I had the opportunity, through the courtesy
of Dr. W. H. F. Addison, to prepare sections and examine the
cortical thickness at the dorsal part of the gyrus centralis ante-
rior (regio Rolandica) from a child thirteen months old (ma-
terial hardened in 4 per cent formaldehyde, imbedded in paraf-

264 NAOKI SUGITA

fine, and stained by Nissl’s method). The mean value of the
cortical thickness at the summit of the gyrus was 3.55 mm.,
or within 10 per cent the value obtained by Brodmann at the
same locality in the adult brain and on a section similarly pre-
pared and measured (table 8). So far, then, as this observation
goes, it helps to support my conclusion presented earlier that the
human cortex has attained nearly its full thickness at the age of
fifteen months (Sugita, 717 a).

VII. THE BRAIN WEIGHT, THE CORTICAL VOLUME, AND THE BODY
WEIGHT

Dhéré and Lapicque (’98) and DuBois (98 a, ’98 b), working
independently, found several important relations existing be-
tween the body and the brain weights in man and a number of
other vertebrates. Recently DuBois (713) has obtained results
which he has formulated in following terms:

1) In species of vertebrates that are alike in organization of
their nervous system and their shape, but differ in size, and also
in the two sexes of one and the same species, the quantity of the
brain increases; A) as the quotient of the superficial dimension
divided by the cube root of the longitudinal dimension. B) as
the product of the longitudinal dimension by the square of its
cube root.

2) In individuals of one and the same species and of the
same sex, but differing in size, the quantity of brain increases
as the square of the cube root of the longitudinal dimension of
the body.

So, briefly stated, 1) reads: in any species of vertebrates that
are equal in organization, in form of activity and in shape, the
weights of the respective brains are proportional to the 0.55 power

3 According to a study by Fuchs (’83), the child is born without any mye-
linated fibers in the cerebral cortex. Inthe laminazonalis the first myelination
appears at five months, in the lamina pyramidalis at the end of the first year,
while in the innermost layers we see some faintly stained fibers at two months.
The fibrae arcuate (association fibers) appear clearly at seven months. Later
the myelinated fibers increase in caliber and number as the age advances, and
at eight years they attain nearly the appearance which they have in the adult
cortex.

GROWTH OF THE CEREBRAL CORTEX 265

of the weights of bodies, and 2) the exponent of correlation within
the same species is for all vertebrates the 0.22 power.

These relations were based on a series of observations, and
this illuminating idea is now generally accepted as true.

The brain in general consists of the white and the gray matter,
and in higher animals the gray matter as represented by the
cerebral cortex occupies a relatively large part of the entire
cerebrum. This cortex is the seat of a complex series of physio-
logical nerve centers, and the possibility that it has definite
quantitative relations with the body as a whole is suggested by
the following statement made by Du Bois (’13):

If the quantity of brain does not increase proportionally to the
volume of the body, expressed by the weight, it might be that this is
really the case with regard to the superficial dimension, as being pro-
portional with the receptive sensitive surfaces and with the sections
of the muscles, thus measuring the passive and active relations of the
animal to the outer world, for which in this way the quantity of brain
can be a measure.

This statement, to be sure, is applied by DuBois to the weight
or volume of the entire brain, but if the volume of the cortex
stands in some definite relation to the volume of the entire
brain, then the cortical volume should be also in a definite rela-
tion to the size or weight of the body.

The cortica’ volume is determined by the area of surface of the
cerebral hemisphere and the thickness of the cortex. Theformer
factor is not easy to determine exactly, even in lissencephala,
while in higher animals the hemispheres have many convolutions
which increase still further the difficulty of this determination.
In lissencephala, the surface area of the hemispheres in two
brains, which are nearly similar in the form of cerebrum, are
approximately comparable with squares of the corresponding
diameters of the cerebra.

The cortical thickness, on the other hand, is not so hard to
determine exactly. The average thickness of the cortex in dif-
ferent mammals is given in table 11, quoted from various sources,
and, as seen from this table, it is not directly related to the size
or weight of the brain, since, as Marburg’s (’12) table shows, the

266 NAOKI SUGITA

cortical thickness in several primates ranges within rather nar-
row limits (2.3 mm. to 2.8 mm.), while the brain weight shows a
distinetly wider range (82 grams to 400 grams) (table 11). In
some cases indeed the smaller brain has a thicker cortex, even in
the same family (e.g., the smaller hapale has a thicker cortex than
the larger lemur). But in general we may conclude with Brod-
mann (’09) that, within one and the same order or family of
mammals, the large brain tends to have a larger average value
for the cortical thickness.

The relative cortical volume has been formerly computed by
me, employing the formula especially devised for this purpose,
in the albino and the Norway rat brains, so that the two forms
may be compared directly (Sugita, ’18b). The ratio of the
cortical volumes in the adult Albino (brain weight, 2.0 grams)
and the Norway (brain weight, 2.3 grams) is 1.31, as the rela-
tive cortical volumes are, respectively, 393 and 517 (Sugita,
18 b, table 15), and the ratio of the body surfaces in the two
animals amounts also to 1.30, when the body weights of the
adult albino and the Norway rats are taken as 300 grams and
450 grams, respectively. Moreover, the ratio of cortical volumes
in the two forms at any given age will prove to be almost equal
to the ratio of body surfaces of the two at the same age.*

As above tested, the body weight and the cortical volume of
the animals in the same family stand in a definite relation, at
least in this instance. But, as we cannot compute the volume
of the cortex in other mammals from the data given in table 11,
the relation can not be tested further.

4 For example, according to my former presentation (Sugita, “18 b), the com-
puted cortical volume in the Albino Group XV (brain weight, 1.54 grams) is
about 346 and that in the Norway Group N XVIII (brain weight, 1.83 grams)
is about 423, and according to another determination (Sugita, 718 a) these two
groups may be regarded nearly equal in age, as the Albino brain weight would
be about 18 per cent less than the Norway brain weight of the like age. The
ratio in cortical volume of the above two is 1.22. The body weight correspond-
ing to the brain weight of 1.54 grams in the albino rat is 64 grams and that cor-
responding to the brain weight of 1.83 grams in the Norway rat is 90 grams
(‘The Rat,’ Donaldson, °15). The ratio of the body surface in the above two,
therefore, is about 1.25, quite near to the ratio in cortical volume.

TABLE 11

Giving for several species of mammals the adult body weight and brain werght, the
average cortical thickness and the name of author from whom the data for the
cortical thickness or for the brain and body weights were cited, arranged in the

order of decreasing body weight within each family of mammals.

The abbre-

viations of the names of authors are as follows: B = Brodmann (’09), I = Isen-

schmid (11), L = Lewis. (’79),

M = Marburg, (12), S = Sugita (17a,

18 a, MS.)
Se
= & =e)
OF MAMMALIA NAME OF SRECIES ortee Ce, aie
| a
&
grams grams
Simia satyrus (orang-outang).| 7,350); 400.0 M
Prrmintes EHiylobatess.20% wil ocdyteys deel: 950} 130.0 M
6 Cynocephalus hamadryas...... 920} 142.0 M
Macacus rhesus (macaques)... 356} 82.0 M
Cercopithecus (long-tailedape)| 2,500) 85.0 B
Memunayanitist eer Seer rne 2,170} 28.7 M
Prosimiae Nel Bret 071 URN an renee ee eee eee 1,800} 23.0 B
Hep ale(@niarmoseti=ss.ss-6-4- 200 8.0 B
IWMitenocebustee ye. ee meen oe 62 1.9 B
geen Ovis musimon (sheep).........| 23,000] 100.0 L
* Felis domestica (cat)..........| 3,000} 30.0 L
Erinaceus europaeus (hedge-
Insectivora IsKOye RAT atl On a sts eee 700 SPO} a les By
Talpa europaea (mole)........ 75 esi} HAO) B
Lepus cuniculus (rabbit)...... 2°200)|8) 20k0 eee B
Cavia cobaya (guinea-pig)..... 600 4.5} 1.9 8
Mus norvegicus (Norway rat). 450 2 5\) ae2eel Ss
Rodentia Mus norvy. albinus (albino rat) 300 BAD — 1.9) S
Spermophilus citillus (ground-
SQUIETED acas eee eres whe 200 2 Diese B
Mus musculus (mouse)........ 20 0.44 +O I
Pteropus edwardsii (vampire i
Chiroptera arte ec es eae ahi ony hain: 375 7.0 B
Vespertilio murinus (bat)..... 23 0.3 4 B
Macropus giganteus (kanga-
Marsupialia FOO) Pict eRe Reine: 5,000} 25.0 B
| Didelphys..................... 1,100 5.8) B

‘The body and brain weights of some animals were not given by the author

who has given the cortical thickness.

were taken from the list given by Weber (’96).

2 According to Lewis (’79), the values given here without brackets were taken
from Meynert and show the value measured on the slide and the values given
within brackets were obtained by his own observation and represent the natural
depth of the cortex.

267

In such cases the body and brain weights

268 NAOKI SUGITA

VIII. SIZE AND GROWTH CHANGES IN SOME NERVE CELLS IN THE
MAMMALIAN BRAIN

Albino rat. The results obtained by me regarding the size
and the growth changes of the pyramidal cells and of the ganglion
cells in the cerebral cortex of the albino rat were summarized in
a previous study (Sugita, 718 c¢). Four of the conclusions are
here quoted:

1. The full size of the pyramids in the lamina pyramidalis is
cell body 21 x 27 uw and nucleus 18 x 20 uw in the fresh condition
(on the slide, respectively, 16x 21 yu and 14x15uy). The full
size of the ganglion cells in the lamina ganglionaris is cell body
27 x 37 w and nucleus 23 x 25 uw in the fresh condition (on the
slide, respectively, 21 x 29 u and 18x 19 yn).

2. The cell body and the nucleus of the pyramids attain their
maximum size at twenty to thirty days in age. Up to ten days
they still retain their fetal morphology. After having passed
the maximum size at about twenty-five days, they diminish
somewhat in size, but the internal structure differentiates as the
age advances.

3. The cell body and the nucleus of the ganglion cells attain
nearly their maximum size at ten days, when they remain still
in fetal form. After this stage, the size of the cell body still in-
creases slowly but steadily as the age advances, while the nucleus
remains nearly unchanged in size throughout life.

4. Taking a general view of the data already presented in this
series of studies, it is very interesting to observe that the thick-
ness of the cortex, the total number of the cortical nerve cells,
and the size of the cortical cells, all attain nearly their full values
at the same age of twenty days; that is, at the weaning time of
the albino rat.

For comparison with these results on the cells of the cerebral
cortex, there are some observations by Addison (711) on the post-
natal growth of the Purkinje cells in the cerebellar cortex of the
albino rat. His material was also obtained from the rat colony
at The Wistar Institute and the cerebellum was fixed in Ohl-
macher’s solution, imbedded in paraffine, and stained with

GROWTH OF THE CEREBRAL CORTEX 269

carbol-thionine and acid fuchsin. <A part of his results on the
Purkinje cells is here quoted:

The Purkinje cells are easily distinguishable at birth along the
inner boundary of the molecular layer by their relatively large size and
lightly staining nucleus. These cells measure 12x 7m and nuclei
8x 6.3 u. During the first week, there is great increase in size of
both nucleus and cytoplasm. The main bulk of the latter is at the
ectal pole and from it several fine processes radiate into the molecular
layer. At eight days the cells measure 18x 12m and nuclei 10x 8 u
to 12x9u. At-eight to ten days there is definite change in form by
the elongation of the cytoplasm of the ectal pole to form the main
dendrite, the previously existing fine processes becoming its branches.
At the same time all the dendries become arranged in one plane, and
this plane is parallel to sections directed across the folia. Nissl gran-
ules appear in the cytoplasm at eight to ten days. The arrangement
of Purkinje cells changes with the increase in the surface area of the
cortex. At birth they are arranged in two to three irregular rows;
at three days in one to two irregular rows, and at five days in one
continuous row. As growth of the cortex continues, the space inter-
vening between the Purkinje cells becomes greater. Some nuclei reach
their maximum size of 12x 9 u at eight days, while the cell bodies
usually continue to grow, reaching a maximum size of 24x 19m at
twenty days. The dendrites reach the outer limiting membrane
when all the outer granule cel’s have migrated (twenty-one to twenty-
five days), and continue to develop new branches until a much later
period as is shown by a comparison of cells from a 31 day with cells
from a 110—day cerebellum.

From this it is plain that the Purkinje cells (cell bodies) of the
albino rat cerebellum have also reached full size at about the
weaning time (twenty days of age).

From the foregoing, we see that the functional cortical cells
both in the cerebrum and in the cerebellum reach their full size
at an early age—before the weaning time—and though they
continue to mature after that they change only slightly in size,
sometimes even diminishing. Thus the cortical nerve elements
are all precocious in their growth, which is nearly complete
when the young become independent of the mother and their
education begins. Addison (’11) has stated also that the de-
velopment of motor control in the young rat is closely correlated
with the completion of the cerebellum and the rat attains its
full motor control when the cerebellum has attained structural

270 NAOKI SUGITA

maturity at twenty-one to twenty-five days of age. At that age
the cells are nearly full size. We may conclude, therefore, at
least regarding some of the nerve cells, that the beginning of
functional education of the cells at twenty days is preceded by
the attainment of nearly full size, and after this period there is
very little change in size, though the internal structures mature
as the age advances.

Mouse. <A study in this field was made by Stefanowska (’98)
on the cortical cells of the mouse. She stained the cells by the
method of silver impregnation and studied mainly the develop-
ment of the cell attachments. Her conclusions may be condensed
as follows:

1. In the new-born mouse most of the cortical nerve cells have a
simple morphology. 2. The cells are usually arranged in chains, dis-
posed perpendicularly to the surface of the cortex. 3. Besides these,
there are some groups of cells more advanced in developmen. and
having many dendrites, and cells which have the adult form having
many, long, ramified dendrites. 4. The different parts of the cortex
do not attain the same degree of development at the same time. Some
cell groups are more precocious. 5. In the lamina multiformis and
in the lamina ganglionaris, we find always the most advanced cells
in large numbers. 6. In the lamina pyramidalis the development of
the cells is very slow. On the ectal surface, near the pia mater, many
cells not at all differentiated are often found. 7. At one day after
birth, the dendrites of cortical cells are covered with varicosities. The
axis-cylinders have also many nodal swellings. 8. As the neurons
develop, the varicosities become more and more rare. At fifteen
days, varicosities are no longer seen on the dendrites and the neurons
at this age have completed their development. 9. The appearance
of the piriform appendices on the dendrites is somewhat delayed.
At ten days all pyramidal cells show these appendices. These latter
are the constant feature of the neuron, while the varicosities are only
a temporary formation. The piriform appendices may be the terminal
apparatus of the dendrites. 10. The piriform appendices are the
last element which appears on the cortical cells during growth. This
fact seems to suggest the high importance of these appendices for this
nerve function.

As seen from the foregoing, the morphological completeness in
respect of the dendrites and the axis-cylinder of the cortical cells
is attained at fifteen days or at the weaning time of the mouse
also.

GROWTH OF THE CEREBRAL CORTEX Birla

TABLE 12

Giving for man and other mammals the size of the largest ganglion cells in the lam-
ina ganglionaris of the cerebral cortex as presented by different authors. Data
are arranged according to the order of the average diameters

MAXIMUM SIZE
REPORTED IN MICRA
NAME OF SPECIES Average Author
Dinear diameter or
diameters pcre ry
product
Homo sapiens, (man) i. ..4..o0.A2te ae aaeese es =| COXK120 85 Betz
EO OS aplens) (man): ease eae eee eae OO LO, 83 Lewis
Homoisapiens: (mam)h.) esse see once 53x 106 WS Brodmann
OMOPs a plenish (main) erent eileen eee 40X 80 iC Hammarberg
BSNS. (Oni As eas oS accraeeh. Stee ee 60133 90 Brodmann
Helistivorisa (irene oe een Lee seer 60> 100 78 Brodmann
Cercoleptus caudivolvulus (kinkajou)........ 50110 74 Brodmann
Winsuisisymacuss (bea) ie annmerrccie caters coer 53 X 100 73 Brodmann
Ttinc liste) (otovsll Xow), be oo Sod bo nabs Oe uoatinccoee 44x 80 59 Brodmann
Helishdomestica (cat)... ..02.:.5.-) 4 Le ee Ne 32 106 58 Lewis
Cercopithecus mona (African monkey).......| 40 72 54 Brodmann
Blephase(clephant) airs eae ceeerrne BoD< 60 46 Brodmann
IGE TINIE Ean Ooh teeta acct ook ysrie pa iteee Ne leks 30 70 46 Brodmann
Mus norvegicus (Norway rat)................ 33x 48 40 Sugita
Ovigumusimon (SHEED). 26. 6 cheb ee ae. 2s 23 65 39 Lewis
SULTS) (Up) ee a Re ho Cn aR A 27x 48 36 Lewis
Mus norvegicus albinus (albino rat)......... 30 42 36 Sugita
Hepusscunieuluss(@abbit)iasceee sce saeee eee 18x 60 33 Lewis
Gepus cuniculus (rabbit). ..:0.0.5..-8-.-..----| 18x 40 27 Brodmann
Pteropus edwardsii (vampire bat)............ 16X 36 24 Brodmann
Miisimirsculitise mouse) sees sssae- sale eee are aloe 2O 19 Isenschmid

There are no other systematic investigations on the postnatal
development of the cortical nerve cells in mammals, although
there are some studies on the growth of nerve cells in the fetus,
among which the researches by His (’04) (see footnote 2),
Koelliker (96), and Vignal (’89) are the most important.

Table 12 was compiled by me in order to compare the size of
the largest ganglion cells in the lamina ganglionaris (the fifth
layer of Brodmann) of the cerebral cortex of man and some
other mammals. The tabulated data were taken from Brod-
mann (’09), Lewis (’79, ’82), Hammarberg (95), and others.

ihe NAOKI SUGITA

The results obtained by me (Sugita, 718 c) in the albino and the
Norway rats have been also entered.

IX. THE SIZE OF THE LARGEST CORTICAL CELLS IN MAN AND
SOME OTHER MAMMALS

From table 12 we can draw only very general conclusions as to
the significance of the size of the largest cortical cells. The giant
Betz cells even in man vary rather widely in size according to the
different authors, probably owing largely to the different tech-
nical methods used, as has been pointed out repeatedly in the
course of this paper.

From time to time attempts have been made to formulate a
general interpretation of the size of the Betz cells and of the
nerve cells in general. From the examination of table 12, it is
seen that the values for the mean diameters do not, except in
the very most general way, follow the size of the animal, but
that the Felidae, even the cat, stand high in the series.

We are not able to contribute any general explanation for the
size of these cells, although it may not be out of place to repeat
that in the Norway rat with the heavier brain these cells are
larger than in the albino rat with the lighter brain (Sugita,
18 ¢), and so will merely call attention to the various authors
who have had something to say in the matter: Lewis (’79),
Hughlings Jackson (’90), Schwalbe (’81), Barratt (01), Dunn
(00, ’02), Herrick (’02), Donaldson (03), Campbell (’05),
Boughton (’06), Johnston (708), and Kidd (15).

X. SUMMARY

1. In the present paper I have attempted to compare my con-
clusions regarding the development of the cortical elements in the
brains of the albino and the Norway rats with the corresponding
changes in other mammals. The data used for these comparisons
were taken from various sources, but the comparisons are in
many instances hampered by differences in technique or the
lack of essential information.

2. The relations of the cortical thickness at different locali-

GROWTH OF THE CEREBRAL CORTEX 273

ties in the cerebrum are quite the same in the mouse and rabbit
as in the rat. The development of the cortical thickness has
proved to be similar in the mouse and guinea-pig: it attains
nearly its full value at the weaning time of the animal.

3. The statement that the cortical thickness diminishes from
the frontal to the occipital pole and from the dorsal to the ven-
tral aspect probably holds true throughout mammals, including
man.

4. The results given by different authors for the cortical
thickness of human brain (averages or for each locality) are by no
means in accord. Even for the same locality there are wide
deviations. The best data indicate that the average cortical
thickness of the adult human brain is about 3 mm.

5. The mode of increase in cortical thickness in man according
to age appears to be similar to that in the albino rat, if the brains
are compared at equivalent ages. The developmental stage of
the brain of a new-born child corresponds to that of an albino
rat of five days of age, and throughout the postnatal life the rela-
tive growth rate of the rat and man areas 30 to 1. The span of
life 30 for man corresponds to 1 for the rat and the equivalent
ages are represented by like fractions of the span of life. The
human cortex probably attains nearly its full thickness at fifteen
months, equivalent to twenty days of rat age.

6. The relative cortical volumes of the albino and the Norway
rat brains, computed formerly by me (Sugita, ’18 b), appear to be
proportional to the surface areas of the entire bodies at the like
age. This relation may be generally applicable within a given
order of mammalia. The cortical thickness or the brain weight
is in general only loosely correlated with the body weight or size
of the animal.

7. The cortical nerve cells in the cerebrum and in the cere-
bellum of the albino rat are precocious in their growth, attaining
almost the full size at twenty days, the weaning time. The
maturation of the intracellular structures probably continues
after the size is apparently completed. This process is shown
also in the mouse.

8. The size of the Betz giant cells in the adult human cortex

THE JOURNAL OF COMPARATIVE NEUROLOGY, VOL. 29, No. 3

274 NAOKI SUGITA

(found in the gyrus centralis anterior) is reported differently by
different authors. The mean value is about 75 micra in average
diameter.

9. The size of the cortical cells, especially the Betz motor
ganglion cells, of adult animals has no clear relationship to
brain size or body size. These cells are notably large in the
Felidae.

10. As a general conclusion to this series of studies the follow-
ing statement may be made:

The morphological organization of the cerebral cortex is gener-
ally precocious. The size of individual cortical nerve cells, the
total number of cortical cells, and the thickness of the cortex,
all attain nearly their full values at the same time and very
early in life (corresponding to the weaning time in some rodents),
after which the maturation of internal structures of the cell body
and the nucleus continues. The brain weight and the cortical
volume continue to increase even after this stage throughout the
postnatal life, though not so rapidly as during the early period.
This later growth is due principally to the development of the
cell attachments, intercellular tissues (neuroglia tissue and blood-
vessels), the ingrowth of axons into the cortex and their mye-
lination, which together separate the cells from each other, and
cause an increase in cortical volume. The cortical volume is
primarily dependent on the size of individual cortical cells and
their total number and it appears in animals belonging to a
given zoological order to have a definite relationship to the
size (or area of surface) of the body of the animal.

GROWTH OF THE CEREBRAL CORTEX 215

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GROWTH OF THE CEREBRAL CORTEX 277

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AUTHORS’S ABSTRACT OF THIS PAPER ISSUED
BY THE BIBLIOGRAPHIC SERVICE, APRIL 20

THE PERIPHERAL TERMINATIONS OF THE NERVUS
LATERALIS IN SQUALUS SUCKLII

SYDNEY E. JOHNSON

From the Anatomical Laboratory of Northwestern University Medical School
TEN FIGURES

The observations set forth below supplement the writer’s
previous paper on the structure and development of the lateral
canal sense organs of Squalus acanthias and Mustelus canis.?
In the investigation referred to the peripheral terminations of the
lateral nerve were demonstrated in Mustelus canis, but not in
Squalus acanthias, as fresh specimens of the latter species were
unobtainable at that time. Last summer (July, 717), while at the
Puget Sound Biological Station, I secured a number of living
specimens of the Pacific coast’ dogfish, Squalus sucklii, which
appears to be practically identical to the Atlantic form, Squalus
acanthias. The histological structure of the lateral sense organs
of these specimens was examined and the peripheral terminations
of the lateral nerve were demonstrated by the pyridine silver
method and also with methylene blue. These observations
supply the omission which was necessitated in the paper referred
to above.

The papers which deal specifically with the peripheral termina-
tions of the nervus lateralis and which are of more than historic
value are those of Retzius 792, v. Lenhossék ’92, Bunker ’97,
Heilig 12, and Pfiiller °14. They are discussed briefly in the
writer’s previous paper and need no further comment except to
say that most attempts to stain the peripheral terminations of
the lateral nerve have heretofore yielded rather meagre results.

1 Contribution No. 60.
2 Jour. Comp. Neur., Vol. 28, No. 1.

279

280 SYDNEY E. JOHNSON

In comparing the lateral sensory canals of Mustelus canis
and Squalis sucklii there are a number of differences to be noted.
Perhaps the most striking is the difference in calibre of the sensory
tubes. The sensory tubes (or canals) of Squalus are much
smaller than would be found in a Mustelus specimen of the same
size. The column of sensory epithelium is_ proportionately
narrower in Squalus. A slight but apparently constant differ-
ence in the course of the lateral canals of the two species is seen
in the slight elevation of the canal above the anal fin in Mustelus.
There are other differences in the distribution of the canals, but
they are less striking and have not been carefully examined.
The lateral canals of both species lie chiefly in the dermis and
their tubules pass directly ventrad for a short distance before
making a sharp bend laterally to open on the surface of the integ-
ument. The surface tubules correspond in number with the
ramuli of the lateral nerve and there are approximately five
tubules for every four segments of the vertebral column.

The lateral nerve lies at a considerable depth from the sensory
canal, especially in the anterior region, and its ramuli pass
obliquely to the basilar membrane of the sensory column, where
their fibers diverge caudad and cephalad to form a continuous
longitudinal fiber zone just outside of the basilar membrane.
This fiber zone differs from that described for Mustelus only in the
fact that it contains a considerably smaller number of nerve
fibers.

The sensory epithelium of Squalus sucklic differs considerably
from that of Mustelus canis. It is much less extensive and the
sensory cells are aggregated in smaller groups. This can be
seen readily in transverse and longitudinal sections. In the
former one to three sensory cells can ordinarily be seen in the
cell clusters (fig. 1), and in the latter, usually three to six
(figs. 2 and 10). The groups of sensory cells are somewhat more
widely separated from each other than they are in Mustelus,
and the sensory column appears to show a stronger tendency
towards segmentation. This apparent segmentation of the
column of sensory epithelium, however, bears no relationship
to the normal body segments for there are usually more than ten

LATERAL SENSE ORGANS OF SQUALUS SUCKLII 281

clusters of these cells between adjacent surface tubules, and the
tubules, in turn, are more numerous than the segments of the
vertebral column. Nor is there any marked regularity in the
number and size of the individual clusters of sensory cells.
While the sensory column is thus essentially continuous through-
out the entire length of the sensory canal it shows considerable

Fig. 1 Transverse section of the entire sensory canal of a Squalus sucklii
garter. Camera lucida sketch. Iron haem. tech. X 432, 2 off. Can., canal
wall; Fb.Zn., longitudinal fiber zone; Sn.Cl., secondary sensory cell; Sn.Col., sen-
sory column; Spn., spindle cells.

variation in thickness. It becomes gradually thinner posteriorly
and, as in Mustelus, it is usually thinner between adjacent
ramuli of the lateral nerve. The base of the column of sensory
cells is limited by a continuous basilar membrane.

The same types of cells can be distinguished in the lateral
sensory epithelium of Squalus sucklii as were found in the sensory

282 SYDNEY E. JOHNSON

column of Mustelus and of Squalus acanthias. The hair cells or
secondary sense cells are large, pear-shaped, and have centrally
placed nuclei. In many specimens hair-like processes could be
seen at their distal ends, but whether one or more for each cell
has not been determined. The relative length of the cells is
usually one-half to two-thirds the thickness of the sensory

Fig.2 Longitudinal section 0 the lateral sensory column (Sn. Col.) of Squalus
suckhi (adult). The sensory epithelium was drawn with the aid of a camera
lucida {rom an iron haematoxylin preparation, and the nerve fibers were put in
free hand from pyridine silver sections. The outlines of the canal wall (Can.)
and the surface tubule (7'ub.) are not drawn to scale but are greatly reduced in
order to conserve space. For correct proportions, see figure 1. Sensory column,
x 650, 4 off. Fbr., terminal fibrillae; Fb.Zn., longitudinal fiber zone; Grp.,
one group of secondary sensory cells (hair cells).

column. Spindle-shaped cells, basilar cells, and columnar cells
constitute the supporting elements (see figs. 1, 2, 3 and 10).
The rest of the canal wall is formed by a double layer of epi-
thelial cells, both layers of which are continuous with the walls
of the surface tubules and also with the columnar and stratified
layers of the epidermis.

LATERAL SENSE ORGANS OF SQUALUS SUCKLII 283

The peripheral terminations of the lateral nerve. On reaching
the base of the sensory column the fibers of the lateral ramuli
diverge caudad and cephalad in the subbasilar fiber zone. This
fiber zone is shown in longitudinal section in figures 2 and 4, and
in transverse section in figures 1 and 3. The majority of the
fibers are medullated but a few non-medullated fibers can be
found. These can be traced back through the ramulus to the
lateral nerve, which indicates that they are not simply non-
medullated branches of the large medullated fibers.

Two zones of distribution or branching of the nerve fibers
appear well marked. Primary distribution takes place from the
longitudinal fiber zone and the branching is almost entirely
subbasilar (figs. 4 and 10), while a secondary zone of distribution
or branching is located roughly between the limits marked by the
-nuclei of the basilar cells and the proximal ends of the hair cells.
It is from this zone that the fine fibrillae arise which pass out
freely between the hair cells.

The primary branches are large and coarse as a rule (fig. 7),
although many fine branches arise from this zone also (fig. 4).
Branching of the fibers appears frequently to be dichotomous but
not uncommonly three or more branches arise at the same level.
This statement holds for both zones of distribution. Enlarge-
ments of considerable size are commonly seen at the level of
branching of the nerve fibers (fig. 9), but it seems likely that the
majority of these extra large ‘‘varicosities’”’ are caused by an
over-deposit of silver at the points of branching. One or more
fibers may rise from the subbasilar fiber zone to supply a single
cluster of hair cells, and occasionally the fibrillae of a given fiber
ramify in adjacent groups of hair cells (fig. 10). The medullary
sheath is usually lost just outside of the basilar membrane.

The primary branches rise to a considerable height in the
sensory epithelium—usually beyond the nuclei of the basal cells—
where they form a rather rich plexiform network (figs. 4, 7, and
10). This network forms the secondary zone of distribution and
it is from it that the ultimate distribution of fibrillae to the hair
cells takes place. While this secondary zone of distribution is
present in the lateral sensory epithelium of Mustelus canis, it is

4

NM.F b.

LATERAL SENSE ORGANS OF SQUALUS SUCKLII 285

not as uniformly developed and is much less conspicuous than it
is in Squalus suckli.

The fine fibrillae which arise from the secondary zone of dis-
tribution rise to various levels in the sensory epithelium. In
many instances they can be traced to within a short distance of
the outside limiting membrane (figs. 8 and 9). Varicosities of
various sizes and shapes appear on the fibrillae at practically all
levels and not infrequently at their distal extremities. In many
cases the fibrillae appear to surround the bases of the hair cells
(figs. 8 and 9), and in others, to pass out freely and separately
between the hair cells.

The observations set forth above corroborate the results
obtained on Mustelus canis. Only minor differences exist in the
structure and innervation of the sensory epithelium of the two
species. In Squalus sucklii the sensory epithelium is less ex-
tensive, there is a stronger suggestion of segmentation, and in
nerve supply there is a more definite and conspicuously second-
ary zone of distribution.

A number of features which stand out in the embryonic and
adult structure of the lateral canal system of Squalus and Muste-
lus appear to me to reflect doubt on the theory that this sytem of
sense organs has a phylogenetic relationship with the segmental
sense organs of certain invertebrates and that the system itself
is segmental in the sense suggested by John Beard? and W. H.
Gaskell.4 The evidence, in part, against such a view may be

Fig. 3 Transverse section of the sensory column, showing the peculiar condi-
tion of two groups of hair cells (Grp.) existing side by side. Camera sketch,
xX 650. Nf., nerve fibers of the subbasilar fiber zone.

Fig. Longitudinal section of the lateral sensory column and the subbasilar
fiber zone (Fb.Zn.). The secondary zone of distribution (Snd.Zn.) is also shown.
Camera sketch. Pyridine silver tech. X 650, 3 off. Grp., group or cluster of
hair cells; VN.M.Fb., non-medullated nerve fibers.

Fig. 5 Transverse section of the sensory column showing large enol and
fibrillae diverging at a large varicosity. Pyridine silver tech. X 1525, 2 off.

Fig. 6 Transverse section of sensory epithelium showing long, fine sens: and
varicosities. Pyridine silver. > 650, + off.

3 See Zool. Anz., Bd. 7, 1884, p. 125 et seq., and also Bd. 8.
4 The Origin of Vertebrates, 1908.

E. JOHNSON

SYDNEY

286

LATERAL SENSE ORGANS OF, SQUALUS SUCKLII 287
summarized briefly. The lateral sense organs do not develop
in situ from successive or segmental patches of ectoderm along
the side of the body, but each lateral sensory column arises from a
thickened area of ectoderm located on the side of the head; this
invades the posterior segments of the body not as a segmental
structure, but in the form of a continuous column of epithelial
cells. The grouping of the sensory cells in small clusters occurs
comparatively late inthe development of the embryo. It has
been pointed out that these groups, when they do appear, are not
segmental in the sense of the term as here employed. It is only
in a degenerating or breaking down condition of the sensory
ridges that isolated groups (pit-organs) of hair cells are found
(e.g., dorsal series of sense organs in Squalus acanthias). These
so called pit-organs show no relationship to the body segments
either in their number or in their innervation. Further, their
early development is identical with that of the lateral sense
organs, the separated organs simply representing parts of what
was earlier a continuous ridge of epithelium. So much for the
developmental aspect.

The opinion has already been expressed that the slight tendency
towards segmentation as seen in the lateral sensory column of the
adult is probably of no significance as an argument for the seg-
mentation theory. This is one of the anatomical features, how-
ever, which might be considered as pointing in that direction.
Another one is seen in the innervation of the sensory epithelium
by separate and successive ramuli (of the lateral nerve) which cor-
respond in number and level with the surface tubules. The first
condition named loses segmental significance when one remembers

Fig. 7 Longitudinal section of lateral sensory epithelium showing the exten-
sive branching of a single large nerve fiber. Pyridine silver. 1525, 2 off.

Fig. 8 Longitudinal section of a group of hair cells, showing various relations
of the terminal fibrillae. Pyridine silver. X 650, } off. Var., varicosity.

Fig. 9 Section showing several slender fibrillae diverging from a large vari-
cosity (Var.). Pyridine silver. X 650, 4 off.

Fig. 10 Longitudinal section of the lateral sensory column, showing two
groups of hair cells (Grp.), and a network of fibers arising from the subbasilar
fiber zone (Fb.Zn.). Pyridine silver. XX 650, 4 off. B.Cl., basal cell; N.M.Fb.,
non-medullated nerve fibers.

288 SYDNEY E. JOHNSON

that there are from fifteen to twenty clusters of hair cells for
every vertebral segment. Evidence based on the arrangement
of the lateral ramuli and the surface tubules is unsatisfactory
partly for the same reason and partly for other reasons. As
shown above, the lateral ramuli and the surface tubules are
considerably nore numerous than the vertebral segments and a
constant ratio between the number of vertebrae and ramuli of the
lateral nerve is wanting. Furthermore, these ramuli are merely
the branches of distribution of a cranial nerve which differs from
other cranial nerves only because of the fact that it supplies this
remarkable type of sense organ and extends from the head to the
caudal fin. In this connection it must be remembered that the
fibers of the ramuli diverge at the base of the sensory epithelium .
to form a continuous fiber zone from which the ultimate dis-
tribution takes place.

Further difficulty is met in attempting to relate the numerous
organs of the head canals and of the cross-commissures to a cor-
responding number of ancestral segments.

In view of these considerations it seems improbable to me that
the organs of the sensory canals have a phylogenetic history which
would relate them either to the segmental sense organs of certain
invertebrates, as claimed by Beard, Gaskell, and others, or to
the posterior (body) segments of primitive vertebrates. To
assume that the lateral sense organs have had such a past history
involves the necessity of explaining why the innervation of the
body organs should change from a segmental spinal nerve supply
to a cranial nerve supply, and also, why the organs do not arise
in situ on each segment of the body rather than from cephalic
ectoderm which invades the posterior segments and carries with
it its own nerve supply, probably from a corresponding primitive
cephalic segment. It appears to me more likely that if the lateral
sensory apparatus is segmental it is so only in relation to a limited
number of cephalic segments. The several lines of organs, then,
would represent simply an invasion or extension of a primitive
cephalic sensory apparatus into other segments of the body.

Clearly the evidence at hand is not sufficient to warrant
dogmatic statements or conclusions. The need is emphasized

LATERAL SENSE ORGANS OF SQUALUS SUCKLII 289

for further histological and embryological work, to be conducted
on a comparative basis. ‘The amphibia, especially, need further
investigation along this line.

LITERATURE CITED

Bunker, F. 8. 1897 On the structure of the sensory organs of the lateral line
of Ameiurus nebulosus. Anat. Anz., Bd. 13.

Heriic, Kart 1912 Zur Kenntnis der Seitenorgane von Fischen und Amphibien.
Arch. fiir Anat. und Physiol.

LenuosseK, M. v. 1892 Der feinere Bau und die Nervenendigungen der
Geschmacksknospen. Anat. Anz., Bd. 8.

PFULLER, ALBERT 1914 Beitrige zur Kenntnis der Seitensinnesorgane und
Kkopfanatomie der Macruriden. Jen. Zeitschr., Bd. 52.

Retzius, G. 1892 Ueber die peripherische Endigungsweise des Gehérnerven.
Biol. Unters., Bd. 1.

THE JOURNAL OF COMPARATIVE NEUROLOGY, VOL. 29, NO. 3

AUTHOR’S ABSTRACT OF THIS PAPER ISSUED
BY THE BIBLIOGRAPHIC SERVICE, JUNE 1

ON THE DEVELOPMENT OF THE NERVE ENDORGANS
IN THE EAR OF TRIGONOCEPHALUS JAPONICUS

TOKUYASU KUDO
Anatomical Institute, Medical High School, Niigata, Echigo, Japan

ONE PLATE

The endorgans of the auditory nerve in reptiles have been
investigated morphologically with considerable thoroughness.
Many authors have interested themselves particularly in the
macula neglecta (described for the Amphibia by Deiters in 1862
and given the name now in common use by Retzius) and this
endorgan has been studied in various vertebrates, especially in
the fishes, the Sauropsida, the mammals and even in man.

Relatively few embryological investigations, however, have
been published on this subject. Concerning the genesis of the
macula neglecta, Retzius and Alexander concluded that this
organ originates from the crista acustica posterior, the former
basing his opinion on its comparative anatomy and the latter on
observations of its innervation. In Hertwig’s Handbuch Krause
briefly states that a small region of common neuroepithelium
differentiates upon the separation of the saccular from the
utricular portions. Fleissig, who, working on reptiles (Gecko),
was the first to investigate extensively the development of the
macula neglecta, disagrees with both of these statements and is of
the opinion that the organ arises from the macula sacculi. The
same conclusion is reached by Okagima in the case of Hynobius;
but this author remarks that because in the Amphibia the macula
neglecta lies within the sacculus, its origin in these forms is easier
to determine than in the reptiles, where the macula is found in the
utriculus. Corroboration of this view, according to which the
macula neglecta arises from the neuroepithelium of the pars in-
ferior, is found in Okagima’s study of the salmon embryo and
Wenig’s recent work on Pelobates fuscus.

291

292 TOKUYASU KUDO

This simple interpretation of the genesis of the macula neglecta
has been considerably complicated by the studies of P. and F.
Sarasin, who claim to have found a second endorgan in the
Caecillidae, for they distinguish two different maculae, one of
which lies in a small evagination of the sacculus (macula neglecta
of Retzius), the other in the floor of the utriculus (macula neglecta
fundi utriculi). The existence of the latter was, however, denied
by Retzius, in which opinion he is joined by Ayers. Retzius
states: ‘Hs geht nicht hervor, dass die am Boden des Utriculus
der Caeciliiden gefundene Nervendstelle einer neu entdeckten
Nervendstelle entspricht. Denn gerade am Boden des Utriculus
liegt die von mir bei vielen Fischen, Reptilien und Vogeln ent-
deckte Nervendstelle, Welche von mir schon laingst ‘Macula
neglecta’ genannt wurde. Hsist deshalb ganz unrichtig, wenn die
Herren Sarasin die von ihnen bei Ichthyophis am Boden des
Utriculis beschriebene Nervendstelle als von ihnen neu entdeckt
bet achten und sie als eine ‘Macula fundi utriculi’ auffiihren.
Die echte ‘Macula neglecta’ liegt am Boden des Utriculus oder
Offnung des Canalis,utriculo-saccularis, oder auch-nach meiner
Ansicht—bei den niederen Amphibien in der eigentiimlichen
Ausstiilpung dieses Canalis, welches ich ‘Pars neglecta’ gen-
nannt habe, bei den héheren aber in einer von ihm abgetrennten
Ausstiilpung der Sacculuswand.” He adds that it would be
interesting to know whether both of the endorgans as described
by P. and F. Sarasin really do occur, in view of the fact that in all
Amphibia that have been thoroughly studied a single macula
neglecta occurs. Ayers contends that the new endorgan of the
Sarasins is probably none other than the macula neglecta of
Retzius. But Fleissig, from his study on the development of the
labyrinth in Gecko, was able to demonstrate a transitional con-
dition between the two described above. According to this
author the macula neglecta of Retzius is to be regarded as a
persisting organ in the sinus inferior, while only traces of the
macula neglecta of the Sarasins occurs in adult individuals; and
these traces may Well be regarded as vestiges of Sarasin’s macula,
which is present as a developing organ only at a certain stage.

NERVE ENDORGANS IN THE EAR 293

To this much mooted and interesting question, then, I wish to
contribute the modest results which I have been able to obtain
from my study of Trigonocephalus japonicus.

The viperid embryos which were placed at my disposal comprise
more than 27 stages! (Suzuki-Okajimas series), of which I have
employed four for the present study. The embryos were fixed
in formol-alcohol, potassium bichromate-acetic and corrosive
sublimate-acetic and were stored in alcohol until stained and im-
bedded in paraffin. Mainly frontal sections 10-15u thick were
made through the heads of the embryos. These were stained
in toto with alcoholic borax carmine and Weigert’s iron haema-
toxylin, and in the latter case orange G was employed as a counter
stain. The two adult specimens were fixed in potassium bi-
chromate, imbedded in celoidin and cut vertically through the
head. These sections, 30u thick, were stained in haematoxylin-
eosin and orange G.

Stage 1 (fig. 1). The embryo is coiled up in 4% turns. Ol-
factory pit very deep. Wall of optic cup thickened anteriorly;
lens solid. Fixation: corrosive-acetic. Stain: Weigert’s iron
haematoxylin; sections 15u. Frontal sections of head and body.

The auditory vesicle, which is distended into a sac-like struc-
ture, is already oval in shape and, since it runs through 47 sec-
tions, is about 0.705 mm. in antero-posterior diameter. It lies
some distance removed from the brain. Differentiation in the
epithelial lining of the wall of the auditory vesicle is already
apparent. Laterally the epithelium is flattened, while the medial
and lower walls are stratified several cells deep and show here and
there a mitotic figure. This thickened portion represents the
common neuroepithelium which will later separate into the pars
superior and the pars inferior. The ductus endolymphaticus is
already tubular in form, with the dilated saccus endolymphaticus
at the end.

Stage 2 (fig. 2) The embryo consists of 314 coils. The
parietal elevation is prominent. The lens is approximately as in
the preceding stage; the retina moderately pigmented. The

1 The number includes 7 sectioned by the writer.

294 TOKUYASU KUDO

pocket-shaped olfactory pit is deep and the oral sinus deeply
cleft. Fixation: formol-aleohol. Stain: alcoholic borax car-
mine. Sections 15y in thickness cut frontally through head and
entire body. The antero-posterior diameter of the auditory
vesicle is calculated to be 0.48 mm., since it runs through 32
sections.

The auditory vesicle has at this stage undergone considerable
development. The pars superior and the pars inferior are dis-
tinetly separated. The anterior and the posterior semicircular
canals are now completely constricted off; but this is not the case
with the lateral canal; i.e., this canal is not yet independent of,
but still broadly in communication with the main lumen of the
vesicle. The pars inferior is well differentiated and possesses an
elongated oval swelling on the ventro-medial wall of the vesicle.
The ductus endolymphaticus appears as a long slender tube.

In correspondence with the external change in form the epi-
thelial lining is also well differentiated. The anterior canal,
which is flattened in a medio-lateral (partly dorso-ventral)
direction, widens out at its anterior end into an ampulla, and the
crista acustica anterior is here represented by high epithelium
which is continuous, without any decrease in thickness, with the
macula utriculi. The same holds true for the crista lateralis, the
epithelium of which is somewhat lower than that of the anterior
crista. The medial and ventral walls of the utriculus are made
up of especially high stratified epithelium, which, bending
upon itself at the entrance of the pars inferior, passes over into
this without any sharp boundary line. The tallest epithelium
of the medial wall decreases somewhat in thickness as it passes
over into the medial wall of the endolymphatic duct. The
flattened lateral wall of the utriculus presents no points of espe-
cial interest. The crista posterior has moved back some distance
and appears as a thickened zone of cells in several layers at the
ventro-medial portion of the semicircular canal.

Stage 3 (fig. 3) The embryo consists of about 23 coils.
On the surface of the body striations are observed. which
are transverse on the ventral and crossed on the dorsal surface.
Fixation: Corrosive-acetic. Stain: alcoholic borax, carmine.

NERVE ENDORGANS IN THE EAR 295

The 15 sections cut frontally through head and body. The
membranous labyrinth runs through 102 sections and hence
has an antero-posterior diameter of 1.53 mm.

The utriculus and the sacculus communicate by a narrow
foramen, the canalis utriculo-saccularis; the lateral semicircular
canal is now an independent structure. Each nerve endorgan is
well developed. The crista anterior is mound-shaped; the crista
lateralis is a thick cell mass which appears as a crescent in the
sections. Both structures still maintain their connection with the
erista utriculi.

The tall epithelium of the utricular froor, which diminishes in
thickness as it passes upward, doubtless represents the first
anlage of the macula neglecta Retzii. It is continuous with the
macula partis inferioris through the still cylindrical epithelium
of the canalis utriculo-saccularis. The macula partis inferior
consists in this stage of an extended zone of neuroepithelium on
the medial wall of the pars inferior and already there is to be seen
on its margin several minimal though unmistakable points devoid
of nuclei. The fine nerve-fiber bundles that arise from the gan-
glion acusticum show excellent mitotic figures where the fibers
enter the macula. The low cylindrical epithelium of the ductus
endolymphaticus is continuous with the tall neuroepithelium of
the medial wall of the sacculus.

Stage 4 (fig. 4). The embryo, which is made up of 23 coils,
has the appearance of a fully developed individual. Its peculiar
dermal spots are prominently displayed over the entire body.
Fixation: formol. Stain: Alcoholic borax carmine. Sections:
15 » in thickness, cut frontally through the head.

The nerve endorgans are nearly all differentiated and on each
the marginal zone free of nuclei may be recognized. The
cristae anterior and posterior are separated from the macula
utriculi by a low epithelium.

It is worthy of notice that the thick epithelium of the utricular
wall shows clearly a border without nuclei and that it is differ-
entiated from the epithelium of the canal by its greater thickness.
It soon becomes thinner as it passes gradually over into the un-
differentiated epithelium lining the vesicle. This thickening just

296 TOKUYASU KUDO

referred to may well be considered as the first anlage of the macula
neglecta Retzii. In the wall of the canal there is no zone marked
out by a cell-free border, although the epithelium is still rather
thick, and this in turn is continuous with the mound-shaped
swelling, the macula sacculi.

Corresponding to the external changes in form, the macula
partis inferioris is now separated into the papillae basilaris and
lagenae, which are still united by cubical epithelium. The
crista posterior is quite separated from the macula sacculi by an
unspecialized epithelium.

Stage 5. The embryo consists of 23 coils. The external
characters are quite comparable to those of the preceding stage.
Fixation: potassium bichromate. Stain: alcoholic borax car-
mine. The 15 u sections are cut frontally through the head.

The macula neglecta Retzii, which lies closely adjoining the
canalis utriculo-saccularis, is mound-shaped and consists of two
or three layers of cells. The maculae neglecta and sacculi are
united by means of cubical epithelium except in the wall of the
canal, where the epithelial cells are still tall.

The Adult Animal (fig. 5). Fixation in potassium bichromate-
acetic. Stain: haematoxylin-eosin and haematoxylin-orange G.
The section are cut frontally through the head.

Among the endorgans the cristae anterior and posterior are
composed of two- to three-layered epithelium and project as
rounded protuberances into the lumen. The macula utriculi
lies on the anterior-medial wall of the utriculus and is composed
of auditory and supporting cells. The macula neglecta appears
as a swelling in the proximity of the canalis utriculo-saccularis
on the floor of the utriculus; its vesicular auditory cells rest upon
one or two layers of supporting cells. The macula diminishes
in thickness as it passes over into the simple cylindrical epithe-
lium which makes up the wall of the canal and which is continued
beyond in the wall of the sacculus. The tall epithelium found
on the medial wall of the canal is also to be seen on and near the
lateral wall. In several places within and near the canal the
lining is thrown up into wave-like folds.

NERVE ENDORGANS IN THE EAR 297

DISCUSSION

The results of my studies, as presented above, agree on the
origin of the macula neglecta with the view of Fleissig, for it has
been shown that this macula is derived directly from the macula
partis inferioris. Even after the neuroepithelium has been com-
pletely separated by the undifferentiated epithelium from the
pars inferioris, the macula neglecta remains for a long time in
‘connection with the macula sacculi.

The common neuroepithelium on the ventro-medial wall of the
auditory vesicle of stage 1 begins to divide into the utricular and
the saccular portions (stage 2), the histological changes in the
epithelium keeping pace with the external changes in form.
The more strictly utricular portion swells to form the crista
anterior, crista lateralis and macula utriculi, which are united
by means of a tall epithelium. The more strictly saccular por-
tion, separated from the utricular portion by flattened epithe
lium (stage 3) still extends from the medial wall of the canalis
utriculo-saccularis upwards further into the floor of the utriculus.

After the macula saccularis has been differentiated (stage 3)
the macula neglecta gradually protrudes more and more into the
lumen and in stage 4 discloses a border free of nuclei, but is still
connected by means of a cubical epithelial layer with the macula
sacculi. Furthermore, the crista ampullaris posterior becomes
entirely free from the saccular portion, while the papillae basilaris
and lagenae still maintain their connection with the macula
saccularis by means of a bridge of cubical epithelium. In stage
5 the well developed macula neglecta may be seen as a mound-
shaped structure as in adult specimens.

The existence of two maculae neglectae I have failed to demon-
strate in my Trigonocephalus material, although I have minutely
examined the rather comprehensive series of the different stages.
Fleissig says: ‘‘1) die macula sacculi, welche nicht mehr die
ganze mediale Sacculuswand, sondern nur mehr deren unteresten
Abschnitt einnimmt. Ein Epithel, das etwas hoher ist als das
indifferente Wandepithel und ganz typisch in der Umgebung der
Nervendstellen vorkommt, erstreckte sich von der Macula

298 TOKUYASU KUDO

sacculi nach aufwirts zum Foramen Utr.-Sace., wo es zu einer
zweiten Neuroepithelstelle—2) Macula neglecta Sarasinian-
schwillt, die im Foramen Utr.- sacc. (an dessen hinterem Rand)
gelegen, zum kleineren Teil in den Sacculus, zum grésseren in
den Utriculus hineinragt. Von dieser erstreckt sich wieder ein
niedriges Epithel in den Sinus inferior hinein zu persistierenden
3) Macula neglecta (Retzii). Beide Maculae neglectae stehen
auf derselben Entwicklungsstufe.”’

Now even if the bulging endorgan found in the floor of the utric-
ulus of stages 4 and 5 were not to be regarded as the macula
neglecta Sarasini but rather as the macula neglecta Retzii, | would
not feel justified in interpreting the thickened epithelium which
extends through the canalis utriculo-saccularis to the macula sac-
cularis as the macula Sarasini. The further the development
progresses the thinner does the epithelium of the inner wall of the
alveus become as compared with the early stage of the auditory
vesicle. One may readily see that the medial wall of the alveus
communis is lined with relatively taller epithelial cells in stage
2 than in stage 3. From this it is apparent that the neuroepi-
thelium, except where it progressively develops into nerve endor-
gans, is destined to be reduced to indifferent epithelium, even
though the time when it retrogresses be very variable.

According to my opinion, therefore, the tall epithelium of
medial wall of the canal and its proximity represents a develop-
mental stage in the neuroepithelium which later retrogresses.
If this epithelium were to be interpreted as a nerve endorgan, the
tall epithelium of other regions, as e.g., of the lateral wall] of the
canal and the medial wall of the utriculus and the ductus endo-
lymphaticus, would have to be regarded as neuroepithelium, since
these latter regions are quite similar in structure and arrangement
of their epithelial cells to those in the medial wall of the canal.
At any rate, the macula neglecta does not occur in my material
as it has been pictured by Fleissig in his work. But it should be
noted that in the adult snake the epithelium of the canalis
utriculo-saccularis and its immediate environs is relatively much
thicker as compared with the medial and lateral walls.

NERVE ENDORGANS IN THE EAR 299

From the above it appears, then, that the macula neglecta
Retzii, which comes to lie in the floor of the utriculus, arises from
the neuroepithelium of the pars inferior, as was first established by
Fleissig in the case of Gecko; but, as stated above, I am unable
to demonstrate in my material any progressively developing
endorgan which could represent the macula neglecta Sarasini.

Alexander has suggested that in the embryo of Echidna the
tall epithelium at the mouth of the ductus endolymphaticus may
represent the vestige of the Amphibian macula neglecta Sarasini.
This tall epithelium, which is continuous with the neuroepithelium
of the medial utricular wall, Fleissig has also observed in the em-
bryo of Gecko, but his interpretation is a totally different one,
for he does not consider it remarkable that the mouth of the
ductus endolymphaticus, which is still in active growth, should
possess tall epithelium where it passes suddenly into the neuro-
epithelial anlage of the medial utricular wall.

In conclusion I desire to record the observation that the three
semicircular canals of Trigonocephalus japonicus do not develop
synchronously, the medial and posterior canals anticipating the
lateral canal in their development.

SUMMARY

1. The macula neglecta arises directly from the macula partis
inferioris.

2. The occurrence of two maculae neglectae is not to be
observed in my material: while the macula neglecta Retzii is well
developed, there does not form a persistent macula Sarasini nor
does this endorgan even develop temporarily as in Gecko (Fleis-
sig).

3. The anterior and the posterior semicircular canals are
separated off much earlier than the lateral canal.

Kyoto, Sept. 15, 1914.

300 ‘ TOKUYASU KUDO

LITERATURE CITED
The references marked with an asterisk (*) were available to the author.

*ALEXANDER, G. 1900 Uber Entwickelung und Bau der Pars inferior laby-
rinthi der héheren Wirbeltiere. Denkschr. d. k. Akad. d. Wiss. Math.-
Naturw. Kl. 70.

*ALEXANDER, G. 1904 Entwickelung und Bau des inneren Gehérorgans von
Echidna aculeata. Jenaische Denkschr., Bd. 6.
1904 Zur Entwickelungsgeschichte und Anatomie des inneren Gehér-
organs der Monotremen. Centralbl. f. Phys. Bd. 17.
1905 Zur Frage der phylogenetischen, vicariierenden Ausbildung der
Sinnesorgane (Talpa europaea und Spalax typhlus). Zeitschr. f.
Psych. u. Phys. d. Sinnesorg. Bd. 38.

Ayers, H. 1892 Vertebrale Cephalogenesis. 2. A Contribution to the mor-
phology of the Vertebrate Ear, ete. Journ. of Morph. vol. 6.
1893 The macula neglecta again. Anat. Anz. Bd. 8.

Deiters, D. 1862 Ueber das innere Gehérorgan der Amphibien. Reichert u.
Du Bois Reymonds Arch.

Fuetssia, J. 1908 Die Entwickelung des Geckolabyrinthes. Ein Beitrag zur
Entwickelung des Reptilienlabyrinthes. Anat. Hefte, Bd. 37.

Krause, R. 1906 Entwickelungsgeschichte des Gehérorgans. Hertwigs Hand-
buch d. Vergl. u. Experim. Entw.-Lehre.

Krausg, R. 1906 Das Gehororgan der Petromyzonten. Anat. Anz. Erg.-Heft
ion ede 29:

Oxastma, K. 1911 Die Entwickelung des Gehérorgans von Hynobius. Anat.
Hefte. Bd. 45.

Oxagima, K. 1911 Die Entwickelung der Macula neglecta beim Salmoembryo.
Anat. Anz. Bd. 40.

Rerzius, G. 1878 Zur Kenntniss von dem membranésen Gehérlabyrinth bei
den Knorpelfischen. Arch. f. Anat. u. Phys. Anat. Abt. Jahrg.

Retzius, G. 1880 Zur Kenntniss des inneren Gehérorgans der Wirbeltiere.
Arch. f. Anat. u. Phys. Anat. Abt. Jahrg.

*SaraAsiIn, P. uv. F. 1890 Ergebnisse naturwissenschaftlicher Forschungen auf
Ceylon. Bd. 2.

Sarasin, P. vu. F. 1892 Ueber das Gehérorgan der Caeciliiden. Anat. Anz. Bd.
th

Stitz, L. 1912 Ueber sogenannte atypische Epithelformation im hautigen
Labyrinth.-Eine rudimentire Mac. negl. Morph. Jahrb. Bd. 44.

Wenig, J. 1913 Untersuchungen iiber die Entwickelung der Gehérorgane der
Anamnia. Morph. Jahrb. Bd. 45.

*Wirrmaack 1911 Ueber sogenannte atypische Epithelformation im mem-
branosen Labyrinth. Verh. d. Deutsch. Otol. Gesell.

PLATE

301

PLATE 1

1 Stage 1. Stain: Weigert’s Iron haematoxylin, Leitz Achromat 6; Ocular I.

2 Stage 2. Stain: Boraxcarmine. 3XI.

3 Stage 3. Stain: Boraxcarmine. 3XI.

4 Stage 4. Stain: Boraxcarmine. 3XI.

5 Adult. Stain: Haematoxylin-eosin. 1XI,

ABBREVIATIONS

C.u.s. Canalis utriculo-saccularis M.n., Macula neglecta
B., Brain M.s., Macula sacculi
A.v., Auditory vesicle O., Otolith
Lag., Lagena P.i., Pars inferior
L.c., Lateral semicircular canal P.s., Pars superior
A.c., Anterior semicircular canal S., Sacculus

U., Utriculus

302

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AUTHOR’S ABSTRACT OF THIS PAPER ISSUED
BY THE BIBLIOGRAPHIC SERVICE, MAY ll

AN INTRODUCTION TO A SERIES OF STUDIES ON THE
SYMPATHETIC NERVOUS SYSTEM

S. W. RANSON
From the Northwestern University Medical School!

ONE FIGURE

Anatomists have devoted little thought to the functional
pathways within the sympathetic nervous system. Yet it is
obvious that no account of the structure of any part of the
nervous system is complete which does not include an analysis
of the more important conduction paths. Such an analysis
cannot, as a rule, be made by purely morphological methods, but
requires the aid of physiological procedures including degenera-
tion experiments. Above all, the investigator must approach
his subject from the right point of view; he must regard the
structures to be analyzed as parts of a functional mechanism
and strive to understand how it works.

While histologists have given us many details concerning the
structure of the ganglia, they have ignored the composition of the
various nerves and plexuses in the sympathetic system and have
made little effort to analyze what seemed to them a hopeless con-
fusion of interconnected elements. In the anatomical and
histological texts we find no hint that the sympathetic nervous
system is made up of definite functional groups and chains of
neurones as distinct and sharply limited as are any of the con-
duction systems of the brain and spinal cord. Nevertheless,
such is the case; it is even probable that the functional groups
and chains of neurones are more sharply limited in the sympa-
thetic than in the central nervous system. The latter is provided
with a mechanism for the widest possible diffusion of incoming
impulses, while such diffusion does not occur in the former.
Strong stimulation of a single small cutaneous nerve will give

1 Contribution No. 53, February 15, 1918.
305

THE JOURNAL OF COMPARATIVE NEUROLOGY, VOL. 29, No. 4
AuGustT, 1918

306 S. W. RANSON

rise to nerve impulses which are distributed throughout the brain
and spinal cord and may eall into action any part of the smooth
or striated musculature of the body. Nothing in any way com-
parable to this occurs in the sympathetic system.

Excluding the terminal ganglionated plexuses which require
further study, we may say that there is probably no more op-
portunity for diffusion of nerve impulses in the sympathetic nerv-
ous system than there is in an ordinary spinal nerve. This ean

Fig. 1 Diagram of two conduction paths from which all purely topographic
details, such as spinal nerves, rami communicantes, and sympathetic trunk, have
been omitted: a, somatic path with branching efferent fiber; 6, autonomic path
with branching preganglionic efferent fiber, the branches ending in relation to two
postganglionic neurones.

be made clear by a diagram (fig. 1). So far as the possibility
for diffusion of nerve impulses is concerned, it is immaterial
whether the efferent fiber branches in the course of a nerve or
within a ganglion and whether its branches come in contact with
the innervated structure directly or through the mediation of a
second neurone, provided there is in the ganglion no other type
of synapse than that indicated in the diagram.

Thanks to the work of Langley, we have reason to believe that
the sympathetic system, with the probable exception of the
terminal ganglionated plexuses, is built up on the simple lines

STUDIES ON THE SYMPATHETIC NERVOUS SYSTEM 307

indicated in the diagram; and, if so, the working out of conduc-
tion pathways should not be as difficult as we had supposed. In
fact, a great deal along this line has already been accomplished
by the physiologists; but there yet remains a large amount of
work to be done before the course of nerve impulses through the
sympathetic nervous system can.be mapped with accuracy

Since there is considerable confusion in the use of terms re-
ferring to this division of the nervous system, we wish at the
outset to define those which we shall have occasion to use.

The sympathetic nervous system is an aggregation of ganglia,
plexuses, and nerves through which the glands, heart, and all
smooth muscle receive their innervation. It is a term belonging
primarily to descriptive anatomy and includes the ganglionated
plexuses associated with the fifth nerve and the vagal plexuses
of the thorax, as well as the sympathetic trunk and the parts
more directly associated with the latter. Since it is connected
at many points with the cerebrospinal nerves, it is necessary to
decide what shall be included in it. The logical point of separa-
tion is that at which the cerebrospinal nerves give off branches
which run exclusively to the sympathetic system. These
branches of the cerebrospinal nerves form an integral part of
this system. ‘This is well recognized in the case of.the rami com-
’ municantes; but the principle has never been carried through
systematically. On this basis it would include the radix brevis
of the ciliary ganglion, the cardiac and pulmonary rami of the
vagus, and the visceral rami of the second, third, and fourth
sacral nerves. We pass now to a consideration of the terms
selected from the vocabulary of the physiologists.

The autonomic nervous system is that functional division of
the nervous system which supplies the glands, heart, and all
smooth muscle with their efferent innervation. It is the sum
total of all general visceral efferent neurones both pre- and post-
ganglionic.

The preganglionic visceral efferent neurones have their cells
located in the cerebrospinal axis, and their fibers make their
exit from this axis in three streams: 1) cranial—via the III, VII,
IX, X, XI cranial nerves; 2) thoracicolumbar—via the white

308 S. W. RANSON

rami communicantes from the thoracic and upper lumbar spinal
nerves; 3) sacral—via the visceral rami of the II, III, and IV
sacral nerves. The fibers of the thoracicolumbar stream run
to the sympathetic trunk and are distributed through it to ganglia
at higher and lower levels. The fibers of the cranial and sacral
streams make no connection with the sympathetic trunk, but
run directly to the various plexuses. While the fibers of the
thoracicolumbar stream end in the ganglia of the trunk or in
collateral ganglia, those of the cranial and sacral streams end in
terminal ganglia. In these two respects the cranial and sacral
streams agree with each other and differ from the thoracicolum-
bar stream. Also physiologically and pharmacologically the
two former agree with each other and differ from the latter. It
is therefore desirable to divide the autonomic nervous system
into two divisions:

1. The thoracicolumbar autonomic system (called by many
physiologists the sympathetic nervous system).

2. The craniosacral autonomic system (called by many physi-
ologists the parasympathetic system).

The importance of this division is further emphasized by the
fact that most of the structures innervated by the autonomic
system receive a double nerve supply, being furnished with
fibers from both divisions of that system. The thoracicolumbar *
fibers are accompanied in most peripheral plexuses by cranio-
sacral fibers of opposite function, so that an analysis of these
plexuses is greatly facilitated by subdividing the autonomic
system in this way. These statements may be summarized in
the form of three definitions:

The autonomic nervous system is that functional division of
the nervous system which supplies the glands, the heart, and all
smooth muscle, with their efferent innervation and includes all
general visceral efferent neurones both pre- and postganglionic.

The thoracicolumbar autonomic system is that division of the
autonomic system, the preganglionic fibers of which make their
exit from the spinal cord through the thoracic and upper lumbar
spinal nerves.

STUDIES ON THE SYMPATHETIC NERVOUS SYSTEM 309

The craniosacral autonomic system is that division of the
autonomic system, the preganglionic fibers of which make their
exit from the cerebrospinal axis through the III, VII, IX, X,
and XI cranial nerves and the IJ, III, and IV sacral nerves.

The preganglionic neurones are those, the cell bodies of which
lie in the brain or spinal cord and whose axons run through the
cerebrospinal nerves to enter the sympathetic system and end
in its ganglia. The autonomic nervous system therefore includes
certain cells in the brain and spinal cord and certain fibers in the
cerebrospinal nerves and is not contained exclusively in the
sympathetic system. The postganglionic neurones are those
whose cellbodies lie in the sympathetic ganglia and whose axons
run to end on cardiae or smooth muscle or in glandular tissue.

In order to show how these terms will aid in the presentation
cf the facts of visceral innervation, we may give a few examples.
While some points are still obscure, the outlines given below are
as nearly correct as our present knowledge enables us to make
them. They are given not as an ultimate statement of fact, but
as an illustration of the sort of information which we should strive
to perfect.

IMPORTANT FUNCTIONAL PATHS IN THE AUTONOMIC SYSTEM

1. Paths for the efferent innervation of the eye.
a. Ocular craniosacral pathway.

Preganglionic neurones. Cells in the oculomotor nu-
cleus, fibers by way of the III cranial nerve to end in the
ciliary ganglion.

Postganglionic neurones. Cells in the ciliary ganglion,
fibers by way of the short ciliary nerves to the ciliary
muscle and the circular fibers of the iris.

Function—accommodation and contraction of the
pupil.

b. Ocular thoracicolumbar pathway.

Preganglionic neurones. Cells in the intermedio-
lateral column of the spinal cord, fibers by way of the
upper white rami and sympathetic trunk to end in the
superior cervical ganglion.

310 Ss. W. RANSON

Postganglionic neurones. Cells in the superior cer-
vical ganglion, fibers by way of the internal carotid
plexus to the ophthalmic division of the Vth nerve,
the nasociliary and long ciliary nerves to the eyeball:
other fibers pass from the internal carotid plexus through
the ciliary ganglion, without interruption, into the short
ciliary nerves and to the eyeball.

Function—dilation of the pupil by the radial muscle
fibers of the iris.

2. Paths for the efferent innervation of the submaxillary gland.
a. Submaxillary craniosacral pathway.

Preganglionic neurones. Cells in the nucleus. sali-
vatorius superior, fibers by way of the seventh cranial
nerve, chorda tympani and lingual nerve to end in the
submaxillary ganglion on the submaxillary duct.

Postganglionic neurones. Cells in a number of groups
along the chorda tympani fibers as they follow the sub-
maxillary duct, fibers distributed in branches to the sub-
maxillary gland.

Function—increases secretion.

b. Submaxillary thoracicolumbar pathway.

Preganglionic neurones. Cells in the intermedio-
lateral column of the spinal cord, fibers by way of the
upper white rami, and the sympathetic trunk to end in
the superior cervical ganglion.

Postganglionic neurones Cells in the superior cer-
vical ganglion, fibers by way of the plexuses on the ex-
ternal carotid and external maxillary arteries to the
submaxillary gland.

Function—increases secretion.

3. Paths for the efferent innervation of the heart.
a. Cardiac craniosacral pathway.

Preganglionic neurones. Cells in the dorsal motor
nucleus of the vagus, fibers through the vagus nerve to
the intrinsic ganglia of the heart in which they end.

Postganglionic neurones. Cells in the intrinsic cardiac
ganglia, fibers to the cardiac muscle.

Function—cardiac inhibition.

STUDIES ON THE SYMPATHETIC NERVOUS SYSTEM 311

b. Cardiac thoracicolumbar pathway.

Preganglionic neurones. Cells in the intermedio-
lateral column of the spinal cord, fibers by way of the
upper white rami and the sympathetic trunk to the
superior, middle, and inferior cervical ganglia.

Postganglionic neurones. Cells in the cervical ganglia
of the sympathetic trunk, fibers by way of the correspond-
ing cardiac nerves to the musculature of the heart.

Function—cardiac acceleration.

4. Paths for the efferent innervation of the musculature of the
stomach exclusive of the sphincters.
a. Gastric craniosacral pathway.

Preganglionic neurones. Cells in the dorsal motor
nucleus of the vagus, fibers by way of the vagus nerve to
end in the intrinsic ganglia of the stomach.

Postganglionic neurones. Cells in the intrinsic gas-
tric ganglia, fibers to end on the gastric musculature.

Function—excites peristalsis.

b. Gastric thoracicolumbar pathway.

Preganglionic neurones. Cells in the intermedio-
lateral column of the spinal cord, fibers by way of the
white rami from the 5th or 6th to the 12th thoracic
nerves, through the sympathetic trunk without inter-
ruption, and along the splanchnic nerves to the coeliac
ganglion where they end.

Postganglionic neurones. Cells in the coeliac gan-
glion, fibers by way of the coeliac plexus and its offshoots
to the stomach to end on the musculature of the stomach.

Function—inhibits peristalsis.

It will be noted that the organs receive a double autonomic
innervation and that the impulses transmitted along the cranio-
sacral pathways are usually antagonistic to those transmitted
along the thoracicolumbar paths.

The afferent innervation of the viscera. General visceral
afferent fibers are found in the IX and X cranial nerves and in
the spinal nerves. Their cells of origin are located in the cere-
brospinal ganglia. The fibers run through the sympathetic

a2 Ss. W. RANSON

nervous system, passing through the ganglia and plexuses with-
out interruption, to end in the viscera. There is no satisfactory
evidence that any afferent neurones have their cell bodies lo-
cated in the sympathetic ganglia. The function of these afferent
fibers is to convey to the central nervous system impulses giving
rise to vague sensations, and other impulses, which never rising
into consciousness, give rise to visceral reflexes.

Visceral reflex arcs. In the gastrointestinal tract there may
be a mechanism for purely local reflexes, i.e., there are prob-
ably refiex ares complete within the gut wall. With this excep-
tion the evidence strongly indicates that all visceral reflex arcs

ass through the cerebrospinal axis and involve a series of three
neurones: 1) visceral afferent; 2) preganglionic autonomic, and
3) postganglionic autonomic. The purely local reflexes which
seem to occur within the gut wall after section of all the nerves
leading to the intestine are known as the myenteric reflexes and
must depend upon a mechanism different from that of other
visceral reflexes. We do not know what this mechanism is, but
it must be located in the enteric plexuses. The term enteric
nervous system should be restricted to the elements responsible
for the myenteric reflex.

In the papers which follow there will be presented some of the
evidence that has led me to take the general position in regard
to the sympathetic nervous system outlined in the preceding
pages. For much of the evidence, however, it will be necessary
for the reader to refer to the papers of Langley. To this evidence
Dr. Johnson has made an important contribution in showing
that there are no commissural neurones in the ganglia of the
sympathetic trunk of the frog. The papers of Dr. Billingsley
and myself are primarily concerned with details of structure, a
knowledge of which will be necessary for any future attempt to
map the functional pathways of the sympathetic nervous system.

AUTHORS’ ABSTRACT OF THIS PAPER ISSUED
BY THE BIBLIOGRAPHIC SERVICE MAY 11

THE SUPERIOR CERVICAL GANGLION AND THE
CERVICAL PORTION OF THE SYMPATHETIC
TRUNK

S. W. RANSON AND P. R. BILLINGSLEY

From the Anatomical Laboratory of Northwestern University Medical School!

FIFTEEN FIGURES

4

In this paper we shall report observations on the superior cervi-
cal ganglion and the nerves immediately associated with it.
But in dealing with the literature it has been necesssary to treat
the subject in a somewhat broader way and to set forth what is
known concerning the sympathetic ganglia in general.

The general plan of the cephalic end of the sympathetic trunk,
according to the evidence obtained by the nicotine and degenera-
tion methods, is as follows: The trunk below the superior cervical
ganglion consists of fibers ascending to end in that ganglion
(fig. 1). These are preganglionic fibers, the axons of cells located
in the intermediolateral cell column of the spinal cord, which
have entered the trunk through the upper thoracic white rami and
are ascending to the ganglion. Having reached the superior
cervical ganglion, these fibers end in synapses with the postgan-
glionic neurones, whose cell bodies are located there, and to which
belong the postganglionic fibers that leave this ganglion through
its various branches of distribution. Those branches which run
to the internal carotid artery, known collectively as the internal
carotid nerve and forming the internal carotid plexus, carry
postganglionic fibers which are distributed to the eyeball, lacrimal
gland, mucous membrane of the nose, mouth, and pharynx and
many of the blood-vessels of the head. The fibers to the salivary
glands run by way of the branch to the external carotid artery

1 Contribution No. 54, February 15, 1918.
313

314 S. W. RANSON AND P. R. BILLINGSLEY

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Fig. 1 Diagram representing the arrangement of the more important tho-
racicolumbar autonomic pathways to the head in man. The preganglionic fibers
are indicated by solid lines. The cells of the postganglionic neurones are
located in the superior cervical ganglion and their fibers are indicated by dotted
lines. 1, Postganglionic fibers to sweat glands of the face; 2 and 3, to the mu-
cous membrane of the nose; 4, N. cardiacus superior; 5, Rr. laryngopharyngel;
6, branch to the N. hypoglossus; 7, branch to the N. vagus; 8, n. caroticus internus;
9, branch to the N. glossopharyngeus; 10, 11, 12, 13, Rami communicantes (gray)
to Nn. cervicales I, II, III, and IV.

THE CERVICAL SYMPATHETIC TRUNK 315

and follow along its branches to the glands. Through the supe-
rior cardiac nerve postganglionic fibers run to the heart in man.
Other postganglionic fibers join the upper four spinal nerves and
the ninth, tenth, and twelfth cranial nerves to be distributed to
the blood-vessels and glands in the regions supplied by these
nerves, and still others run by the laryngopharyngeal - branches
of the superior cervical ganglion to the larynx and pharynx.

This will serve as a general survey of the field to be studied.
In the pages which follow we will take up in detail the structure
of the superior cervical ganglion, sympathetic trunk and internal
carotid nerve and pay particular attention to the synapses which
occur in the ganglion.

MATERIAL AND METHODS

The superior cervical ganglion of man, the dog, and cat were
prepared by the pyridine silver method and cut into sections
12 to 20 micra thick. Osmie acid preparations were also made
from the dog and cat. Many of the preparations were cut into
serial sections at right angles to the long axis of the ganglion,
beginning at the internal carotid nerve and extending through
the ganglion and some distance along the sympathetic trunk.
Other ganglia were also examined, such as the stellate ganglion
of the cat and the superior cervical ganglion in the rabbit.

In addition to the study of these parts in normal animals,
experiments were carried out to determine the effect of partial
and of complete degeneration of the preganglionic fibers. It
had been noticed in a study of degenerating and regenerating
nerves, made several years previously that certain fibers in the
early stages of degeneration showed an increased affinity for sil-
ver. It was hoped that this might furnish a clue which would
lead to the development of a differential stain for degenerating
axons. A number of ganglia were prepared by the pyridine
silver method sixteen or seventeen hours after section of the
sympathetic trunk in the neck to see if by this method the pre-
ganglionic fibers might be made to stain more intensely through
an increased affinity for the silver. So far we are not convinced

316 S. W. RANSON AND P. R. BILLINGSLEY

that any advantage was obtained by this procedure. It is true
that the majority of our best preparations of the preganglionic
fibers were obtained in this way, but since we occasionally ob-
tained just as good stains in normal animals we are in doubt
as to the value of the preliminary division of the fibers. We
shall consider these as preparations of the normal ganglia since
if there is any change it is only in the direction of an increased
affinity of these fibers for the silver.

In order to obtain complete degeneration of the preganglionic
fibers the sympathetic trunk was divided in the neck. The
operation was performed aseptically on cats and dogs, the nerve
being cut about 2 inches below the ganglion. After periods of
from eight to fifty days some of the animals were killed. It was
found that after the longer periods some regeneration had oc-
curred and the shorter periods were scarcely adequate for full
degeneration. In order to avoid these difficulties, a second
operation was performed on some of the animals twenty to
fifty days after the first, the nerve being cut cephalad to the
neuroma. Eight days after the second operation the animals
were killed.

In dealing with small nerves and ganglia we have found that
the pyridine silver stain often fails to give good results apparently
because the volume of the tissue is too small. In order to over-
ecme this difficulty we find it desirable to imbed the small nerve
or ganglion in the spinal cord. For this purpose we have tied a
fine silk thread to the sympathetic trunk and with a long fine
needle have drawn the trunk with the attached superior cervical
ganglion and internal carotid nerve into a lateral half of the
spinal cord along the line of the ventral gray column. After
fixation for two hours in ammoniated alcohol the block of spinal
cord can be pared down with a razor until it forms a bar the cross-
section of which is not more than 4 mm. square. Within this
block of cord the nerve is held extended and straight and is pro-
tected from the two direct action of the reagents. The cord is
dissected away from the nerve just before it is dehydrated and
cleared in preparation for imbedding.

THE CERVICAL SYMPATHETIC TRUNK oL7

STRUCTURE OF THE CEPHALIC END OF THE SYMPATHETIC TRUNK

As has been said, the cervical portion of the sympathetic trunk
serves to convey preganglionic fibers from the upper white rami
to the superior cervical ganglion. Whether it also contains other
than preganglionic fibers is a question which we will consider in
this paper. In the cat this nerve, a short distance below the
superior cervical ganglion, has the structure shown in figure 2.
In cross-section it is uniform throughout except for one or two
small well-defined bundles at the periphery. These bundles are
not constant and, as we shall see, represent fine branches of dis-
tribution from the ganglion which have been incorporated for
a short distance in the trunk.

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Fig. 2 From a section of the truncus sympathicus a short distance below the
ganglion cervicale superius in the cat. a, area occupied by a bundle of unmye-
linated fibers. Osmic acid. X 425.

Exclusive of these peripheral bundles which really do not
belong to it, the sympathetic trunk below the superior cervical
ganglion in the cat consists almost exclusively of myelinated
fibers as shown in figure 2. These are uniformly distributed and
closely packed. It is as well myelinated a nerve as there is any-
where in the body. The fibers are all rather fine. The majority
vary in diameter from 1.5u to 3.5u. Between these two extremes
there are fibers of all sizes and about as many of one size as
another. Fibers larger than 4.54 are few in number but there
may be two or three as large as 6.5 or 7u. Pyridine silver prep-
arations show rather small axons, each surrounded by an un-
stained halo representing a myelin sheath; these are uniformly
distributed, each well separated from its neighbor. ‘There are

318 S. W. RANSON AND P. R. BILLINGSLEY

no bundles of closely packed unmyelinated axons and no indi-
vidual ones can be made out with certainty. From a study of
the normal truncus sympathicus we may conclude that it is
composed almost exclusively of small myelinated fibers.

The fine peripheral bundles, which represent branches of dis-
tribution from the superior cervical ganglion, can usually be
followed in serial sections to the point where they are given off
as fine branches from the trunk. They do not degenerate after
section of the nerve more caudally. The structure of these
peripheral bundles is entirely different from that of the rest of
the nerve and corresponds to that of the other branches of dis-
tribution given off from the superior cervical ganglion. They
contain a few small myelinated fibers, 1.54 to 6u in diameter,
scattered among the unmyelinated fibers. Such a bundle is seen
at a in figure 2 where the area occupied by the umyelinated
fibers is indicated by stippling. In osmie acid preparations
bundles of unmyelinated fibers are recognized by their being
somewhat more darkly stained than the rest of the background.
A fascicle of axons, even though lightly stained, is easily differen-
tiated from connective tissue. Additional information may be
obtained by the study of the degenerated nerve. In an osmic
acid preparation taken from a cat eight days after neurotomy
of the sympathetic trunk in the neck most of the medullated fibers
are degenerated, although a few cannot be distinguished from
normal fibers. But eighteen days after the operation all the
medullated fibers were degenerated except for a small number in a
single peripheral fascicle, such as has been described and which
is not to be regarded as belonging to the nerve. There were 16
myelinated fibers in this bundle varying in size from 1.8 to 3.6un.
All the other myelinated fibers in the nerve were degenerated.
From this we may conclude that all the myelinated fibers in the
cephalic end of the sympathetic trunk (exclusive of branches
of the superior cervical ganglion which may be incorporated with
it for a short distance) are ascending fibers. There are no medul-
lated fibers arising in the superior cervical ganglion and running
to the ganglia placed more caudally in the truncus sympathicus.

THE CERVICAL SYMPATHETIC TRUNK 319

Waller and Budge showed long ago that the sympathetic trunk
after section in the neck degenerated toward the superior cervical
ganglion. Their results have been confirmed by Langley (’96,
700). This author used the rather unsatisfactory method of
examining the degenerated nerve in teased preparations stained
with osmic acid. He found, however, just as we, in sections
stained with osmic acid, that some fine branches of the superior
cervical ganglion may accompany the nerve for a certain distance.
He also found that occasionally a branch from the vagus might
run to the superior cervical ganglion and accompany the nerve
for a way. This may have been the depressor nerve (p. 374).

After the sympathetic trunk below the stellate ganglion and the
rami communicantes to the first and second thoracic nerves were
cut and time allowed for degeneration, he found no sound myelin-
ated fibers in the cervical portion of the nerve, aside from the
bundles just mentioned which may happen to be included in the
same sheath with it. He concluded that no myelinated fibers
run from ganglion to ganglion through this nerve and none join it
from the cervical rami communicantes.

We have pyridine silver preparations of the degenerated nerve
in both cat and dog. In each case the structure is the same.
Take, for example, Cat XII which was killed fifteen days after
the division of the sympathetic trunk in the neck. In that part
of the nerve just below the superior cervical ganglion the sections
stained with silver showed two fascicles of fine undegenerated
axons mostly unmyelinated at the periphery of the trunk. Fol-
lowing the sections caudally through the series, one of these
fascicles can be seen to leave the trunk, but the other remains
with it as far as our series goes, although it would no doubt
separate off a little farther down.

Aside from these two peripheral fascicles, which, properly
speaking, do not belong to the nerve, almost all of the axons
have degenerated. Here and there throughout the section there
seems to be an isolated unmyelinated axon of normal appearance.
These normal unmyelinated fibers are not numerous. In fact,
since we have never seen such isolated unmyelinated axons

320 S. W. RANSON AND P. R. BILLINGSLEY

elsewhere except in regenerating nerves, we are somewhat skepti-
cal of this observation. The presence of these few axons descend-
ing from the superior cervical ganglion, however, raised the ques-
tions, are there commissural fibers joining the superior cervical
with the stellate or other ganglia?

Here we can take up only the question of the existence of fibers
connecting cells in different ganglia, and will leave out of account
for the moment that of the interconnection of the cells within a
single ganglion. According to Langley, there is no evidence
which would justify us in assuming the existence of commissural
fibers between the cells of different ganglia, and in certain parts
of the sympathetic nervous system he has given strong evidence
that no such connections exist. The mass of evidence which he
has presented is very convincing, but is too extensive to be
summarized here. The reader is referred to the account in
Schiffer’s Physiology, vol. 2, p. 683, and other articles by Lang-
ley in the Journal of Physiology, vol. 25, p. 468, and vol. 31, p. 244.
We can refer here only to that part of the evidence which con-
cerns the cervical portion of the sympathetic trunk. After this
nerve was cut below the ganglion stellatum, and the rami com-
municantes to the first and second thoracic nerves divided and time
allowed for degeneration, stimulation of the trunk in the neck
produced no effect on the pupil, nictitating membrane, eyelids,
hairs, or blood-vessels. Hence the cells of the ganglion stellatum
or the middle cervical ganglion do not send nerve fibers to the
superior cervical ganglion or to the head by way of this nerve.
Even in the normal cat stimulation of this nerve produces no
vasomotor, pilomotor, or secretory effect in the territory supplied
with such fibers by the ganglion stellatum. It is clear, then, that
the superior cervical ganglion does not send commissural fibers
to the vasomoter, pilomoter, or secretory nerve cells of the gan-
glion stellatum which include the great majority of the cells in the
ganglion. It is easy to show that stimulation of the sympathetic
trunk in the neck is without appreciable effect on the heart of the
cat. Hence no fibers descend from the superior cervical ganglion
to the cardio-accelerator neurones of the middle cervical and
stellate ganglia.

THE CERVICAL SYMPATHETIC TRUNK 321

Langley has shown that stimulation of the sympathetic trunk
in the neck causes no general body reflexes of any kind. It must,
therefore, be devoid of sensory fibers, at least of those carrying
painful afferent impulses. We have been able to confirm this
physiological observation and our histological results are also
in agreement with it. On page 4382 we will shotv that the char-
acteristic sensory fibers of the sympathetic trunk are the large
myelinated and the unmyelinated. Except for two or three large
myelinated fibers, there are no fibers which would be interpreted
as sensory ascending in the cervical portion of the sympathetic
trunk.

STRUCTURE OF THE NERVUS CAROTICUS INTERNUS

The chief set of branches given off by the superior cervical
ganglion ascends from its upper pole to the internal carotid
artery. Of these one or two are of large size in the cat. These
large ones are easily and positively recognized in serial sections
of the ganglion and its branches. The entire group of from three
to five branches forms the nervus caroticus internus. It con-
sists of both myelinated and unmyelinated fibers the latter of
course predominating. Figure 3 shows the relative size, number,
and arrangement of the myelinated fibers in this nerve in the cat.
These fibers are rather widely separated by great numbers of
unmyelinated axons and are of about the same size as those of
the sympathetic trunk. They vary in diameter from 1.5y to
4.5u with an occasional larger fiber up to 7u. Their distribution
is quite uniform throughout the nerve. The thickness of their
myelin sheath seems to be somewhat less than that of those in
the sympathetic trunk.

These myelinated fibers are so numerous that interest is at
once aroused as to their source, and the possibility suggests
itself that they are preganglionic or perhaps afferent fibers from
the trunk which have run through the ganglion without interrup-
tion. This possibility is easily excluded, however, by section
of the trunk below the ganglion. After all the myelinated fibers.
in that trunk have degenerated the structure of the internal

THE JOURNAL OF COMPARATIVE NEUROLOGY, VOL. 29, No. 4

322 S. W. RANSON AND P. R. BILLINGSLEY

carotid nerve remains unchanged and contains as many myelin-
ated fibers as the nerve of the opposite side. Measurements
show that fibers of all sizes from 1.5 to 7u are present, showing
that there has not occurred a dropping out of the fibers of a
particular size. In fact, figure 3 represents an internal carotid
nerve after the complete degeneration of the sympathetic trunk
below the superior cervical ganglion of the same side, but illus-
trates perfectly well the normal structure of the nerve.

Fig. 3 From asection of the nervus caroticus internus in the cat. Osmic acid.
x 425.

One must also consider the possibility of these myelinated
fibers being contributed through the rami connecting the superior
cervical ganglion with the upper cervical and certain of the cranial
nerves. Against this assumption are the observations that can
be made on serial sections through the superior cervical ganglion
and ‘the internal carotid nerve after degeneration of the trunk.

THE CERVICAL SYMPATHETIC TRUNK 323

The myelinated fibers in such a ganglion are extremely few at the
caudal pole, but increase gradually toward the cephalic end of the
ganglion. They are scattered uniformly through the cross-sec-
tion of the ganglion, until they begin to assemble at the upper
pole to enter the internal carotid nerve. The few myelinated
fibers that can be seen in the various side branches of the ganglion
(to the cervical and cranial nerves) are at once lost in the ganglion.
There are no bundles of medullated fibers running through the
ganglion from one branch to the other. We believe that all or at
least most of the myelinated fibers in the branches of the superior
cervical ganglion arise from cells located in that ganglion. This
will receive additional support from more detailed study of the
structure of the superior cervical ganglion to follow.

Langley (96) has shown that after section of the branches
peripherally of the superior cervical ganglion nearly all of the
myelinated fibers which remain connected with the ganglion are
normal, while nearly all of those separated from the ganglion
have degenerated, showing that the cells of origin of the great
majority of these fibers are located in that ganglion. These
observations were made on the cat. In the dog he has traced
two small bundles of fibers from the tympanic plexus by way of
the internal carotid artery to the superior cervical ganglion.

It is therefore evident that a considerable number of the
axons arising in the superior cervical ganglion acquire a myelin
sheath. This is in keeping with the results of v. Kolliker (’94),
Dogiel (95), Langley (96), Michailow (’11), and others. It is
interesting to note, however, that Cajal (’11) is of the opinion that
the axons of the cells of the sympathetic ganglia never acquire
myelin sheaths. It is easy to understand how he may never have
been able to trace such an axon into a myelinated fiber, but as
we have seen this is not the only line of evidence that can be
brought to bear on the problem. All things taken into considera-
-tion, the evidence is conclusive that postganglionic axons not
uncommonly acquire myelin sheaths.

324 S. W. RANSON AND P. R. BILLINGSLEY

STRUCTURE OF THE SUPERIOR CERVICAL GANGLION

While we have examined a number of ganglia, including the
stellate and coeliac, the observations which we have to report
are restricted to the superior cervical ganglion. In the account
which follows we will consider the results obtained by others,
topic by topic, as we present our own. Unless otherwise stated,
citations from the literature are applicable to the collateral
ganglia and to all the ganglia of the sympathetic trunk. They
should not be carried over without qualification to the terminal
ganglia. These present special problems and require separate
consideration. .

Ganglion cells. It is well known that almost all of the neurones
in the sympathetic ganglia are multipolar, although there are
also a restricted number of unipolar and bipolar cells located
near the poles of a ganglion or within its longitudinal fiber bundles,
Huber (’99). Like other nerve cells these neurones have but a
single nucleus, except in rodents. In the rabbit we have seen
many cells with two nuclei. These have been figured and de-
scribed with a summary of the related literature by Huber (’99).
The neurofibrils of the cells of the sympathetic ganglia have been
described by a number of authors, including Michailow (’08)
and Cajal (711). The Nissl granules have been described and
figured by Carpenter and Conel (’14).

Dendrites. The dendrites of the cells of the sympathetic
ganglion may be divided into two chief categories—intracapsular
and extracapsular. The former, although presenting great vari-
ety in length and form, are all situated beneath the cell capsule.
Although these intracapsular dendrites are common in the
sympathetic ganglia of man, they are rarely met with in the
other mammals. Michailow (711), in his careful study of the
collateral and trunk ganglia in horses, dogs, cats, rabbits and
guinea-pigs, described and figures only one form of subcapsular
dendrite. These are present on his cells of types II and V.
They are short and club-shaped (fig. 8, a). There are usually
from five to seven of them and they begin as relatively thick
fibers soon going over into bulbous endings. A fiber may
divide and end in two such clubs. The expanded ends of these

THE CERVICAL SYMPATHETIC TRUNK B yaa)

dendrites usually contain pigment in large quantities and are
sometimes vacuolated. Cajal (711) does not describe any sub-
capsular dendrites in the sympathetic ganglia of animals, al-
though they are very prominent in his descriptions and figures
of these ganglia in man. But these dendrites were demonstrated
in the human ganglia by means of his silver stain which was not
used in his earlier studies on animals.

It might be supposed that the use of the newer silver stains
would demonstrate their general occurrence in the mammalian
sympathetic ganglia, but in pyridine silver preparations of the
superior cervical ganglia of cats and dogs we have seen no cells
with subcapsular dendrites. This shows that they must be
relatively rare here and establishes a very striking contrast
between the superior cervical ganglion of man and that of the
carnivora.

The intracapsular dendrites reach their highest development
inman. Here they give rise to complicated subscapsular forma-
tions which were first described by Cajal (11), whose observa-
tions have been confirmed by Marinesco (’06). Both investi-
gators worked with the superior cervical ganglion stained by
the Cajal method. Their observations are confirmed by our
own observations on the human superior cervical ganglion stained
by the pyridine silver method. The account which follows is
based on our own preparations, but is in accord with the results
of the two investigators who preceded us. The subcapsular
dendrites are arranged in a great variety of ways underneath the
capsule of the cell from which they take origin. In general
they may be said to give rise to two types of complicated intra-
capsular networks which Cajal has called dendritic crowns and
glomeruli.

Figure 4 furnishes a good example of a dendritic crown.
Numerous dendrites of varying caliber come off from the cell
and run toward the inner surface of the capsule where, with or
without branching, they turn to run in the subcapsular space.
Here they cross and recross, but do not anastamose, and form an
open network more or less uniformly distributed around the cell.
In some cases these dendrites can be seen to end in small bulbs

RANSON AND P. R. BILLINGSLEY

Se Vie

326

THE CERVICAL SYMPATHETIC TRUNK 320

or rings. The long thick process which is seen piercing the cap-
sule in the illustration is probably the axon, although it might
be an extracapsular dendrite. In that case one would have to
assume that the axon came off from that surface of the cell which
has been cut away at the plane of section.

According to Cajal, these dendrites frequently apply them-
selves against the capsule to terminate on its internal surface or
among the satellite cells by pear-shaped thickenings. Some-
times they are more delicate and bend in beneath the capsule
to terminate by fine pale extremities. Sometimes they run
beneath the capsule in great circles about the cell. The dendritic
nest which envelops the cell is easy to distinguish from the rami-
fications of axons by the greater caliber of its fibers and the
rarity of its divisions. Cajal’s figures show that the spaces among
the subeapsular dendrites contain small cells which he calls
satellite cells.

The dendrites which enter into the formation of the glomeruli
are also subcapsular, but are usually coarser than those just
described. Instead of coming off from all parts of the surface
of the cell, they usually arise from a restricted region. Branch-
ing repeatedly and interlacing they form a mass of considerable
size over which the capsule of the cell is continued. Cajal has
shown that the spaces between the dendritic branches are
occupied by satellite cells. Following his classification, we may
enumerate simple, bicellular, tricellular, and multicellular glom-
eruli according to the number of neurones the dendrites of
which enter into their formation.

The simple glomeruli are formed from the dendrites of one cell.
They are short and thick, come off from one side of the cell, and
raise the capsule to form a pocket within which these dendrites

Fig. 4 Nerve cell surrounded by dendritic crown from the ganglion cervicale
superius of man. Pyridine silver. X 800.

Fig. 5 From the ganglion cervicale superius of man. a, unicellular dendritic
glomerulus; b, cell provided only with extracapsular dendrites. Pyridine silver.
x 800.

Fig. 6 Tricellular glomerulus from the ganglion cervicale superius of man.
Pyridine silver. X 700.

328 S. W. RANSON AND P. R. BILLINGSLEY

branch and intertwine (fig. 5, a). All transition stages are found
between the simple glomeruli and the dendritic crowns. When
the glomerulus is located on the side from which the axon arises
it may be prolonged out for a short distance along the axon,
giving rise to a comet-shaped formation.

The glomeruli formed from the dendrites of more than one
cell may be called composite glomeruli and are somewhat more
complicated than the simple glomeruli just described. The
large subcapsular dendrites of two or more cells converge toward
each other to form a circumscribed mass of branching and inter-
lacing dendrites. Figure 6 gives a good idea of a tricellular
glomerulus, which, along with the three cells, seems to be en-
closed in a single capsule. The capsules and subcapsular satel-
lite cells are not well differentiated in pyridine silver preparations,
but, according to Cajal, the glomeruli are surrounded by a cap-
sule that separates them from the fiber bundles. The capsule is
better defined in the bi- and tricellular than in the multicellular
forms.

The fine black fibers seen interlacing with the dendrites in
figures 5 and 6 are the branches of axons and will be discussed
in another place.

The extracapsular dendrites pierce the capsule and run for
longer or shorter distances among the cells, helping to form an
intercellular plexus of dendritic and axonic ramifications. ‘The
cells of the superior cervical ganglion of the dog and cat are pro-
vided almost exclusively with this type of dendrite. Such dendrites
are also numerous in this ganglion in man. Here they may come
from cells devoid of subcapsular processes (fig. 5, 6) or from cells
provided with dendritic crowns or glomeruli (fig. 5, a). They
are usually coarse fibers and may branch near the cell or may
remain unbranched until they leave the section. Often it is
possible to trace them much longer distances than is indicated
in the figure, but in no case could they be followed to what seemed
to be their true termination (fig. 7). Cajal differentiates three
types of cells in the human superior cervical ganglion: 1) cells
provided exclusively or almost exclusively with subcapsular
dendrites; 2) cells provided only with long dendrites, and 3)

THE CERVICAL SYMPATHETIC TRUNK 329

cells provided with both kinds of dendrites. While such a classi-
fication facilitates description it must not be supposed that these
types are separated by sharp lines of cleavage or that there is
any reason to assign them different functions.

In pyridine silver preparations of the superior cervical ganglion
of dogs and cats the dendrites have not been very well stained.
We could find only extracapsular dendrites, but could trace
none of them to their termination. Figure 12 gives an idea of
how they look when freed from intercellular axonic ramifications.
In order to make an intelligent analysis of the functional con-

Fig. 7 Cell with long extracapsular dendrites from the human superior
cervical ganglion. Pyridine silver. > 400.
nections in the ganglia it is necessary to have a clear idea of the
course and termination of these extracapsular dendrites.

Concerning the true endings of these dendrites our preparations,
which could not be made very thick, give us no information
because all the long dendrites seem to be cut off at the surface
of the section. According to Cajal (711), there are three ways in
which these long intracapsular dendrites in the human superior
cervical ganglion end: 1) They may run into a fascicle of
dendritic fibers where they run parallel to the other fibers of the
fascicle and within which they may end with long interstitial
appendages. At other times they end in olive-shaped extremities,
or in fusiform swellings which give rise to fine varicose branches.

330 S, W. RANSON AND P. R. BILLINGSLEY

2) They may end in glomeruli where they encounter the branches
of other dendrites of the same kind. As indicated in his figures,
such glomeruli are located at a distance from the cells of origin
of the dendrites concerned. 3) They may end in pericellular
baskets. These dendritic baskets have been found in animals
by Cajal (11), Van Gehuchten (’90), Sala (92), and Michailow
(11), and will be discussed more in detail in connection with the
account given by the latter author.

Michailow (’11) has enumerated nine types of cells in the sym-
pathetic ganglia of mammals. This grouping like that of other
authors is chiefly of value as an aid to description, since there
is no evidence that any one type is responsible for a particular
function. From among the various forms, which, according to
him, the dendrites of the cells in the sympathetic ganglia may
assume, we have selected five as the most typical and significant.
Such dendrites may be found in the ganglia of the sympathetic
trunk as well as in the collateral and terminal ganglia. ‘They
are represented in figure 8.

1. Dendrites ending in a brush formation (fig. 8, a). These are
given off insmall numbers (1 to 4) from Michailow’s Type II cells.
They run between the cells of the ganglion where some of them
end; others enter bundles of fibers that leave the ganglion. He
has followed such a dendrite from a ganglion of the solar plexus
of the horse and seen it run as a typical unmyelinated fiber into
another ganglion of the same plexus. These dendrites end in
special formations in the shape of little brooms, consisting of
numerous end branches beset with enlargements. These thick-
enings are of various shapes and sizes. Usually they are flattened
and have the appearance of end plates or of large varicosities.

2. Dendrites terminating in end plates (fig. 8, 6). These are
given off from Michailow’s Type III cells. They begin as rather
thick processes which in unipolar and bipolar cells may be so
thick that it is hard to tell where the cell body ends and the
dendrite begins. Sometimes these dendrites end in the same
ganglion, sometimes they join bundles of nerve fibers and either
end in them or run with them to end in other ganglia. Some
remain thick and coarse to their end, others branch and become

THE CERVICAL SYMPATHETIC TRUNK aol

Fig. 8 Sympathetic ganglion cells showing various types of dendrites. Re-
drawn from Michailow (711). All were stained with methylene blue; a, cell of
Michailow’s Type II from the ganglion mesentericus superius of the horse; b,
cell of Type III from the ganglion coeliacum of the horse; c, cell of Type IV from
the ganglion stellatum of the horse; d, cell of Type VI from the ganglon cervicale
superius of the dog; e, cell of Type IX from the ganglion coeliacum of the horse;
f, cell of Type VIII from the ganglion cervicale superius of the dog.

332 S, W. RANSON AND P. R. BILLINGSLEY

thin, take on the character of unmyelinated fibers and run out
of the ganglion. The endings are in the form of plates of various
sizes and shapes. ‘These may lie free in the connective tissue or
may be pressed against the outside of the capsules of other cells
so close as to produce an impression on the cells. Other end
plates of this type are found in the fiber bundles outside the
ganglia. Hefound great numbers of such end plates in the fiber
bundles of the solar plexus.

3. Dendrites ending in a number of fine branches with end
bulbs closely grouped together as illustrated in figure 8, c. Such
dendrites arise from Michailow’s cells of Type IV. They branch
freely and occupy much space, greatly increasing the territory
of these neurones. They may end in the same or in other ganglia.
Near their termination they begin to divide di- and tricotomously.
The branches are provided with terminal enlargements which
may be rounded or pear-shaped. All the branches of a dendrite
form together an end-apparatus, which may vary in size and
appearance, but is always applied to the outer surface of the
capsule of a cell of Type IV. That is to say, these fibers arise
from cells of Type IV and end upon the surface of the capsules
of other cells of Type IV.

4. Dendrites forming pericellular nests (fig. 8, d). These
arise from the cells of Michailow’s Type VI, are usually short,
and divide repeatedly. The branches approach another cell, and
anastamosing with each other form a network that encloses the
cell. Sometimes such a basket-like network surrounds the cell
from which the dendrite arose. Similar formations have been
described by Dogiel, according to whom they are always extra-
capsular. As already mentioned, Cajal, Van Gehuchten, and
Sala have seen such dendritic nests. The significance of these
structures can best be discussed in a later paragraph.

5. Dendrites the branches of which anastomose to form a
true net out of which a fine fiber, probably the axon, arises
(fig. 8, f). One or more dendrites break up into a great number
of fine branches which anastomose with each other, giving rise to
a network. Out of the net fine filaments arise, which join to-
gether to form a smooth fiber that remains unaltered as far as it

THE CERVICAL SYMPATHETIC TRUNK aaa

ean be followed. Michailow thinks it probable that these smooth
fibers are axons. It will be seen that these neurones resemble
some described by Dogiel in the spinal ganglion.

Are there special sensory dendrites in the sympathetic ganglia?
This problem has been in the foreground ever since 1896 when
Dogiel published his paper on ‘‘Zwei Arten sympathischer
Nervenzellen.”” The one type of dendrite which he thought
belonged to motor cells branched repeatedly in the neighbor-
hood of the cell and ended within the ganglion; the other, which
he thought belonged to sensory cells, resembled unmyelinated
nerve fibers and could be traced long distances. Many of them
could be followed out of the ganglion and were thought to end as
sensory fibers in the viscera. Cajal (11) finds no evidence in
favor of the sensory function of these long dendrites and was not
able to find any of them leaving the ganglia and associated nerve
trunks to end in the viscera. ;

Carpenter and Conel (714), working with Cajal’s method on
the superior cervical ganglion of the cat, could find cells answering
to the description of Dogiel’s two types, but were not convinced
that such cells represent two distinct categories, since all grada-
tions between the two extremes were found. In Nissl prepara-
tions all the cells of the sympathetic ganglia appeared to Carpen-
ter and Conel to be of one type. In the cerebrospinal system
it is easy to recognize sensory and motor cells by the arrangement
of their chromatophile substance, but all the sympathetic gan-
glion cells seemed to have a structure intermediate in character
between that of the cerebrospinal sensory and motor types.
Since these results would indicate that there is but one functional
type of cell in these ganglia and since we know that the majority
of the cells are motor, the probability against the presence of
sensory cells is increased.

So far as we have been able to find no one has confirmed Dogiel’s
account of the sensory type of cell except Kuntz (’13), who found
certain structures which could be interpreted in this way. Nor
has the correlated observation of Dogiel, that fibers, arising from
sensory cells in the sympathetic ganglia, run to end in peri-
cellular baskets about spinal ganglion cells, been much better

334 S. W. RANSON AND P. R. BILLINGSLEY

supported. In regard to this point Huber (’13) has recently
said

the evidence presented by Cajal, Dogiel, Retzius, Huber, and others
cannot be regarded as entirely conclusive, since it has not been de-
termined that the fine medullated fibers or the unmedullated fibers

which appear to enter the spinal ganglia from without and end in
pericellular plexuses, are, in fact, the neuraxes of sympathetic neurones.

Very strong evidence has been presented by Langley (’03) to
show that no medullated sensory fibers run from the sympathetic
to the spinal ganglia.

As regards the white rami, which contain most of the afferent visceral
fibers, there is conclusive evidence that the very great majority of
them have their trophic center in the posterior root ganglia. It con-
sists in the fact that after intraspinal section of a nerve just periph-
erally of the posterior root ganglia, either all, or all but a few, of the
medullated fibers in the white rami degenerate; and that after section
of the sympathetic or of the splanchnic or of the inferior splanchnies
no degenerated fibers are present in the white rami.

Similarly in the sacral autonomic system, the pelvic nerves contain
about 1,000 afferent nerve fibers, and about twice this number of
efferent nerve fibers; on cutting the roots of the sacral nerve, as shown
by Anderson and myself, about half a dozen fibers only remain unde-
generated in the pelvic nerve, and these are probably post-ganglonic
medullated fibers.

Axons of the cells of the sympathetic ganglia. In pyridine silver
preparations of the superior cervical ganglia of the cat, dog, and
man, it is very difficult to follow an axon for any considerable
distance. In fact, it is usually no easy matter to tell which of
the several processes of a cell is to be regarded as an axon. In
a preceding section of this paper it has been shown that some of
these axons acquire a myelin sheath. According to Ko6lliker
(96) and Langley (’00), these axons always end at the periphery,
and never terminate in the sympathetic ganglia.

According to Cajal (’11), who worked with the Golgi and meth-
ylene blue stains on the sympathetic ganglia of animals and
with his silver stain on the superior cervical ganglion of man,
the axons of the cells of the sympathetic ganglia are rather thick,
smooth, and devoid of branches. He says that his anatomical
studies are in accord with the physiological experiments of Lang-

~

THE CERVICAL SYMPATHETIC TRUNK 330

ley and indicate that the axons of these cells dispose themselves
in one of the three following ways: 1) Usually they run trans-
versely to the long axis of the ganglion to enter a gray ramus.
In the initial part of their course these fibers do not give rise to
branches. 2) The axons may run through a connecting nerve
trunk into another ganglion. He is not able to say whether
these axons only run through the second ganglion or whether
they make connections with its cells. In the chick embryo he at
one time described collaterals coming from those longitudinal
fibers of the ganglia which take origin in neighboring ganglia.
He is now inclined to doubt this observation and thinks it likely
that these collaterals all come from fibers that have entered the
sympathetic trunk through white rami at other levels. 3) In
some cases they leave the ganglion and run toward the neighbor-
ing arteries in the visceral nerves.

Sala (’93) described two kinds of fibers in the sympathetic
ganglia. Those of one variety are unbranched, varicose, and
unite to form smaller or larger fascicles which run through the
ganglion in every direction. These are the axons of the cells
of the sympathetic ganglia. The fibers of the other kind area
little larger, non-varicose,and give off collaterals which are finer
and in their turn ramify abundantly. These are less numerous
than the first and are found almost exclusively in the branches
from the cerebrospinal system. It is not improbable, he says,
that these are of cerebrospinal origin.

In his elaborate description of nine types of cells in sympathetic
ganglian Michailow has given very few details regarding the
axons. However, it is to be noted that in none of these nine
types does he describe the axon as terminating in a sympathetic
ganglion and in only one does he describe it as giving off colla-
terals (fig. 8, e).

v. Lenhossék (’94), using Golgi preparations of the chick, traced
axons of sympathetic ganglion cells into the neighboring ganglia,
but did not say what became of them there. In one case he saw
fibers entering a ganglion from a visceral nerve break up into
branches. He considered these the axons of cells lying some-
where in the visceral ganglia. From what we know now they
might just as well be interpreted as the endings of long dendrites.

336 S. W. RANSON AND P. R. BILLINGSLEY

The axons of Dogiel’s Type II cell are figured by that author
as passing through several ganglia giving off collaterals and
finally ending by branching in another ganglion. In the text,
however, he does not claim to have followed such an axon to its
termination. But, as we have said before, no one has been able
to confirm Dogiel’s findings in regard to these cells.

Both Dogiel (95) and Huber (’99) are of the opinion that the
fine fibers which enter the ganglion through its various branches
and take part in the formation of the intercellular plexuses are
the axons of cells in other sympathetic ganglia. Satisfactory
evidence of this is not presented, however, and in the next
section of this paper we will present what seems to be conclusive
evidence that these fine fibers are of cerebrospinal origin.

While it has not been shown that the axons of sympathetic
ganglion cells ever end in connection with the cells of the same
or adjacent ganglia, it seems to be well established that these
axons may give off collaterals within these ganglia. The axons
have been seen to give off collaterals either in the same or adja-
cent ganglia by v. Lenhossék (’94), Dogiel ((95), and Michailow
(11). These do not seem to be present on the majority of the
axons. Michailow is the only one who has seen the mode of
termination of these collaterals. According to him (fig. 8), they
end in little plates, either in the connective tissue of the ganglion
between the nerve cells or pressed against the capsule of a cell.
From their mode of termination it is not evident how these
collaterals could serve to transmit impulses from one neurone
to another. They rather resemble certain collaterals on the
axons of spinal ganglion cells, seen by Huber, Dogiel, and Ranson,
which since many of them end on the cell from which the axon
arose cannot serve for the spreading out of nerve impulses.

Huber (713), in summing up the evidence concerning the inter-
connections of the cells of the sympathetic ganglia, concludes
that “there is at hand morphologic evidence that the neuraxes
of sympathetic neurones, the cell bodies of which are in one
ganglion, terminate either on the cells of the same ganglion or
of other ganglia.’’ To us the evidence seems far from convincing.
Such fragmentary and unsatisfactory histological evidence as

THE CERVICAL SYMPATHETIC TRUNK 337

may exist is more than offset by the strong physiological evidence
against such connections. Some of this physiological evidence
will be briefly presented in a succeeding paragraph.

The intercellular plexus. Throughout the ganglion there is a
rich plexus of dendritic branches and fine axons. This has been
described and figured by Dogiel (’95), Huber (99), and Michailow

Fig.9 Intercellular plexus formed by dendrites and myelinated and un-
myelinated fibers from the semilunar ganglion of the cat. Redrawn from Huber
(799).

(11). The part which the dendrites take in this formation has
been discussed in a preceding section. We are interested here
chiefly in the axonic ramifications which help to constitute it.
According to Huber, one of whose drawings is reproduced in
figure 9, there are in addition to the medullated fibers entering
the ganglion from the white rami, ‘‘small medullated fibers, which
may be traced from this or that nerve root of a ganglion” into

THE JOURNAL OF COMPARATIVE NEUROLOGY, VOL. 29, No. 4

338 S. W. RANSON AND P. R. BILLINGSLEY

the ganglion where ‘‘they are found branching and rebranching,
and forming, with the dendritic processes of the ganglion cells,
what Dogiel has described as the intercellular plexus.’? Huber
quotes with approval the conclusion of Dogiel (95): “Die feinen
Fasern, welche in den Ganglien mit intercellularem Geflechte
endigen, zu den sympathischen, augenscheinlich vorzugsweise
markhaltigen Fasern gehoren.”’ It is interesting to note that
Huber was able to trace some of the fine unmyelinated fibers of
this plexus to definite endings on neighboring dendrites.

According to Dogiel (95), whose observations were made on
the terminal ganglia, the finer myelinated and unmyelinated
fibers enter the ganglion, branch and intertwine, and break up
into fine branches which cross in various directions and finally
break up into finer fibers of uncountable number. These form
a thick plexus among the cells and at the periphery of the ganglion.
The fibers of the plexus are in contact with the dendrites, but
separated from the cell bodies by their capsules. All the fibers
of the plexus are beset with varicosities.

Michailow’s (11) conception of the intercellular plexus differs
from that of the two preceding authors in that, according to him,
the constituent fibers of the plexus anastomose with each other
forming a closed network. By means of this network all or at
least many of these fibers are united together, one neurone being
in this way united with many others. As will be seen later, there
are good reasons for discarding this part of Michailow’s descrip-
tion of the intercellular plexus.

In preparations of the superior cervical ganglion of the cat or
dog by the pyridine silver method one can readily see a plexus of
fine unmyelinated fibers running among the cells in every direc-
tion through the ganglion (fig. 10). The dendrites are not well
stained in these preparations and only their coarser branches are
visible. The finer dendritic ramifications, which, according to
those who have worked with the methylene blue stain, help to
form the intercellular plexuses, are not to be seen. In these
preparations the network of fibers under discussion corresponds
only to the axonie constituents of the intercellular plexuses of
Dogiel and Huber.

THE CERVICAL SYMPATHETIC TRUNK 339

The constituent fibers of this plexus stain rather heavily with
silver and range in color from hght brown to black. They also
vary greatly in size, the smallest being perhaps not more than
one-eighth the thickness of the largest. The larger axons can
often be seen to branch, but the smaller ones seem to run for

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Fig. 10 Intercellular plexus in the ganglion cervicale superius of the dog.
Section 204. Pyridine silver. X 800.

considerable distances without branching. The majority of the
fibers are very fine. They run in and out among the cells, twist-
ing and turning, crossing and recrossing and forming together
a dense interlacement. That practically all of these fibers are
unmyelinated can be seen at once by comparing such a prepara-

340 S. W. RANSON AND P. R. BILLINGSLEY

tion with one stained by osmic acid. In the latter, in place of
the dense interlacement of fine fibers just described, one sees
only here and there an isolated myelinated fiber. In many
parts of the ganglion these are less numerous than the nerve cells.

So far as we can determine the intercellular plexus is entirely
extracapsular. Although some of the fibers wrap themselves
about the cells and form what might seem to be pericellular
plexuses (fig. 11), these are found not to be in any way separated
from the general plexus which fills in the intervening spaces.
We believe that these apparently pericellular baskets are really
pericapsular and represent merely portions of the general plexus
which are in contact with the cell capsules. It is not clear

Fig. 11 Three cells from the ganglion cervicale superius of the dog showing
fibers of the intercellu ar plexus wrapped about them. These fibers seem to be
extracapsular. Pyridine silver. > 800.

whether these formations correspond to the pericapsular nets of
Michailow or not. It is evident, however, that they do not
correspond to Huber’s pericellular plexus which is endocapsular
and forms a closed network. That all of the fibers of the inter-
cellular plexus are extracapsular is shown by the examination
of sections in which the ganglion cells have shrunken, leaving a
cleft between them and their capsule. In such cases the fibers
in question always remain in or upon the capsule and never lie
on the shrunken cell. An additional point of distinction is found
in the fact that the pericellular plexus is a closed network while
as we shall see anastamoses do not seem to occur among the fibers
under discussion. Furthermore, we have twice seen a fragment

THE CERVICAL SYMPATHETIC TRUNK 341

of a closed network on the surface of a cell which we were in-
clined to regard as a true pericellular plexus. From all these
facts we conclude that the pericellular network is ordinarily not
stained in the pyridine silver preparations, but that the axonie
constituents of the intercellular plexuses come out with great
clearness.

It will be remembered that Michailow regarded the plexus
under discussion as forming a true net by means of which all or
at least many of the fibers are united together, one neurone
being thus united to another. This would mean diffuse conduc-
tion in the ganglion, which must then act as a whole. This is
directly at variance with what is known of the physiology of the
sympathetic ganglia. There is no evidence that diffuse con-
duction occurs in any of them, and in at least two, the superior
cervical and the coccygeal ganglia, Langley (00a, ’04) has been
able to show that diffusion does not occur. We will take this
up in connection with a discussion of the synapses in the sym-
pathetic ganglia.

Neither Dogiel nor Huber gives the impression that the inter-
cellular plexus is a closed net and we have carefully examined
pyridine silver preparations for evidence in this regard. While
branching fibers are common, it can usually be seen that a larger
fiber is dividing into two smaller ones. The junction of three
fibers of the same size as at the nodal point of a net does not seem
to occur. Often two fibers could be seen crossing, one im-
mediately over the other, but each retained its individuality
and sharp contour. If the plexus were a true network, one should
be able to find closed meshes surrounded on all sides by anasta-
mosing fibers—an arrangement which does not seem to occur.

In the pyridine silver preparations of the human superior
cervical ganglion the fibers of the intercellular plexus stand out
prominently, as is seen in figure 5. The fibers of this plexus
mingle with the branches of the long or extracapsular dendrites.
Except that the plexus is not as uniformly distributed throughout
the ganglion and is perhaps not quite so dense, it resembles that
in the dog. There is, however, one important feature in which
the human ganglion differs. Fine axons, apparently continuous

342 S. W. RANSON AND P. R. BILLINGSLEY

with those of the intercellular plexus, penetrate into the dendritic
glomeruli and the dendritic crowns forming subcapsular plexuses
in close relation to the subcapsular dendrites. This is well
illustrated in figure 5, a. Cajal has considered these fine darkly
staining axons as preganglionic fibers of spinal origin. From what
has been said and from the accompanying illustrations it will
readily be seen that these fibers are the same as those which form
the intercellular plexuses in the superior cervical ganglion of the
dog and cat. In a paragraph which follows evidence will be
presented to show that these are fibers of spinal origin.

Here and there in this plexus in the superior cervical ganglion
of the dog or cat one can see faintly stained yellow axons about
the size of the larger dark fibers forming the plexus. In many
places these lightly staimed axons are united into bundles of
parallel fibers which run as straight a course as is possible through
the ganglion. These light yellow axons and the bundles into
which they unite do not seem to belong to the plexus, although
necessarily they run through it. The color contrast between
the two kinds of fibers is quite sharp in good preparations, but
since all gradations are found the color alone is not sufficient to
distinguish them. The light axons are among the largest in the
ganglion, are of uniform contour and apparently unbranched.
They show a marked tendency to group themselves into bundles
of parallel fibers in contrast with the more irregular course of the
dark fibers:

Distribution of nerve fibers in the ganglion. In regard to the
termination of axons in the sympathetic ganglia, Cajal (11)
states that in his first work in this field he described two kinds of
terminal arborizations, one set representing the branches of the
longitudinal sympathetic fibers arising in neighboring ganglia,
the other representing branches given off by fibers from the white
rami. That distinction does not seem probable to him any
longer because of the results of Langley’s experiments and be-
cause of the presence of many medullated fibers in the commis-
sural cords which are known to come from the spinal cord (Lang-
ley, ’03, and Miller, 09). Cajal now believes that the two
kinds of terminations belong to spinal motor fibers, distinguished

THE CERVICAL SYMPATHETIC TRUNK 343

only by their course in the sympathetic trunk. One innervates
the ganglion to which the ramus brings it. The other runs
through two or more ganglia before it terminates.

A study of serial sections through the superior cervical ganglion
of the cat stained with osmie acid is instructive. At the lower
pole a large bundle of myelinated fibers can be traced into the
ganglion from the sympathetic trunk. This comes to lie near
the center of the ganglion and breaks up into smaller bundles.
Many of the fibers seem to lose their myelin sheaths while still
within the smaller bundles. At least this seems to be the best
explanation of the fact that the number of myelinated fibers
scattered among the ganglion cells is so small.

When the sympathetic trunk is cut and time allowed for
degeneration all these bundles of fibers have degenerated. There
are, however, still present even in the caudal pole of the ganghon
a very few scattered myelinated fibers which have their cells of
origin in the ganglion. The number of such fibers increases
toward the cephalic pole. Here the myelinated and the more
numerous unmyelinated postganglionic fibers accumulate in
bundles located especially near the periphery of the ganglion.
From the pole large branches representing the internal carotid
nerve are given off. Other smaller branches are given off in
various places from the ganglion.

The small number of myelinated fibers which are scattered
among the ganglion cells in comparison to the number entering
and leaving the ganglion would indicate that they run consider-
able distances in the ganglia as unmyelinated fibers.

In following through a series of sections stained by the pyridine
silver technique, one sees that the fine axons entering the ganglion
from the sympathetic trunk are all stained a dark brown. Each
fiber is surrounded by a thin unstained ring of myelin. This
central bundle of the ganglion can be seen to break up into smaller
and smaller bundles of dark fibers and the constituent fibers of
these smaller bundles can be seen to run into and become a part
of the intercellular plexus described in the preceding section.

Following the series toward the cephalic end of the ganglion,
one sees bundles of axons collecting especially near the periph-

344 S. W. RANSON AND P. R. BILLINGSLEY

ery of the ganglion and these can be followed into its various
branches of distribution. These fibers are stained yellow or
light brown in contrast to the darker fibers entering by way
of the trunk. The staining reaction of these axons is exactly
like that of the bundles of ‘sympathetic fibers’ described in the
vagus and its branches by Chase and Ranson (’14) “where they
are differentiated from the vagus fibers by their lighter stain.”’
We have repeatedly noticed this characteristic light staining
of postganglionic autonomic fibers in the various spinal and
cerebral nerves. Here the contrast with the darker unmyelin-
ated fibers of cerebrospinal origin could not easily be overlooked.

It is true that these lightly stained axons run among the cells
and therefore through the intercellular plexus, but the great
bulk of that plexus is composed of fibers whose staining reaction
resembles that of the fibers entering by way of the sympathetic
trunk. And the impression is gained by a study of such serial
sections that this intercellular plexus is formed by the fibers de-
rived from the trunk, and that the other fibers run through the
plexus as directly as possible to their point of exit from the
ganglion. Were it not for the difference in the color of the two
kinds of axons, however, the impression would undoubtedly be -
given that the plexus is formed by fibers that stream into the
ganglion through all its branches. This is the impression that
Dogiel, Huber, and Michailow have gained from the study of
methylene blue preparations.

The proof that the intercellular plexus is formed by the rami-
fications of the preganglionic fibers is furnished by the experi-
ment of cutting the sympathetic trunk in the neck and allowing
time for degeneration to take place. Pyridine silver preparations
of the superior cervical ganglion in which the preganglionic fibers
have degenerated show no trace of an intercellular plexus (fig.
12). Our technique does not stain the finer branches of the
dendrites and these do not appear in either the normal or altered
ganglia, but the fine axonic ramifications that form the normal
network are gone. One can readily recognize small bundles of
the lightly staining postganglionic fibers and many such fibers
running an isolated course. But these fibers do not coil and

THE CERVICAL SYMPATHETIC TRUNK 5 US

turn about the cells, and wherever several are grouped together
they run parallel to each other in small compact bundles. They
do not give in any way the appearance of the intercellular
network.

By way of summary we may say that the fine myelinated fibers
entering the ganglion through the sympathetic trunk are pre-
ganglionic elements and form by their ramifications a compli-
cated intercellular plexus of fine unmyelinated fibers. The
other branches of the ganglion consists of many unmyelinated
and a few myelinated fibers. These all represent the axons of

Fig. 12 Three cells from the ganglion cervicale superius of a dog in which
the sympathetic trunk had been cut 58 days before the dog was killed. The fine
fibers of the intercellular plexus are absent. Pyridine silver. 800.

the cells in the ganglion and take no part in the formation of
the intercellular plexus. They are the postganglionic fibers of
Langley.

SYNAPSES IN THE SUPERIOR CERVICAL GANGLION

Where are the synapses on the paths through the superior cervica
ganglion located? Langley (00), using his method of paralyzing
the endings of preganglionic fibers by nicotine, has shown that
the fibers of the sympathetic trunk, destined for the superior
cervical ganglion, come from the upper thoracic white rami and
run without interruption through the upper thoracic ganglia.

346 S, W. RANSON AND P. R. BILLINGSLEY

By the same method he has shown that all these fibers end in the
superior cervical ganglion. After painting that ganghon with a
solution of nicotine no response can be obtained on stimulation
of the upper thoracic nerves, showing that all the pathways
through the ganglion are blocked. It is generally admitted
that this blocking occurs at the synapse. The same effect can
be obtained by the intravenous injection of nicotine. Since,
however, large doses of nicotine given intravenously will not
eliminate the effects of stimulating the internal carotid nerve or
other branches of distribution from the ganglion, it is argued
that there are no other synapses interposed between this ganglion
and the tissues innervated. This conclusion is shown to be cor-
rect by the results of the method of degeneration.

That the degeneration, after section of the internal carotid branches,
spreads to the periphery, is shown by stimulating the sclerotic before
and after degenerative section. In the former case, there is a double
effect—local contraction of the radial muscle leading to local enlargement
of the pupil, and loeal contraction of the circular muscle of the iris;
in the latter case, the radial contraction is lacking, the circular takes
place as before.

The results obtained from section of the sympathetic trunk
in the neck and of the internal carotid nerve are all in accord with
the conclusions to be deduced from the nicotine experiments.

Our own observations are in full agreement with the concep-
tions just presented. The trunk consists almost exclusively
of medullated fibers, which would not be the case if it contained
postganglionic fibers ascending from the thoracic ganglia. All,
with the exception of a small bundle of unmyelinated fibers,
degenerate in an ascending direction and the degeneration stops
in the superior cervical ganglion. The internal carotid nerves
are not affected either as to their myelinated or unmyelinated
constituents. The conclusion that the only synapses on the
functional pathways through the superior cervical ganglion are
located in that ganglion is well established. We may now ask
what is the nature of the synapses which are to be found there.

Ts there a mechanism within the ganglion for the general diffusion
of impulses such as occurs in the central nervous system? As a
result of the diffusion of impulses in the brain and spinal cord the

THE CERVICAL SYMPATHETIC TRUNK 347

stimulation of a small sensory nerve may bring about reflex
activity of the skeletal and involuntary musculature over the
entire body. Are impulses disseminated in a similar way in the
sympathetic ganglia? Langley (00) maintains that a pregan-
glionic fiber branches and becomes associated with several
postganglionic neurones and that these taken together form a
functionally isolated unit. That is to say, there is no general
diffusion of impulses through the ganglion. This is beautifully
illustrated by his experiments on the pupilodilator pathway.

As pointed out by Hoffmann (’04), the stimulation of a long
ciliary nerve causes local dilation of the pupil, while stimulation
of the white ramus of either the first or second thoracic nerve
causes a general and symmetrical dilation. This might appear
to be due to a spreading of the impulses within the superior cervi-
eal ganglion to all postganglionic pupilodilator neurones. This
is not the case, however, as Langley (04) has shown: 1) Because
stimulation of a small number of postganglionic fibers as they
leave the ganglion in any one of the four bundles that form the
internal carotid nerve will also cause a symmetrical general
dilation. Fibers from such a bundle undergoing rearrangement
in the internal carotid plexus are distributed to all parts of the
iris. It is therefore unnecessary to assume any spreading out of
nerve impulses through diffusion in the ganglion. 2) Local
dilation of the pupil can, on the other hand, be obtained by
stimulating a few preganglionic fibers in one of the rootlets of the
upper thoracic nerves. It is difficult to see how, on any theory
of the cells being connected together to form a codrdinating
center, stimulation of a small number of preganglionic fibers
could cause rather marked local dilation of the pupil. The spread-
ing out of the impulses which does occur is due to the intermin-
gling of the postganglionic fibers in the preterminal plexuses.

An even more striking case has been made out against the
general diffusion of nerve impulses within sympathetic ganglia in
the case of the coccygeal ganglion.

In all compound ganglia it is obvious that stimulation of certain of

the preganglionic fibers running to the ganglia excites some only of the
nerve cells, and no increase in the strength of the stimulus can cause

348 S. W. RANSON AND P. R. BILLINGSLEY

irradiation of nervous impulses to other cells of the ganglion. And the
nerve cells which cannot then be brought into action may be nerve
cells of the same class as the cells which are in a state of excitation.
Of this we may give an example. In the cat, at times, when the ar-
rangement of nerves is posterior, the fourth lumbar nerve causes erec-
tion of hairs on the tip of the tail; the nervous impulses pass through
nerve cells in the coceygeal ganglion; other nerve cells in the coceygeal
ganglia will, on stimulation cause erection of hairs in the greater part
of the rest of the tail; but no stimulation of the fourth lumbar nerve
will affect this region. Hence, pilomotor nerve cells, set in action by
the fourth lumbar nerve, send no commissural fibers to the other pilo-
motor nerve cells of the coceygeal ganglion. (Langley, ’00.)

It thus appears that there is no physiological evidence indi-
cating that diffusion of nerve impulses occurs in the sympathetic
ganglia and in certain cases, like those cited, there is positive
evidence that diffusion does not occur. We shall now see that
there is no histological evidence of any mechanism which could
serve to bring about such diffusion.

We may picture such a diffusion mechanism in three ways.
The first that suggests itself is a diffuse network formed by
anastomosing branches of the preganglionic fibers. Such a
network has been assumed by Michailow (11), but without
adequate evidence. In this respect his description of the inter-
cellular plexus does not coincide with that given by Dogiel and
Huber. Very clear pictures of the intercellular plexus are ob-
tained in pyridine silver preparations, and these give no indication
of anastomosing fibers or of a closed network. The histological
evidence is therefore distinctly against the existence of this sort
of mechanism for diffusion of nerve impulses.

In the second place, the purpose of diffusion might be served
by purely intraganglionic neurones whose axons would branch
repeatedly and end within the ganglion. So far as we have been
able to find, no one has ever described an axon of a sympathetic
ganglion cell as ending within the ganglion where it began.
Wherever axons have been traced they have always been seen
to leave the ganglion through one or other of its branches. The
intercellular plexus of fine fibers, which Dogiel and Huber thought
represented the ramifications of such axons, and which, if inter-
rupted in this way, might serve as a mechanism for diffusing

THE CERVICAL SYMPATHETIC TRUNK 349

nerve impulses through the ganglion, we have shown to be formed
by the branching of the preganglionic fibers. In a paper which
follows, Johnson presents conclusive evidence that commissural
neurones do not exist in the ganglia of the sympathetic trunk of
the frog.

Finally, diffusion of nerve impulses might occur through
collaterals given off by the postganglionic axons before they left
the ganglion.

That such collaterals exist has been shown by Dogiel, but we
must conclude from his descriptions and figures that they do not
occur on the majority of the axons. Michailow does not find
them except on the axons of his cells of Type [X. He shows that
they end in plates located in the connective tissue of the gangha
between the nerve cells or against the outside of the capsule of a
nerve cell. This mode of termination does not speak for them as
serving the function of transferring impulses from one neurone to
another. In fact, they rather resemble certain collaterals from
the axons of spinal ganglion cells which in all probability serve
no such function.

The complete absence of fine branching axons in the superior
cervical ganglion after degeneration of the preganglionic fibers
is strong evidence against the existence of connections between
the various cells of the ganglia. In such a ganglion the post-
ganglionic axons can be seen to accumulate in bundles of parallel
fibers and run as directly as possible toward the emerging nerves.

From all that has been said we may conclude that there is no
physiological or histological evidence for the existence in the
superior cervical ganglion of a mechanism for the general diffu-
sion of nerve impulses. And the same conclusion would prob-
ably be equally valid for all the ganglia of the sympathetic
trunk. We have already discussed the question of commissural
fibers joining cells located in adjacent ganglia.

Are there any synapses between sensory and motor neurones
within the superior cervical ganglion such as would be required
by the conception of the ganglion as a center for visceral reflexes?
So far as we have been able to learn, no one has ever described
any reflex through this ganglion. According to Langley (’00 a),

300 S. W. RANSON AND P. R. BILLINGSLEY

there are no sensory fibers in the cervical sympathetic trunk,
since stimulation of this trunk produces no reflex effect through
the spinal cord. Since no one has ever claimed that this ganglion
contained sensory elements, it is not necessary to discuss this
question in detail here. The question of the presence of sensory
neurones in the sympathetic ganglia was discussed at some
length in the section of this paper dealing with the dendrites.
The negative evidence (the absence of fine branching axons in the
ganglion after degeneration of the preganglionic fibers) which
indicated the absence of connections between the sympathetic
ganglion cells would also speak against the existence of sensory-
motor synapses.

Synapses between pre-and postganglionic neurones are the only
ones of which physiological experiments have given evidence.
These are also the only ones that have been demonstrated
histologically. The clearest demonstration has been given by
Huber (’99) on the frog (fig. 13 and 14). In preparations stained
with methylene blue he was able to trace the fibers of the white
rami into the trunk ganglia and see them divide repeatedly.
Some of these branches he was able to follow to their termination
as subeapsular pericellular baskets. In a well stained ganglion
it could be seen that the cell body of each neurone was enclosed
in such a pericellular plexus. As a rule, the fibrillae of the plexus
form a closed network, but now and then fibrillae were found end-
ing free. Similar pericellular plexuses were observed by him in
the trunk ganglia of mammals and here again the evidence pointed
to their being the endings of fibers from the white rami. These
pericellular plexuses have been seen by others, including Ehrlich
(96), Retzius (’89), Arnstein (’87), Aronson (’86), Sala (93),
Van Gehuchten (’92), v. Lenhossék (’94), Dogiel (’95), and
Kolliker (96).

Dogiel (95) and Huber (713) could not determine whether all
or only a part of the cells of a sympathetic ganglion were sur-
rounded by pericellular plexuses. I take these statements to
refer to the mammalian ganglia since Huber (’99) has himself
shown that all these cells are so surrounded in the frog. For a
full account of this form of synapse the reader is referred to

THE CERVICAL SYMPATHETIC TRUNK Bll

Huber’s three papers. It seems that the pyridine silver method
usually does not stain these pericellular networks; only occasion-
ally have we seen fragmentary impregnations of them. This is
in keeping with the fact that the method does not readily yield
pictures of nerve endings.

In addition to the pericellular endings thus described there are,
we believe, synapses between preganglionic fibers and the den-
drites of the cells in the superior cervical ganglion. This is true

14

Figs. 13 and 14 Preganglionic fibers and pericellular plexuses of the frog.
Redrawn from Huber (’99). The preparations were stained with methylene blue.
13, preganglionic fibers, the branches of which form pericellular plexuses; 14, a
sympathetic ganglion cell, unipolar, in connection with which a preganglionic
fiber is terminating.

of the subcapsular dendrites in man as well as of the long extra-
capsular dendrites of man and the dog and cat. As was first
shown by Cajal in the superior cervical ganglion of man, the
subeapsular dendrites forming glomeruli and dendritic crowns
are in close relation to fine, darkly staining fibers, which run
among them in every direction. This is illustrated in figure 5
and 6. These fibers have the same appearance, caliber, and

BDZ S. W. RANSON AND P. R. BILLINGSLEY

staining reaction as the fine fibers of the intercellular plexus in
the cat and dog, and they bear the same relation to these sub-
capsular dendrites that that plexus bears to the extracapsular
dendrites. There is every reason to believe that these fibers,
like those of the intercellular plexus, are the branches of pre-
ganglionic axons. There seems to be no essential difference
between the intercellular plexus in man and that which surrounds
the subeapsular dendrites except that of location. So far as we
are able to judge from our preparations, the intercellular plexus
is not so well developed nor so uniformly distributed in man as
in the dog. In the cat and dog there are almost no subcapsular
dendrites, and so far as we have been able to see the intercellular
plexus does not extend beneath the capsule.

We have already given a somewhat extended account of this
intercellular plexus and shown that it consists of the ramifications
of preganglionic axons. Just what is the relation of the rami-
fications to the dendritic branches? In pyridine silver prepara-
tions the fibers do not seem to end on the dendrites, but rather
to form an interlacing feltwork with them. It is probable, how-
ever, that here the actual terminations of the axonic ramifications
are not stained. In methylene blue preparations Huber (’99)
was able to trace some of the fine fibers of the pericellular plexus
to their termination on neighboring dendrites.

It seems to be well established that one preganglionic fiber
may activate several postganglionic neurones (Langley, ’00 b).
Histological evidence points to three ways in which this can be
brought about: 1. The branching of preganglionic fibers, each
branch ending in a pericellular basket about a different neurone.
The best evidence of this has been given by Huber (’99). Figure
13 is a reproduction of one of his drawings of fibers from a white
ramus entering a sympathetic ganglion of the frog. One of
these fibers is associated with three pericellular plexuses. This
mechanism for bringing several postganglionic neurones under
the control of one preganglionic fiber is illustrated diagrammatic-
ally in figure 15, b.

2. The ending of dendrites of one cell in the neighborhood of
another cell so as to come under the influence of the axonic
ramifications in connection with that cell. This relationship is

THE CERVICAL SYMPATHETIC TRUNK 353

illustrated diagrammatically in figure 15, c. The ending of den-
drites of one cell in the immediate neighborhood of another cell
has been observed by a considerable number of investigators.
Such endings occur in a variety of different forms which can
scarcely be accidental. A dendrite may end by forming’ a
pericellular basket about another cell as seen ingfigure 8, d.
Such formations have been seen by Cajal (11), Dogiel (95),

Fig. 15 Diagram Thanet three ways by which one preganglionic fiber
may come into relation with two or more postganglionic neurones. a, pregan-
glionic fibers ending in a tricellular glomerulus in connection with the dendrites of
three neurons; 6, a preganglionic fiber branching to form two pericellular
plexuses; c, a preganglionic fiber ending in connection with the cell body of one
neurone and the dendrite of another which is applied to the outer surface of the
capsule of the first neurone.

Michailow (711), and others. According to’ ‘Dogiel, ‘such dendritic
baskets are always extracapsular. It is obvious that such forma-
tions cannot serve to transmit impulses from one sympathetic
ganglion cell to another unless we are prepared to admit excep-
tions to the law of the dynamic polarity of neurones. But
even then the capsule would be interposed between the nerve
cell and the surrounding dendritic nest. So characteristic an

THE JOURNAL OF COMPARATIVE NEUROLOGY, VOL. 29, No. 4

354 S. W. RANSON AND P. R. BILLINGSLEY
arrangement cannot be entirely accidental; and the most obvious
functional significance of the dendritic nest would be that the
two neurones are thereby in position to be activated by the same
preganglionic fiber. This is now Cajal’s interpretation of the
pericellular dendritic baskets. Such baskets must not be con-
fused with the basket-like appearances produced by dendrites
winding their way between the cells without encircling them as
has been done by Van Gehuchten and Sala. Functionally similar
structures are the plate-like endings of dendrites outside the cap-
sule of another cell as in Michailow’s cells of Type III (fig. 8, 5)
and the smaller egg-shaped endings of the terminal branches of
the dendrites of Michailow’s Type IV cells which are also applied
to the outer surface of the capsule of another cell (fig. 8, c). We
believe that all of these formations are designed to place two
neurones under the influence of the same preganglionic fiber as
illustrated in figure 15, c.

3. Another arrangement of dendrites which seems designed to
favor the simultaneous activation of two or more neurones by
one preganglionic fiber is found in the bi-, tri-, and multicellular
glomeruli in the human superior cervical ganglion. This is
illustrated diagrammatically in figure 15, a. Such glomerulae,
formed by the dendrites of two or more cells, are numerous in the
human ganglion, and one is illustrated in figure 6. A single
axon ramifying within such a glomerulus would be in position to
activate each neurone contributing dendrites to the glomerulus.

SUMMARY AND CONCLUSIONS

Although attention is directed in this paper particularly to the
cephalic end of the sympathetic trunk and the superior cervical
ganglion, the comments drawn from the literature are for the
most part applicable to the entire trunk.

A study of the literature based on the evidence obtained by the
nicotine and degeneration methods shows that the cephalic end
of the sympathetic trunk consists of preganglionic fibers arising
in the upper segments of the spinal cord and terminating in the
superior cervical ganglion, and that the cells located in this gan-
glion give rise to fibers which run to terminate in the glands and
smooth muscle of the head.

THE CERVICAL SYMPATHETIC TRUNK 355

In fact, the cephalic end of the sympathetic trunk consists
almost exclusively of fine medullated fibers, most of which vary
in size from 1.54 to 3.5u. These fibers degenerate in an ascending
direction after section of the nerve. In pyridine silver prepara-
tions no unmyelinated fibers can be distinguished in the normal
sympathetic trunk at this level except for some fine branches of
distribution from the superior cervical ganglion which happen to
be included for a short distance in the same sheath with that
nerve. Our observations along with those of Langley show that
the superior cervical and stellate ganglia are not connected by
myelinated commissural fibers and that unmyelinated commis-
sural fibers if present are very few in number. Physiological
experiments conducted by Langley failed to show any evidence
of commissural fibers joining these two ganglia. Physiological
and histological evidence is also against the presence of afferent
fibers in the cervical portion of the trunk.

The nervus caroticus internus in the cat contains, in addition
to great numbers of unmyelinated fibers, a very considerable
number of fine myelinated fibers, mostly from 1.54 to 5.54 in
diameter. The fibers in this nerve do not degenerate after sec-
tion of the sympathetic trunk in the neck; all or nearly all of them
are postganglionic fibers with their cells located in the superior
cervical ganglion.

The dendrites of the cells in the superior cervical ganglion are
of two kinds, intracapsular and extracapsular. The intra-
capsular dendrites are rare in the sympathetic ganglia of mammals
but abundant in the human superior ganglion. Here they give
rise to the complicated subcapsular formations that have been
designated as dendritic crowns and glomeruli. A glomerulus
may be formed from the dendrites of a single cell or from those
of two or more cells and is designated accordingly as an uni-
cellular, bicellular, tricellular, or multicellular glomerulus.

The extracapsular dendrites are long branched processes which
run in every direction among the ganglion cells. In pyridine
silver preparations it is not possible to follow them to their true
terminations. We have summarized Michailow’s account of the
termination of these dendrites in preparations stained with
methylene blue and illustrated them in figure 8. The dendrites

356 S. W. RANSON AND P. R. BILLINGSLEY

of one cell may form baskets or other special endings about
neighboring cells, but these dendritic endings seem to be always
outside the capsule of the second cell and therefore could not
transmit impulses to it.

Sensory neurones with long dendrites have been described in
sympathetic ganglia by Dogiel, but a review of the literature on
this point shows that his interpretation of these structures has
received little support from the observations of others. It is also
doubtful if the axons of cells in the sympathetic ganglia run to
spinal ganglia to form baskets about the cells located there.

The axons of sympathetic ganglion cells may acquire myelin
sheaths, but usually do not. A study of the literature would
indicate that they usually run, without giving off collaterals,
into one of the branches of distribution arising from the ganglion.
Some run through a connecting nerve to another ganglion, but
there is no evidence to show that they ever end there. It would
seem more likely that these fibers merely run through this second
ganglion to join the nerve to which they are distributed. Some
postganglionic fibers give off collaterals either in the original
ganglion or in a second ganglion through which they pass, but
these collaterals have been shown by Michailow to have endings
not well adapted for the transference of nerve impulses.

Between the cells is a rich plexus of fine axonic ramifications
which is formed by the branching of the preganglionic fibers.
This disappears when the preganglionic fibers degenerate. It is
probable that many of the fibers of the intercellular plexus form
synapses with the dendrites of the sympathetic ganglion cells.

In pyridine silver preparations of the superior cervical ganglion
of the cat it is possible to trace the darkly stained preganglionic
fibers from the sympathetic trunk and to see that they undergo
repeated branching and take a large part in the formation of the
intercellular plexus. The postganglionic fibers, which are more
lightly stained, and for the most part devoid of branches, take
only a minor part in the formation of this plexus, but become
grouped into bundles of parallel fibers which run toward the
branches of distribution of the ganglion.

There is no evidence for the existence of synapses, either com-
missural or sensory-motor, between the neurones located in the

y
THE CERVICAL SYMPATHETIC TRUNK 357

ganglion and there appears to be no mechanism for a diffusion
of incoming nerve impulses to all of the cells nor to all of the cells
of a given function within the ganglion.

Evidence furnished by nicotine and degeneration experiments
shows that all the synapses between the pre- and post-ganglionic
neurones on the pathways through the superior cervical ganglion
are located in that ganglion. There are no ascending postgan-
glionic fibers in the cervical portion of the sympathetic trunk and
no preganglionic fibers are continued through the superior cervical
ganglion into the branches of distribution. The pre-postgan-
glionic synapses seem to be of two kinds: 1) pericellular networks
and 2) relations established between the dendrites and axons
in the intercellular plexus. One preganglionic fiber activates
several post-ganglionic neurones. ‘The dendrites of the post-
ganglionic neurones serve to increase the complexity of these
relationships and may aid in bringing two or more neurones under
the influence of a single axon as indicated in figure 15.

LITERATURE CITED.

ARNSTEIN, C. 1887 Die Methylenblaufairbung als histologische Methode.
Anat. Anz., 2, p. 125.

Aronson 1886 Beitrige zur Kenntniss der centralen und peripheren Nerven-
endigungen. Inaugural Dissertation, Berlin, 1886.

CARPENTER, F. W., AND CoNnEL, J. L. 1914 A study of ganglion cells in the sym-
pathetic nervous system with special reference to intrinsic sensory
neurones. Jour. Comp. Neur., vol. 24, pp. 269-281.

Casa, S. Ramon. 1911 Histologie du systéme nerveux de l’homme et des
vertébrés, vol. 2, p. 891. Paris, 1911.

Cuasz, M. R., anp Ranson, 8. W. 1914 The structure of the vagus nerve.
Jour. Comp. Neur., vol. 24, p. 31.

Doaret, A. 8S. 1895 Zur Frage tiber den feineren Bau des sympathischen Ner-
vensystems bei den Séiugethieren. Arch. f. mikr. Anat., vol. 46, p. 305.
1896 Zwei Arten sympathischer Nervenzellen. Anat. Anz., 11, pp.
679-687.

Enrutcu 1886 Uber die Methylenblaufirbung der lebenden Nervensubstanz.
Deutsche Med. Wochensch., Bd. XII, p. 49.

Hormann, F. B. 1904 Die neurogene und myogene Theorie der Herzthatigkeit
und die Funktion der inneren Herznerven. Schmidt’s Jahrb. d. ges.
Medicin, Bd. 281, p. 118.

Huser, G.C. 1899 A contribution on the minute anatomy of the sympathetic
ganglia of the different classes of vertebrates. Jour. Morph., vol. 16,
pp- 27-90.

358 S. W. RANSON AND P. R. BILLINGSLEY

Huser, G. C. 1913 The morphology of the sympathetic system. XVII In-
ternational Congress of Medicine, London, 1913, Section I, p. 211.

vy. Kéuircer, A. 1894 Uber die feinere Anatomie und die physiologische Be-
deutung des sympathetischen Nervensystems. Gesellschaft Deutscher
Naturforschen und Aerzte. Verhand. 1894, Allgemeiner Theil.

1896 Handbuch der Gewebelehre des Menschen. Bd. 2, pp. 854-871.
Leipzig, 1896.

Kuntz, A. 1913 On the innervation of the digestive tube. Jour. Comp. Neur.,
vol. 23, p. 178.

Lanacuey, J. N. 1892 On the origin from the spinal cord of the cervical and
upper thoracic sympathetic fibers with some observations on white
and grey rami communicantes. Phil. Transact. Roy. Soe. Lond.,
vol. 183, Series B, p. 85.

1896 Observations on the medullated fibers of the sympathetic system
and chiefly on those of the grey rami communicantes. Jour. of Physiol.,
vol:) 205 "p55:

1900 a Remarks on the results of degeneration of the upper thoracic
white rami communicantes, chiefly in relation to commissural fibers
in the sympathetic system. Jour. of Physiol., vol. 25, p. 468.

1900 b The sympathetic and other related systems of nerves. Schié-
fer’s Text-book of Physiology, vol. 2.

1903 The autonomic nervous system. Brain, vol. 26, p. 1.

1904 On the question of commissural fibers between nerve cells having
the same function. Jour. of Physiol., vol. 31, p. 244.

v. LenuosséiK, M. 1894 Beitrige zur Histologie des Nervensystems und der
Sinnesorgane. Wiesbaden, 1894. bs

Marineseo, M. G. 1906 Quelques rechereches sur la morphologie normale et
pathologique des cellules des ganglions spinaux et sympathiques de
Vhomme. Le Névraxe, t. 8, p. 9.

Micuattow, 8. 1908 Die Neurofibrillen der sympathischen Ganglienzellen bei
Saiugetieren. Folia Neuro-biologica, Bd. 1, p. 637.

1911 Der Bau der zentralen sympathischen Ganglien. Internat.
Monatschrift f. Anat. u. Physiol., vol. 28, pp. 26-115.

Mituer, R. L. 1909 Studien iiber die Anatomie und Histologie des sympath-
ischen Grenzstranges insbesondere iiber seine Beiziehungen zu dem
spinalen Nervensysteme. 26. Kongr. innere Med. Wiesbaden, p. 658.
Ref. in Jahres. Anat. u. Entwick., 15 III, p. 731. i

Rertzius, G. 1889 Zur Kenntniss der Ganglien Zellen des Sympathicus. Ver-
handlungen d. biolog. Vereins in Stockholm. Bd. 2, 1889. Cited
after Huber.

Sana, L. 1893 Sur la fine.anatomie des ganglions du sympathique. Archiv.
Ital. de Biol., vol. 18, p. 439.

Van GenucuTen, A. 1892 Les cellules nerveuses du sympathique chez quelques
mammiféres et chez ’homme. La Cellule, t. 8.

WALLER AND BupGE Cited after Langley.

AUTHORS’ ABSTRACT OF THIS PAPER ISSUED
BY THE BIBLIOGRAPHIC SERVICE, MAY l1

ON THE NUMBER OF NERVE CELLS IN THE GANGLION
CHRVICALE SUPERIUS AND OF NERVE FIBERS IN
THE CEPHALIC END OF THE TRUNCUS SYMPATHI-
CUS IN THE CAT AND ON THE NUMERICAL RELA-
TIONS OF PREGANGLIONIC AND POSTGANGLIONIC
NEURONES

P. R. BILLINGSLEY AND S. W. RANSON
From the Anatomical Laboratory of the Northwestern University Medical School!

It is well known that the preganglionic fibers of the white rami
divide and terminate in connection with a number of sympathetic
ganglion cells. But no attempt has as yet been made to secure
data with regard to the number of nerve cells which may be
activated by one preganglionic nerve fiber.

The drawing made by Huber (’99) of the preganglionic fibers:
in the frog shows one fiber with seven branches, four of which
end in pericellular baskets. This would indicate that in the
frog one preganglionic fiber might be associated with at least,
seven postganglionic neurones.

Langley (03) has given us data regarding the number of
ganglia which may receive nerve fibers from a given white ramus
and the number which may receive branches from a given pregan-
glionic fiber.

It must be noted that in the sympathetic system the preganglionic
fibres of any given spinal-nerve have a more extensive connection with
the peripheral ganglia than any single fibre in it has. As an example
I may quote the probable arrangement of the pilomotor fibres of the
first lumbar nerve. The nerve sends fibres to five ganglia, the separate
fibres usually send branches to three ganglia only.

Gaskell (’86) has called attention in a forceful manner to the
great increase in the number of fibers leaving the sympathetic
ganglia by way of the gray rami and other branches of distribu-

1 Contribution No. 55, February 15, 1918.
359

360 P. R. BILLINGSLEY AND 8. W. RANSON

tion over those which enter the ganglia by way of the white rami
and truncus sympathicus.

It is generally acknowledged, since the publication of Bidder and
Volkmann’s paper, that an increase of nerve fibres takes place at the
various ganglia. The nature of such increase is easily seen by the mere
inspection of the nerves which are in connection with such ganglia as the
superior cervical; the number of non-medullated fibres which pass out
of it to proceed peripherally along the internal and external carotid
nerves and along the peripheral grey rami communicantes of the upper
cervical and lower cranial nerves is immensely greater than all the
fibres both medullated and non-medullated which pass to it from the
central nervous system along the cervical splanchnic (cervical sym-
pathetic) nerve. So too the masses of non-medullated fibres which
leave the semi-lunar ganglia to be distributed to the stomach, liver,
intestines, ete., are very much greater than all the fibres contained in
the rami afferentes of these ganglia. It is only necessary to picture
to one self the number of fine medullated nerves contained in the various
nerve roots, In comparison with the number of non-medullated fibres
which pass out of the various ganglia of the body, to see what a great
increase of nerve fibres must have taken place in the course of the
nerves between the central nervous system and the periphery. Doubt-
less such increase is partly to be accounted for by the direct division of
non-medullated nerve fibres. Such division however takes place chiefly
in connection with the passage of the nerve through a ganglion.

It is obvious from all this that the impulses carried by one
preganglionic fiber must be passed on to several postganglionic
neurones. But no observations are furnished which would
enable us to estimate the number. It would add precision to
our conception of the interrelation of these neurones if a fairly
definite numerical ratio could be assigned.

The superior cervical ganglion offers a favorable field for the
investigation of this question. As we have seen in the preceding
paper, there is no reason to suppose that fibers enter it except
those which ascend in the cervical trunk. Aside from a small
peripheral bundle consisting chiefiy of unmyelinated fibers, the
truncus just caudal to the ganglion consists of ascending myelin-
ated fibers. These vary m size from 1.5u to 4.5y, i.e., are typical
preganglionic fibers. In some specimens there are also a few
fibers as large as 64 or 7u which might be interpreted as being
sensory. But in the nerve counted, the largest fiber measured
5y and only eight other fibers approached this in size. In this

.

NUMBER OF PRE- AND POSTGANGLIONIC NEURONES 361

specimen the peripheral bundle of unmyelinated fibers formed a
separate fascicle entirely outside of the perineurium of the trunk.
The few myelinated fibers which this fascicle contained were
descending from the ganglion and were not enumerated. .In the
absence of large myelinated fibers which might possibly be inter-
preted as being sensory, we believe that all of the fibers in the
cephalic end ‘of the trunk proper are ascending preganglionic
fibers (p. 317). So far as we can determine these fibers are not
mixed with any unmyelinated axons.

From these considerations it is evident that an enumeration
of the myelinated fibers in the sympathetic trunk just below the
superior cervical ganglion should give the number of preganglionic
fibers entering the ganglion. We have also ascertained the
number of cells in that ganglion and the ratio between these
cells and the preganglionic fibers.

TECHNIQUE

The cervical portion of the sympathetic trunk was exposed for
its entire length and fixed in osmic acid. During fixation it was
held taut by stretching it over a glass cover-slip with fine silk
threads tied at either end, the upper enclosing the branches of
the internal carotid nerve well above the superior cervical gan-
glion. All the other branches of the ganglion were cut off close
to their origin. The tissue was blocked in paraffine and serial
sections prepared, 10u in thickness, from the superior to the in-
ferior pole of the ganglion, and sections 7 in thickness were made
through the trunk.

The number of fibers in the trunk was determined as follows.
A ruled ocular, No. 10, was used, the ruling enclosing an area of
1 sq. em. subdivided into one hundred forty-four smaller squares.
The lines of the ocular were made parallel to the anteroposterior
and lateral lines of movement of a mechanical stage, the latter
being at right angles to each other. A 7a objective was used.
Beginning at the left side of a section, the fibers within the area
of the ruled square were counted. ‘Then, using only the antero-
posterior movement of the stage, the section was moved the full

362 P. R. BILLINGSLEY AND S. W. RANSON

width of the ruled square, using some well-isolated fiber as a
landmark. This was continued until a column of fibers was
counted extending anteroposteriorly clear through the section.
Then by means of the lateral movement of the stage, the section
was moved the full width of the ruled square and a second column
of fibers counted, and so on until the field was covered.

The number of cells in the ganglion was determined by count-
ing the nucleoli in every fourth section and multiplying the result
by four. The method of using the square ruled ocular and me-
chanical stage was thesameasin counting the fibers. Here especial
care had to be taken to avoid overlooking small nucleoli which
fell behind the ruled lines as well as those which might be out of
focus.

There are several possible sources of error in counting the cells
by this method. Since only every fourth section was counted
and the result multiplied by four to find the total number of
cells, an inaccuracy is introduced, which, however, is made
negligible by the large number of sections counted. A second
source of error may be found in the fact that some few ceiis
contain two nucleoli and the knife may pass between them and
they will then lie in adjacent sections and may each be counted as
representing a cell. This possibility would represent an error
so small as to be negligible. <A third and real source of error is
found in the fact that a certain percentage of all nucleoli are
cut and the parts come to lie in adjacent sections. Parts of
nucleoli would then be counted as whole ones.

Measurements showed that the diameter of the average nucleo-
lus is 2.25u, and since the sections of the ganglion were 10u in
thickness we must assume that 224 per cent of all nucleoli were
cut at some point in their diameters. If the knife passes through
the nucleolus at any point in the middle one-half of its diameter,
each of the resulting parts will probably be thick enough to per-
mit of its being seen and counted as if it were an entire nucleolus.
If the cut passes through either of the outer one-fourths the major
part will be counted but the minor part will be so thin as to be
overlooked. We may therefore assume that one-half of the 223
per cent of cut nucleoli will be so cut as to be seen in two sections

NUMBER OF PRE- AND POSTGANGLIONIC NEURONES 363

and one-half will be so cut as to be recognizable in one section
only. For example, if there actually were four hundred nucleoli
in a ganglion, 774 per cent of these, or 310, would lie wholly
in the sections and be correctly counted. Of the remaining
90 nucleoli which are cut, 45 will be counted twice, and 45 will
be counted once, so that the total number of nucleoli will seem
to be 445. This source of error, amounting to approximately
10 per cent of the number obtained by enumeration, was not
taken into account in the enumerations made by Ranson (’06)
and others on the cells of the spinal ganglia. It seems prob-
able to us that the results of earlier enumerations are therefore
somewhat too high.
RESULTS

The total number of fibers in the sympathetic trunk just below
the ganglion was 3851. In the 138 sections of the ganglion which
were searched for nucleoli 34,334 of them were found. Since
this was done in every fourth section the total for all the sections
would be approximately 137,336. As already stated, we believe
that some nucleoli were cut in such a way as to be recognizable
in two succeeding sections, and for this error a correction of 10
per cent must be made. This would give us 123,603 as the
number of cells actually present in the ganglion.

In this particular specimen, then, there were 3851 myelinated
preganglionic fibers entering the superior cervical ganglion
which contained approximately 123,603 cells. The ratio of
fibers to cells was approximately 1 to 32.

DISCUSSION

Does this ratio of 1 to 32 represent the proportion of pre-
ganglionic to postganglionic neurones? This question raises
two others: Are all the neurones in the ganglion postganglionic,
i.e., cells with axons which run from the ganglion to the tissue
innervated, and to what extent have the preganglionic fibers
given off collaterals to postganglionic neurones in ganglia located
farther caudalward in the truncus sympathicus? The first ques-
tion has been discussed in detail on pages 345-354 of this issue.

364 P. R. BILLINGSLEY AND S. W. RANSON

The evidence is against the existence of any purely intragan-
glionic or commissural neurones; and there is no evidence of the
existence of any sensory neurones in this ganglion. No doubt
the high ratio of fibers to cells will appear to some as an evi-
dence of intraganglionic commissural neurones. But a careful
reading of the paragraph from Gaskell quoted on page 360 should
do away with any feeling that the ratio of preganglionic to post-
ganglionic neurones here given is unreasonably high.

To one who is familiar with the intricate feltwork produced
by the fine branches of the preganglionic fibers which we have
described under the name of intercellular plexus (p. 337) it does
not seem unreasonable that one preganglionic fiber should form
direet synaptic connections with thirty-two postganglionic neu-
rones. However, we do not wish to urge this point and must
admit that, although no satisfactory evidence of their existence
has ever been presented and although we have very strong evi-
dence against their presence in certain ganglia, it is nevertheless
possible that there may be some intraganglionic commissural
neurones in sympathetic ganglia. If there were any in the
superior cervical ganglion the ratio here stated would be by that
much reduced. With regard to the second question we cannot
say with certainty to what extent the fibers ascending in the
cervical sympathetic trunk may have given off collaterals in the
middle cervical and stellate ganglia. We possess, however, in-
formation which makes it possible to form an intelligent opinion
on the question.

The middle cervical ganglion is small and inconstant. The
stellate ganglion, on the other hand, is large and contains many
cells. All the preganglionic fibers running to the superior cer-
vical ganglion must pass by or through it. To what extent do
they give off collaterals to its cells? Some information on this
subject may be gained by a study of the results obtained by
Langley (’92) from stimulating the upper thoracic nerves of the
cat within the spinal canal. So far as the fibers running to
the superior cervical ganglion are concerned, he has shown that
those for the dilation of the pupil arise from the first three thoracic
nerves, those for the nictitating membrane, submaxillary sali-

NUMBER OF PRE- AND POSTGANGLIONIC NEURONES 365

vary gland, and blood-vessels of the head from the first five,
those for the hairs of the face and neck from the first seven. The
fibers to the middle cervical and stellate ganglia for the accelera-
tion of the heart arise from the second to the fifth thoracic nerves,
inclusive. The origin of the fibers terminating in the stellate
ganglion has been determined as follows: pilomotor fibers from
the fourth to the ninth thoracic nerve, secretory and vasomotor
fibers as determined by reactions of the fore-foot from the fourth
to the ninth thoracic nerves.

Since there is no cardiac branch from the superior cervical
ganglion in the eat it is unlikely that the cardiac accelerator
fibers from the second to the fifth thoracic nerves send any
branches beyond the middle cervical ganglion. With the ex-
ception of the accelerator fibers, those from the first three cervi-
cal nerves appear to run exclusively to the superior cervical
ganglion. So far as we can tell, then, there are no fibers running
from the first three cervical nerves which give off collaterals in
the stellate or the middle cervical ganglion and pass on to end in
the superior cervical ganglion.

But the fourth and fifth thoracic nerves send many fibers to
both the superior cervical and stellate ganglia while the sixth and
seventh send a few to the superior cervical ganglion. To what
extent single fibers from these nerves may be connected with
cells in both of these ganglia is uncertain. But there are certain
points worth considering in this connection. Most of the func-
tions controlled through the superior cervical ganglion are highly
specialized, such as dilation of the pupil, movement of the nictita-
ting membrane, salivation and lacrimation; and it is not probable
that preganglionic fibers controlling these functions give off
collaterals in a ganglion of quite different functions like the
stellate. On the other hand, it is quite possible that vasomotor
preganglionic fibers from the fourth and fifth, and pilomotor
fibers from the fourth to the ninth thoracic nerve send branches
to both the stellate and superior cervical ganglia.

The inference to be drawn from this discussion is that while a
. majority of the fibers ascending to the superior cervical ganglion
in the truncus sympathicus pass by the other ganglia in their

366 P. R. BILLINGSLEY AND S. W. RANSON

path without giving off collaterals, a certain unknown percentage
of them may possibly give off such collaterals. Since in our
enumeration the fibers were counted just below the superior cer-
vical ganglion the possibility that collaterals had been given off
from some of these fibers at a lower level makes it not unlikely
that the ratio of postganglionic to preganglionic neurones as
determined in this paper is somewhat too low.

SUMMARY

Careful enumerations show that the superior cervical ganglion
in the cat contains some 123,603 nerve cells and that the truncus
sympathicus near the ganglion contains 3851 ascending pre-
ganglionic myelinated fibers. The ratio between these fibers
and the cells in the ganglion is 1 to 32. We believe that this
ratio may be taken as expressing the approximate numerical
relations between preganglionic and postganglionic elements
for this ganglion.

LITERATURE CITED

Huser, G. Cart 1899 A contribution on the minute anatomy of the sym-
pathetic ganglia of the different classes of vertebrates. Jour. Morph.,
vol. 16, pp. 27-90.

Lanauey, J. N. 1892 On the origin from the spinal cord of the cervical and
upper thoracic sympathetic fibers with some observations on white
and gray rami communicantes. Phil. Transact. Roy. Soc. Lond., vol.
183, Series B, p. 85.

1903 The autonomic nervous system. Brain, vol. 26, p. 1.

Ranson, S. W. 1906 Retrograde degeneration in the spinal nerves. Jour.
Comp. Neur., vol. 16.

AUTHORS’ ABSTRACT OF THIS PAPER ISSUED
BY THE BIBLIOGRAPHIC SERVICE, MAY 11

BRANCHES OF THE GANGLION CERVICALE
SUPERIUS

P. R. BILLINGSLEY AND S. W. RANSON
From the Anatomical Labo atory of the Northwestern University Medical School!

ONE FIGURE

The superior cervical ganglion, which forms the cephalic end
of the sympathetic trunk, has a greater variety of connections
than any other ganglion in the body. Its branches run to three
cranial nerves, three spinal nerves, several arteries, the carotid
glomus, the thyroid, salivary, and lacrimal glands, smooth
muscle of specialized function like that of the eye, the glands and
blood-vessels of the mucous membrane of the head, the glands
and blood-vessels of the skin, and the smooth muscle of the hair
follicles. More information concerning the branches running
to these structures is needed for a proper understanding of the
ganglion. It is possible that fibers ascending through the
sympathetic trunk might leave the ganglion in one of these
branches. The connections with the cervical and cranial nerves
bring it within the bounds of possibility that fibers from one of
these nerves might be running to the ganglion. Neither of
these propositions has much probability in its favor, yet they
should be more carefully ruled out than has as yet been done.
Our chief interest, however, concerns the myelination of the
postganglionic fibers arising from the ganglion.

Throughout the sympathetic nervous system a varying number
of postganglionic fibers acquire myelin sheaths. One might with
reason assume that there is some functional difference between
those which are myelinated and those which are not. On that
assumption some uniformity in the distribution of the two
kinds would be expected. The numerous and functionally

1 Contribution No. 56, February 15, 1918.
367

368 P. R. BILLINGSLEY AND S. W. RANSON

diverse branches of the superior cervical ganglion offer an unusual
opportunity for determining whether or not myelination is
characteristic of any particular functional group of these fibers.
A study of these nerves in several cats also furnishes data as to
how constant the degree of myelination is in any particular nerve.

Since the cat is largely used for experimental work on this part
of the nervous system, it seems desirable to have more accurate
data than has as yet been published concerning the gross anatomy
and topography of these branches in that animal.

In a considerable number of cats the nerves in question were
dissected out, their topographical relations noted, and a stretch
of each fixed in osmic acid. The cats were anesthetized and bled
by cutting the abdominal aorta, to render the field of dissection
free of blood. ‘The dissection was done with the aid of binocular
lenses of X2 magnification. Without such magnification many
of the smallest branches would undoubtedly have been overlooked.
Dissection was further aided by fine threads tied to the vagus,
sympathetic, and other nerve trunks, and to the carotid arteries.
By attaching the threads to iron standards these structures
could be pulled apart at any desired angle and the exposure of
the minute branches of the ganglion rendered more easy. The
field was kept moistened with normal salt solution throughout.
Sections of each nerve were studied and an enumeration made of
its myelinated fibers. It was also determined what proportion
of the fibers fell into each of three dimensional groups. In the
case of the branches to the superior thyroid artery and the
cervical nerves the fibers were grouped into the three following
sizes: 1.5 to 3.3u, 3.3 to 6.6u, 6.64 +. In the other nerves
another grouping was used, namely, 1.5 to 3.3y, 3.3 to 4.5y,
4.5u +. Where the number of fibers was not large the fibers
falling into each group were counted separately with the aid of an ~
ocular micrometer. Where the number was large, as in the
internal carotid nerve, all the myelinated fibers were counted
together with the aid of an ocular ruled in squares. Then the
micrometer eye-piece was placed in the microscope and the
fibers which lay under the micrometer lines were counted sepa-
rately according to size. The field was then shifted and the

BRANCHES OF GANGLION CERVICALE SUPERIUS 369

process repeated until a total of one hundred fibers was counted.
From these data the proportion of fibers of the three sizes was
determined. An oil-immersion objective was used throughout
in measuring the fibers.

In order to determine the relative richness in myelinated fibers,
i.e., the proportion of the myelinated to the unmyelinated, the
area of the section was determined in each case by projecting its
outline with the aid of the camera lucida onto millimeter paper
and determining the number of square millimeters which it cov-
ered. Knowing the magnification, it was easy to determine
the actual area of the nerve in cross-section. This is expressed
in square millimeters in the first column of each table. The
second column gives the total number of myelinated fibers in the
nerve, and the third shows the number of myelinated fibers per
square millimeter. Since none of the nerves had an area as
large as 1 sq. mm., the figures in the third column are greater than
those in column 2. Since the greater part of the area is filled
with unmyelinated fibers, this ratio (myelinated fibers into area)
gives a rough method of comparing the number of myelinated
and unmyelinated fibers in the different nerves. Considerable
error is necessarily introduced into the determination of the
area of the cross-section of a nerve by two factors, unequal shrink-
age during fixation and unequal spreading of the sections on the
slide. But these factors can account for only a small part of the
actual variation of a given nerve in different cats as shown in the
tables. Where a nerve was presented by two or more separate
fascicles their areas were added together and the sum taken as
the area of the nerve. It is probable that in some cases fascicles
belonging to a nerve were lost during dissection, and if so, this
would help to account for a part of the variation in size of the
nerves in different cats. It may be also that there is some ndi-
vidual variation in the course taken by the postganglionic fibers
or in their number. This variation in size is of interest and may
be of significance, but except in so far as it is due to shrinkage
or spreading, does not affect the question with which we are here
primarily concerned, namely, the number of myelinated fibers
per square millimeter of the cross-section of the nerve.

THE JOURNAL OF COMPARATIVE NEUROLOGY, VOL. 29, No. 4

Nearin

BRANCHES OF GANGLION CERVICALE SUPERIUS 371

BRANCHES TO THE CERVICAL NERVES

In accordance with the observations of Langley (93), the
superior cervical ganglion was found to send branches to the
first three cervical nerves only. There was no constant arrange-
ment in the manner of their distribution. A maximum number
of branches is three. They are seen to arise from the lower
pole of the ganglion at the lateral side, and are indicated in
figure 1 by numerals 4, 5, and 6. Their distribution is effected
in several ways, directly with the main trunk of the cervical nerve;
to the communicating loops between the latter, or, especially
when there are less than three branches, they may divide, and
connect with several main trunks, with both communicating
loops, or with a main trunk and a loop. They are directed
ventrally across the nodose ganglion of the vagus to their
terminations.

A fairly constant branch (8) comes from the medial side of the
lower pole, or from the branch to the superior thyroid artery,
or from the main sympathetic trunk just below the ganglion.
It is continued downward a short distance along the common
carotid artery to the level of the origin of the superior thyroid
artery (which arises from the common carotid in the cat) and a
small unnamed artery which turns laterally to the muscles on the
side of the neck. It runs along this latter artery and communi-
cates with either or both of the second and third cervical nerves.

Fig. 1 A diagram of the cervical portion of the sympathetic trunk and of the
branches of the superior cervical ganglion of the cat. The middle cervical gan-
glion (23) has been called the inferior by physiologists; but since it is located at
the upper end of the subclavian ansa, it is more like the middle ganglion in man.
The inferior cervical ganglion is fused with the stellate. 1, branch to the hypo-
glossal nerve. 2, 3, branches to the vagus nerve. 4, 5, 6,8, grayrami. 9, small
branch of the common carotid artery. 10, 22, branches to the superior thyroid
artery. 11, 12, anastamosis with a branch of the hypoglossal nerve. 18, 14,
branches to the external carotid artery. 15, 16, 20, branches to the pharynx.
17, branch to the glossopharyngeal nerve. 18, branch from the glossopharyngeal
nerve to the carotid glomus. 19, carotid glomus. 20, branch from carotid glomus
to the pharynx. 21, perithyroid ansa. 22, branch to the superior thyroid artery.
23, middle cervical ganglion and branch to the recurrent nerve. 24, branch from
the middle cervical ganglion to the vagus nerve.

3i2 P. R. BILLINGSLEY AND S. W. RANSON

When arising from the ganglion or from the sympathetic trunk,
it follows very closely the course of the branch to the superior
thyroid artery as far as the origin of that artery, and then turns
laterally to end as stated above. It is undoubtedly identical
with the branch which Langley says constantly arises as one of
the two terminal divisions of a nerve from the lower pole which
runs downward along the truncus sympathicus and common
carotid artery, the other terminal division being directed along
the superior thyroid artery (see branch to superior thyroid artery).

As table 1 shows, the branches from the superior cervical
ganglion running to the cervical nerves contain relatively few
myelinated fibers. Some of these contained none, and for such
branches the area was not computed. In no ease did a branch
going entirely or in part to the third cervical nerve contain any
myelinated fibers, but in view of the wide variations in the
number of such fibers contained in the other branches it is
doubtful if this is of any significance. The largest number,
44, was found in the branch to the first cervical nerve in Cat |
IV. The number per square millimeter in this branch varied
from 7447 to 251 in the several cats. A study of the table
makes it apparent that there is no regularity in the distribution
of the myelinated fibers nor in the relative proportion of myelin-
ated and unmyelinated fibers. If any particular functional group
were myelinated one would expect more regularity both in the
relative and absolute number of these fibers than is apparent in
the table. The great majority of these fibers did not exceed
3.3u in diameter. In some of the branches larger fibers were
present, and in one case 50 per cent had a diameter of 6.6u
or greater. Are these larger fibers of the same character as the
smaller ones, or are we dealing here with an occasional admixture
of fibers of another category? ‘These larger fibers, for example,
might be sensory and be directed toward the superior cervical
ganglion. Are the small myelinated fibers preganglionic and
coming from the cervical nerves, or postganglionic and taking
their origin in the superior cervical ganglion? These questions
can best be discussed after the other branches from the ganglion
have been studied. The table is instructive, however, in showing

BRANCHES OF GANGLION CERVICALE SUPERIUS 373

TABLE 1 e

Branches to the cervical nerves

AREA IN FIBERS PER| plAMETERS OF MYELINATED FIBERS
SQUARE |NUMBER OF| SQUARE

MJLLIME- FIBERS Mite |=
TERS TER 1.5t03.3u |3.3to6.6u | 6.64 plus

per cent per cent per cent
To nerve 1:
I 0.0079 2 253.50 50 50
II 0.0041 7 1678.25 43 57
Ill 0.0046 11 2888.75 45 55
IV 0.0053 40 7447.17 97.5 Dao
V 0.0021 9 4214.00 | 100
VI 0.0039 i 251.49 100
VII 0.006! 5 757.56 | 100
To nerve 2:
II 0.0076 3 431.81 67 33
IV 0
VI 0.0029 1 339.32 | 100
VII 0.0043 14 3246.25 100
To nerve 3
i 0
To nerves 2 and 3:
VIII 0
xX 0
To loop between
nerves 1 and 2:
VI 0.0049 15 3111.5 él 125 6.5
VIII 0.0035 9 2572.5 100
x
To loop between
nerves 2 and 3:
VIII 0

the complete lack of regularity in the distribution of the myelin-
ated fibers in the branches to the first three cervical nerves.

BRANCHES TO THE VAGUS

A constant communication is found with the nodose ganglion
of the vagus (2) or with the superior laryngeal branch of the
vagus (3) just after it has left the ganglion. The most frequent
arrangement is found in a very small and short twig which
passes laterally from the middle part or from the superior pole
of the superior cervical ganglion to the nodose ganglion. In

374

P. R. BILLINGSLEY

TABLE 2

AND S. W.

Branch to the vagus nerve

RANSON

ane Aone NUMBER OF eAcatin © DIAMETERS OF MYELINATED FIBERS
MILLIMETERS MILLIMETER 1.5 to 3.3 rm 3.3 to 4.5m 4.5 to 6.6
per cent per cent per cent
I 0.0029 18 5939.25 67 28 5
I 0.00027 11 39604. 25 100
5 0.0019 1 510.45 100
IV 0.0018 0
V 0.0021 97 45547 .75 100
VI 0.0018 0
1X 00068 0
one instance as many as four of these twigs were found. In all

other cases there was only one.

In two cases there was no branch to the nodose ganglion, but
instead a short branch was given off to the superior laryngeal
branch of the vagus just after it had left the ganglion, and seemed
in these cases to replace the usual branch.

In table 2 we see that the area of the cross-section of the
branch or branches of communication between the superior cervi-
cal ganglion and the vagus nerve was very much less in Cats II
and IX than in the others. In these cases it is probable that an
additional communicating branch was overlooked when the dis-
section was made. Irrespective of this variation in size, there
was a great variation in the number of myelinated fibers; one
nerve contained ninety-seven of them and another nerve of about
the same size contained none. There was an equally great
variation in the number per square millimeter. In most cases
all of the fibers measured 1.5 to 3.34, but in one nerve there
were some fibers between 3.3 and 6.64. A comparison of tables
1 and 2 shows no essential difference between the myelinated
fiber content of the branches to the cervical nerves and that to
the vagus.

The depressor nerve (7) is sometimes a branch of the superior
laryngeal nerve. It follows the sympathetic trunk and vagus
nerve through the neck into the thorax. Not uncommonly the
fibers of this nerve run to the superior cervical ganglion and leave

BRANCHES OF GANGLION CERVICALE SUPERIUS aie

TABLE 3
Branch to the hypoglossal nerve

DIAMETERS OF MYELINATED FIBERS
can | ivsquare [NUMBER oF| "SOC ane
RULE DES) MILLIMETER | 1 3+t03.3n| 3.3t04.5n| 4.5 to6.6u| 6.6 to 7.5u
per cent per cent per cent per cent
IV 0.0020 6 3123.75 100
VII 0.0019 48 24696 .0 86 v a
VII 0.0049 6 1108.85 50 50
VIII 0.0029 6 1984.5 50 50
IX 0.0025 22 8734.25 95 5
xX 0.0068 20 2964.5 40 25 15 15

it again as a branch from its lower pole. This nerve contains a
large number of medullated fibers which are for the most part
of medium size. When it comes from the superior laryngeal
nerve it may receive a branch from the superior cervical gan-
glion consisting chiefly of unmyelinated fibers.

BRANCHES TO THE HYPOGLOSSAL

A constant branch (1) is found coming from the upper pole, and
is the most lateral of the group of basal bundles, the remainder of
which are continued along as the internal carotid plexus. It
runs upward toward the base of the skull, and is found to com-
municate with the twelfth nerve within its bony canal.

In one instance (11) a small branch was found to come off from
the medial part of the lower pole beside the usual branch to the
superior thyroid artery. It was continued downward with that
nerve to the thyroid artery, along which it coursed for a short
distance, and then ran slightly upward to communicate with a
branch of the twelfth nerve.

A glance at table 3 will show the variation in the myelinated
fiber content which we have already noted in other nerves. The
actual number found varies from six to forty-eight, and there is
an even greater variation in the number per square millimeter.
The great majority of the fibers did not exceed 4.5u in diameter,
but in certain specimens larger fibers were also found. In one
instance 15 per cent measured more than 6.6u, seven of these
fibers having a diameter of 7.5y.

376 P. R. BILLINGSLEY AND S. W. RANSON

TABLE 4

Branch to the glossopharyngeal nerve

bee oe IAT ETON Beach on DIAMETERS OF MYELINATED FIBERS
MMEERS has atau cr 1.5 to 3.3 3.3 to4.5u
per cent i per cent
II ; 0.0033 28 8244.25 93 7
IW 0.0621 655 10547. 25 98 PE
VI 0.0086 85 9934.75 94 6
xX 0.0043 26 6000.5 84.5 15.5

BRANCH TO THE GLOSSOPHARYNGEAL NERVE

Although it is probable that a branch to the glossopharyngeal
nerve is constantly present, it was identified with certainty in
only a few instances. It comes from about the middle of the
anterior surface of the ganglion and runs directly upward with the
branches to the internal carotid and hypoglossal nerve (17).
It joins the petrous ganglion of the glossopharyngeal nerve.
This ganglion is hard to locate in the gross specimen, but was
identified by microscopic examination of that part of the nerve
with which the branch communicated.

Table 4 shows that the relative proportion of myelinated
fibers found in four specimens of this branch was somewhat more
constant than in the case of the preceding nerves studied. These
fibers varied from 6,000 to 10,547 per square millimeter, numbers
which are well within the range of variation found in the other
nerves. The great majority of these fibers did not exceed 3.3y,
-and none measured more than 4.5u.

PHARYNGEAL BRANCHES

These are so small as to be frequently lost in dissection. The
commonest arrangement is to find minute branches coming from
the medial side near the upper pole which run medially over the
carotid artery to the pharynx (16). They are usually paralleled
by the pharyngeal branch of the vagus, and a fusion between
the two may be noted (15). In addition to this there have been
found minute branches from the plexiform arrangement at the

BRANCHES OF GANGLION CERVICALE SUPERIUS 377

TABLE 5
Pharyngeal branches

ste Unopened NUMBER OF yanarees DIAMETERS OF MYELINATED FIBERS
METERS MILLIMETERS 1.5to3.34 3.3 to4.5u
per cent per cent
IV 0.0044 80 18230.25 100
V 0.002 25 12446.0 96 4
VIII 0.0031 4 1274.0 100

bifurcation of the carotid artery (20), where the external carotid
plexus has its origin. .

These branches contain about the same proportion of myelin-
ated fibers as the other branches of the superior cervical ganglion
already studied. These varied from four to eighty in actual
number and from 1,274 to 18,230 per square millimeter. Practi-
cally all of the fibers had a diameter which did not exceed 3.3u.
and in one case 80 per cent of them measured less than 2u.

BRANCH TO SUPERIOR THYROID ARTERY

A constant branch is to be found coming off from the lower
one-third of the ganglion on the medial side (10 and 22). It is
continued downward along the sympathetic trunk and common
carotid artery to the level of the superior thyroid artery, spring-
ing from the common carotid. Here it may give off a lateral
branch (8) which courses along a small unnamed arterial twig
to the second and third cervical nerve. This is the arrangement
noted by Langley (’93) and considered under the description of
the branches to the cervical nerves.

The main part of the nerve can be traced along the superior
thyroid artery to the upper pole of the thyroid gland. It was
thought that in a few instances a twig (21) could be followed
upward along the common carotid artery after curving around the
superior thyroid. If this is true, it would suggest that this is
the perithyroid ansa described by Garnier and Villemin (’10, p.
405). They do not describe their ansa in the cat, but it is pres-
ent in the rabbit and the dog. It is said to give off branches
along the superior thyroid artery and the superficial or ascending

378 P. R. BILLINGSLEY AND 8S. W. RANSON

TABLE 6

Branch to the superior thyroid artery

pl N a a NUMBER OF fone ae DIAMETERS OF MYELINATED FIBERS
MILLIMETERS MILLIMETER 1.5 to 33h 3.3 to 6.6 wu 6.6% plus
per cent per cent per cent
VI 0.0044 28 6238.25 78.5 21.5 ‘
VII 0.0128 45 3503.5 84.5 15.5
VIII 0.004 67 16709.0 100.0 ‘
IX 0.0069 42 6076.0 95.0 2.5m 2.5
x 0.0059 14 2303.0 28.5 50.0 21.5

branch terminates in the plexuses about the lingual and facial
arteries.

On the whole, the myelinated fibers in the branch to the supe-
rior thyroid artery do not differ materially from those in the other
nerves studied. The number per square millimeter shows great
variation and the majority of the fibers do not exceed 3.3y in
diameter. But larger fibers are also found, and in one case 21
per cent measured more than 6.6u.

BRANCHES TO THE EXTERNAL CAROTID ARTERY (NN. CAROTICI
EXTERNIT)

In all but two cases the external carotid plexus was seen to be
formed by two large branches from about the middle of the
medial side of the ganglion (13 and 14), which ran upward and
slightly medialward to the bifurcation of the common carotid
artery. These branches commonly pass medial to the internal
carotid artery, but in one case they passed to either side of the
artery and then joined. At the bifurcation of the common
carotid they communicate by small twigs with the carotid body
and then at once form a rich plexus of fibers which is spread outt,
upon the external carotid artery. At the point of communica-
tion with the carotid body several minute twigs can be traced to
the region of the pharynx.

In two eats, Nos. VIII and X, only one branch was found, in
the others the two branches were treated as one in making up
table 7. The area given in that table is the sum of their areas,

BRANCHES OF GANGLION CERVICALE SUPERIUS 379

TABLE 7

Branches to the external carotid artery

DIAMETERS OF MYELINATED FIBERS
E ARBA NUMBER OF FIBERS PER
CAT IN SQUARE FIBERS SQUARE
MILLIMETERS MILLIMETER

1.5to3.3yu 3.3 to4.5u 4.5 plus

per cent per cent per cent
Ill 0.0207 168 5656 83 13.5 3.5
V 0.0442 © 56 1273 91 6.5 2.5
VII 0.0296 . SF 2949 85.5 1495 oh
VIII 0015 | 21 1433 100
Bx 0.0224 111 4937 88.5 11.5
x 0.0153 298 19428 87 10 3

and the number of fibers is the sum of their fibers. The table
shows that in relative number and size of their myelinated fiber
content these branches do not differ from the others already
studied. Here again we see the now familiar variation in the
number of fibers per square millimeter. Very few fibers exceed
4.5u in diameter.

BRANCHES TO THE INTERNAL CAROTID ARTERY (N. CAROTICUS
INTERNUS)

From the upper end of the ganglion spring some four or five
large branches which are continued directly upward and enter
the skull with the internal carotid artery. These taken together
constitute what is known as the internal carotid nerve. There
does not seem to be any constant number or arrangement of
these bundles and we were unable to verify the scheme of con-
struction outlined by “Langley (04). We have never found
more than five branches.

In each cat the areas of all the bundles belonging to this nerve
were added together and the sum givenin table 8. Inthe same
way the number of myelinated fibers given there is the sum of
that found in the individual bundles. The table shows that the
number of myelinated fibers is both absolutely and relatively
higher in this than in the other nerves studied. The lowest ratio
found was 9,934 per square millimeter and the highest 17,774.
While high ratios were found in individual specimens of other

380 P. R. BILLINGSLEY AND S. W. RANSON

TABLE 8

Branches to the internal carotid artery

oe ne rts poe NUMBER OF Tienes ae DIAMETERS OF MYELINATED FIBERS
MILLIMETERS MILLIMETER 1.5 to 3.3 3.3 to 4.5 25 plus
per cent per cent per cen
iil 0.1173 1346 11466 68 32 ’
VI 0.1038 1845 17774 86 14
VIII 0.1642 2311 14075 68 32
IX 0.3149 3933 12482 68 32
x 0.1751 1741 9934 54 45.5 0.5

nerves, none of these showed the consistently high ratio of the
internal carotid nerve. All of the fibers were under 4.5u, except
in one specimen, not included in the table, in which 32 per cent
of the fibers ranged from 4.5 to 9u in diameter.

DISCUSSION

A comparison of the tables which have been given in this
paper will make it plain that the myelinated fiber content of the
various branches of the superior cervical ganglion is in no way
characteristic of the individual nerves. All of these branches
are characterized by great variation in the absolute and relative
number of myelinated fibers found in different specimens. It
is true that the branches to the cervical nerves show consistently
a relatively low ratio of fibers to area, and the internal carotid
nerve shows consistently a rather high ratio, but we are not sure
that even this represents a significant difference. It would
seem, however, that the relatively small number of myelinated
fibers in the branches going to the cervical nerves might be
characteristic of these branches. .

How are we to interpret the myelinated fibers found in the
branches of the superior cervical ganglion? Are they pregan-
glionic or postganglionic efferent fibers or are some afferent?
Evidence that postganglionic fibers may acquire a myelin sheath
has been presented in other papers of this series (pp. 321-323 of
this issue). The myelinated fiber content of the gray rami
of the other spinal nerves is similar to that of the rami of the

BRANCHES OF GANGLION CERVICALE SUPERIUS 381

first three cervical nerves. On page 419 we will consider the
structure of the gray rami ard the character of the myelinated
fibers they contain. A majority of them are postganglionic.
Sometimes, but not commonly, a few preganglionic fibers, pass-
ing to the sympathetic trunk by white rami, leave it again by gray
rami to end among small groups of cells lying in these rami.
There are also a few afferent medullated fibers in the gray rami.
Most of these enter the trunk through white rami and run out
again through the gray. But it may be that a few, especially
the larger ones, run to the sympathetic trunk by the gray rami.
These statements are based on Langley’s (’96) experiments in
which by a variety of experimental lesions he caused the degenera-
tion of different groups of fibers and in this way determined the
origin of the myelinated fibers in these rami.

There is no reason for supposing that the myelinated fibers in
the other branches of the superior cervical ganglion differ from
those in the grayrami. The majority are certainly postganglionic
fibers. After section of the sympathetic trunk in the neck and
complete degeneration of all the preganglionic fibers ascending
to the superior cervical ganglion there is no degeneration of the
myelinated fibers in the internal carotid nerve. Hence no pre-
ganglionic fibers go through the ganglion into this nerve (p. 321).
The great variation in the proportion of myelinated fibers in
different specimens of the same branch of the ganglion can only
be understood on the assumption that the postganglionic fibers
occasionally acquire myelin sheaths, but that there is no regular-
ity in this. No special functional group of-these fibers acquires
such a sheath regularly or exclusively. The way in which the
myelin sheaths are distributed seems to be entirely accidental.

Kolliker (94) was of the opinion that some functional groups
of postganglionic fibers were better myelinated than others; for
example, the pilomotor fibers of the cat were supposed to be
covered throughout by myelin sheaths, while the fibers to the
intestine, liver, and spleen soon lost their sheaths. If the pilo-
motor fibers were myelinated, consistently, and in any consider-
able number, we should find a different picture in the gray rami
through which these fibers are distributed. But, as we have seen,

382 P. R. BILLINGSLEY AND S. W. RANSON

these rami contained, if anything, fewer myelinated fibers than
the other branches of the superior eervical ganglion.

It will also be clear that there could be no considerable number
of preganglionic or afferent fibers regularly running toward the
superior cervical ganglion in any of its branches without their
presence being indicated in such tabulated data as has already
been presented. The small number of myelinated fibers present
in most of these branches as well as the great variation in the
ratio of such fibers to the area of the nerve speaks against these
fibers being anything other than postganglionic fibers which
have acquired myelin sheaths, and this apparently without rule
or regularity.

The internal carotid nerve is the one which most regularly
contains a high absolute and relative content of myelinated
fibers. But, as has already been said, degeneration experiments
show that this nerve contains no preganglionic fibers continued
into it through the ganglion from the sympathetic trunk. Onthe
other hand, Langley (’96) has shown that section of this nerve
close to the ganglion causes degeneration of its myelinated fibers,
which shows that these fibers are running from and not toward
the ganglion. His statements appear to apply to all the branches
of the superior cervical ganglion, but we are not sure that he
means to include more than the large anterior branches going to
the carotid artery. He says:

On section of the branches peripherally of the ganglion, nearly all the
fibers which remain connected with the ganglion are unaffected, whilst
nearly all the fibers separated from the ganglion degenerate. Hence,
then, nearly all the medullated fibers contained in the nerve strands
given off by the superior cervical ganglion arise from nerve cells in that
ganglion. As to the remaining fibers I have shown (J. Physiol., 14,
p. II) that in the dog there are usually two small bundles which pass
from the tympanic plexus to the internal carotid artery, and run thence
to the superior cervical ganglion by the side of the anterior branches of
the ganglion. Probably in the cat there are some homologous nerve
fibers.

In a few specimens of certain of the branches a limited number
of larger myelinated fibers were found. See tables 1, 3, and 4.
In one specimen of the internal carotid nerve not recorded in

BRANCHES OF GANGLION CERVICALE SUPERIUS 383

table 8 we also found a considerable number of these larger sizes.
Are we to regard these fibers measuring about 6.6u as very large
postganglionic elements or as fibers of another character, for
example, sensory, which, as a variation, have been included in
these particular specimens?

CONCLUSIONS

All of the branches of the superior cervical ganglion, exclusive
of the sympathetic trunk, contain, in addition to great numbers
of unmyelinated fibers, also a limited number of myelinated
fibers. Nearly all of these have a diameter of less than 4.5y,
though in a few specimens we have found some fibers measuring
more than 6.64. The internal carotid nerve seems to contain
regularly a rather large number of myelinated fibers and the
gray rami to the first three cervical nerves a smaller number.
The same relation holds for the proportion of myelinated fibers
per square millimeter in these nerves. Otherwise there is nothing
characteristic about the myelinated fiber content of any of these
branches.

The great majority if not all of these fibers are postganglionic.
This has been ascertained for the internal carotid nerve by
degeneration experiments. If regularly myelinated preganglionic
or afferent fibers were present in any of the branches we should
expect to find evidences of them in the tabulated data given
in this paper. The best explanation of the great variation in the
number of myelinated fibers in different specimens of the same
nerve is that myelination takes place in a limited number of
postganglionic fibers and that this occurs without law or order.
If any functional group of postganglionic fibers was more likely
to become myelinated than another we should expect to find
certain of the functionally diverse branches of the superior
cervical ganglion better myelinated than others, but this is not
the case, except for a slightly better myelination of the internal
carotid nerve and a somewhat poorer myelination of the gray
rami. The indications are that myelination is not related in
any very direct way to the function of the fibers.

384 P. R. BILLINGSLEY AND S. W. RANSON

LITERATURE CITED.

GARNIER, C., AND VILLEMIN, F. 1910 Sur une anse nerveuse sympathique non
encore décrite antour de l’artére thyroidienne supérieure. J. de
VAnat. et Physiol. Par., vol. 46, pp. 405-481.

vy. Kéuurcer, A. 1894 Uber die feinere Anatomie und die physiologische
Bedeutung des sympathischen Nervensystems. Verhandl. Gesell.
Deutsch. Naturf. u. Aerz., Versam. 66, Theil 1, pp. 97-120. +

LanGuey, J. N. 1893 On the ‘accessory’ cervical ganglion in the cat and notes
on the rami of the superior cervical ganglion. Jour. Physiol., vol. 14.
1896 Observations on the medullated fibers of the sympathetic system
and chiefly on those of the gray rami communicantes. Jour. Physiol.,
vol. 20, p: 55.
1904 On the question of commissural fibers between nerve cells hay-
ing the same function. Jour. Physiol., vol. 31, p. 244.

AUTHOR'S ABSTRACT OF THIS PAPER ISSUED
BY THE BIBLIOGRAPHIC SERVICE, MAY 11

ON THE QUESTION OF COMMISSURAL NEURONES
IN THE SYMPATHETIC GANGLIA

SYDNEY E. JOHNSON
From the Anatomical Laboratory of Northwestern University Medical School’

FIFTEEN FIGURES

CONTENTS

eel troduction meeery. = see aera ee so tele od ASI ED Cs 2 erst dcponkt ete ies ae 385
ieee Niertertallixarn came tn odsier., ss shacac aed aatese altes costes cheveverceeaetene seer aicaae ke 387
MO Deenvationss. merswe cet een Meera mci ne iat ai dora een ckie acne ition 389
MUOnveaneliarof mormaltVORs tie: -15% ce cece skh os De hate coat m comrae 389
Be Onteanelia ohjoperatedinpes ys. ee Ogi. oi iis. Ai bee ath Bae Adee 391
1. Winter frogs with spinal cords destroyed................... 391
2. Second lot of frogs—spinal cords destroyed................. 394

3. Third lot of frogs—spinal cords destroyed and sympathetic
CEUTISVCI VAG CGIEAR US Sakaki Aah. skiers ciate eee aoe 397
INES Ulnar ancduconchisionssie sa case ries take Sera ce oinie teeter 400
Wee Diberat Ure Cibedinad teesairancis cls ates ape wate Sei aceehce shane siete aie oeeietal® arecia sreneke 404

INTRODUCTION

The physiological and histological work of J. N. Langley has
lent new interest to the question concerning the occurrence of com-
missural or intrinsic sensory neurones in the sympathetic ganglia.
Langley’s contention against the presence of such neurones is
supported by evidence of a convincing nature. A number of
anatomists, on the other hand, have produced evidence of a
strictly morphological character which stands in opposition to the
results obtained by the author just named. Dogiel’s (’96) descrip-
tion of two types (sensory and motor) of sympathetic nerve cells
‘s well known. Cajal, von Lenhossék, and Huber (Jour. Morph.,
vol. 16, fig. 25, c., and Jour. Comp. Neur., vol. 7, fig. 7,'b)
have reported finding nerve endings in the sympathetic ganglia
which they have regarded as sensory or commissural in nature.

1 Contribution No. 57, February 15, 1918.
385

THE JOURNAL OF COMPARATIVE NEUROLOGY, VOL. 29, NO. 4

386 SYDNEY E. JOHNSON

Michailow has described no fewer than nine varieties of auto-
nomic cells, although he does not specifically state that any one
variety is sensory in character.

The morphological evidence in support of the commi ssural
neurone hypothyses appears, however, to be gradually breaking
down. Autonomic cells of all intermediate stages between the
supposedly sensory and motor types of Dogiel have been reported
by Carpenter and Conel (’14), and these authors have also failed
to differentiate two types of autonomic cells by the Nissl method.

For discussion of Langley’s nicotine and degeneration experi-
ments the reader is referred to Huber (’99, ’13) and Ranson (718),
as well as to Langley’s original papers.

The observations referred to have been made largely on mam-
mals whose sympathetic ganglia are complicated in structure by
the presence of an intercellular plexus of nerve fibers and by the
dendrites of the multipolar autonomic cells. In the frog the
sympathetic ganglia are relatively simple in structure and if, as
Huber and Langley have stated, the structural relations are
fundamentally the same in the autonomic ganglia of all the verte-
brates, this form would appear to be particularly suitable for
disclosing these relations.

The autonomic ganglia of amphibia have been the subject of
many contributions. Ehrlich (86) and Retzius (’89) were
among the first to demonstrate clearly the relations of the spiral
fibers to the neuraxes (straight processes) and to the pericellular
baskets. They believed that the spiral fibers were of cerebro-
spinal origin. Smirnow, Feist, Arnstein, and others held different
views as to the origin and termination of these fibers. (Fora
review of the literature from 1863 to 1896 see Huber, Jour.
Morph., vol. 16.)

Although the belief is now’ generally held that the spiral fibers
and pericellular baskets are of cerebrospinal origin, this has not
been definitely proved on a morphological basis, and it also
remains an open question whether or not nerve endings of any
other type occur in the sympathetic ganglia of amphibia. The
purpose of the experiments reported below was to determine
whether or not all of the spiral fibers and pericellular baskets are

COMMISSURAL NEURONES 387

of cerebrospinal origin and whether or not endings of any other -
type are present.

My thanks are due to Prof. S. Walter Ranson for many cour-
tesies extended during the course of the experiments.

Il. MATERIAL AND METHOD

Material for the observations reported below consisted of three
separate lots of frogs (Rana pipiens), as follows: 1) six dozen
winter frogs received March 20; 2) six dozen frogs received
June 7; and 3) six dozen summer frogs, received September 21,
1917. The first two lots were operated only for destruction of
the spinal cord by reaming the spinal canal with a hot, flat needle
(Huber, Jour. Morph., vol. 16, p. 50), approximately as far
cephalad as the second vertebra. In the frogs of the third lot
the spinal cords were destroyed as just noted and in addition,
in order to eliminate preganglionic fibers which might enter and
run caudally in the sympathetic trunks, from the anterior un-
damaged part of the spinal cord, both sympathetic trunks were
severed between the sixth and the seventh, or the seventh and
the eighth, sympathetic ganglia. This operation was accom-
plished through a small lateral incision just to the side of the
transverse process of the sacral vertebra. Through this open-
ing both trunks were caught with the aid of a hooked needle and
snipped with a pair of fine scissors. The incision was then
sutured, the frog tagged, and a record made of the date of the
operation. On dissection after injection it was found that in two
instances only one trunk had been severed and in one instance
both trunks were still intact. These specimens gave interesting
results, as will be noted later. Aseptic precautions were found to
be unnecessary.

Two staining methods were employed, the intra vitam methyl-
- ene blue process practically as described by Huber (Jour. Morph.,
vol. 16), and the pyridine silver method. In the former it was
found advantageous to use 3 or 4 per cent methylene blue in
Ringer-Locke solution. This was injected into the ventral vein
instead of the lateral vein as described by Huber. For pyridine

SYDNEY E. JOHNSON

388

.

‘ech X ‘antq euatAToWy

“syIOMJou IB[NT[eot1ed puv speatds ur UOT}BUTUTLE} ITO} OF peovsy oq UvO [BIOADG

‘squoineu o1uoT[sues4s0d

JO SOXBANOU SUOTV SpAVMINO OS.IN09 UOIZOI SIT} WO PUB UOT[SULS oy} JO qaed [vajued oy} Joye S1eqy Snued
eyIyM poureys ATYIVp oyL ‘Jory [ewso0U B JO UOT[suLS atyoyyedurks Jo U0Tz00S

jeurpnyisuoyT 7 “aq

COMMISSURAL NEURONES 389

silver preparations sections of the sympathetic trunk were im-
bedded in brain or spinal cord before being immersed in the fixing
fluid.

Every operated specimen was dissected at the end of the de-
generation period in order to determine the condition of the
spinal cord and the sympathetic trunks. Unless otherwise noted,
the spinal cord was completely destroyed as far cephalad as the
second or third vertebra. Both sympathetic trunks were sev-
ered in every specimen except the three referred to above.

III. OBSERVATIONS
A. On ganglia of normal frogs

The conditions found in the sympathetic ganglia of normal frogs
are illustrated in figures 1 to 5. The first three figures represent
methylene blue preparations, and figures 4 and 5 show prepara-
tions stained by the pyridine silver method. Both methods
gave corresponding and uniform results, although the methylene
blue technique was found to be much more convenient and to
show, also, a larger number of spirals and pericellular networks
(especially the latter), for a given area, than could be seen in
pyridine silver preparations. The latter method was used
chiefly as a check against the former.

Figure 1 shows a small section of ganglion at the site of en-
trance of a white ramus communicans. The darkly stained
fibers of the white ramus stand out in marked contrast to all other
nervous elements of the ganglion. A few fibers are seen to divide
and a great many can be traced to their terminations in spirals
and pericellular networks on the neuraxes and bodies of the
autonomic cells. In many methylene blue preparations such
terminations appeared to be present on practically every auto-
nomic cell.

The characteristic relation of fibers to cells is shown in figure 2.
This represents a longitudinal section of a sympathetic ganglion,
and it will be noted that the cells are located near the periphery
cf the ganglion while the nerve fibers form the central part.

390 SYDNEY E. JOHNSON

The neuraxes of the ganglion cells are only faintly stained, never-
theless many can be traced to the central fiber bundle and their
course followed for a considerable distance cephalad or caudad in
the sympathetic trunk. Preganglionic fibers, in many cases,
are seen to accompany neuraxes for a long distance before termi-
nating in spirals and pericellular networks. ‘

Details of structure of the pericellular networks have been
presented by several authors (Huber, ’97, 799), and as this
part of the subject is relatively a side issue I need only say that
my observations on this point, to the extent carried out, are in
accord with those of the author referred to above. Closed net-
works and free endings have been described, but it has been

Fig. 2 Longitudinal section of a ganglion stained with methylene blue.
Note the peripheral position of the cell-bodies and the central location of the nerve
fibers. X 140.

pointed out that one cannot be sure whether the free endings
represent a normal condition or are due to imperfect staining or
to the level of the section. Both free endings and a closed net-
work are shown in figures 4 and 5. It should be noted that the
neuraxes are more prominently stained in the latter than in
methylene blue preparations. That the pericellular networks
are intracapsular can be readily seen in preparations stained by
either method.

The spirals and pericellular baskets described above constitute
the only type of nerve ending that I have been able to find in the
sympathetic ganglia of the frog, either in the normal condition
or after degeneration of the preganglionic fibers.

COMMISSURAL NEURONES 391

B. On ganglia of operated frogs

1. Winter frogs with spinal cords destroyed. A first lot of six
dozen frogs was received on March 20, 1917, and, as the season
was backward, I have regarded these as winter frogs. Forty-two
of the frogs were operated by destruction of the spinal cord to the
second or third vertebra as described above. Thirty-four sur-
vived the operation and were later injected with methylene blue
or their sympathetic ganglia removed and stained by the pyridine

Fig.3 Four autonomic cells and their related spirals and pericellular networks.
In well stained ganglia the pericellular fibrils appear to form closed networks.
Methylene blue. X 546.

silver process. The anterior ganglia were always kept separate
from the posterior ganglia and the results obtained on each com-
pared. Degeneration was allowed to continue from nine to
fifty-four days.

After nine days’ degeneration methylene blue preparations
gave normal histological pictures. No sign of degeneration could
be seen, either in anterior or posterior ganglia. In pyridine
silver preparations, however, evident signs of degeneration were
present in the posterior ganglia. Spirals were less numerous
and many were only faintly stained. Throughout my observa-

392 SYDNEY E. JOHNSON

tions the pyridine silver stain appeared to be more sensitive to
degenerative processes than methylene blue.

Twenty-eight days were allowed to elapse before the next
specimens were injected with methylene blue. These showed a
marked dropping out of pericellular baskets and spirals, especi-
ally in the posterior ganglia. ‘

He

Fig. 4 Autonomic cell of normal frog, stained by pyridine silver method.
> be ®

Fig. 5 Small section of a normal sympathetic ganglion stained by pyridine
silver method. The preganglionic fibers are darkly stained and stand out in
marked contrast to the neuraxes of the autonomic cells. X 1114.

After thirty-three days the ganglia of four specimens were
stained by the pyridine silver process, and all of these showed
marked degeneration in the posterior ganglia. In these many
spirals could be found in the anterior ganglia (fig. 8), and it is
significant to note that the spirals present appeared to be as well
stained as those of normal ganglia. This would appear to indi-
cate that the cells of origin of these particular spiral fibers had
not been destroyed by the operation. Thus these spirals could be

COMMISSURAL NEURONES 393

derived from cerebrospinal fibers entering the sympathetic trunks
at a higher level than that to which the spinal cord was destroyed,
or else endings of commissural neurones with cell bodies located
outside of the spinal cord. In the posterior ganglia of the same
specimens (pyridine silver preparation) no complete spirals have
been observed, although an occasional darkly stained pregan-
glionic fiber could be found. These fibers stand out in sharp con-
trast to the lightly stained postganglionic fibers. A typical
histological picture for the posterior ganglia is shown in figure 9.

Fig. 6 Section of an anterior ganglion of a specimen injected with methylene
blue forty-six days after destruction of the spinal cord. Many spirals can be
found in the anterior ganglia. XX 358.

Fig. 7 From a posterior ganglion of the same specimen (as fig. 6). The

specimens show distinct evidence of degeneration of preganglionic fibers. Meth-
ylene blue. X 358. 3

Pyridine silver preparations made after a degeneration period
of fifty-six days gave histological pictures identical with those
just described.

The remaining frogs were injected with methylene blue after
periods of 46, 48, 54, and 56 days. All of these gave similar
results. Degeneration continued beyond forty-six days did not
appear to affect the results obtained. The anterior ganglia of
all of these specimens show uniformly a large number of spirals
and pericellular baskets. Figure 6 shows a typical section.

394 SYDNEY E. JOHNSON

The posterior ganglia (i.e., the 8th, 9th, or 10th) of the same
specimens showed evident signs of degeneration. In these
there could be seen only an occasional spiral and _ pericellular
basket and a relatively small number of preganglionic fibers.
The neuraxes of the autonomic cells, although faintly stained,
show more prominently as they are not obscured by the’ presence
of the darkly stained preganglionic fibers (fig. 7).

As the experiments described above were carried out on winter
frogs, I was not sure that the time allowed had been sufficient

Fig.8 Small section of an anterior ganglion stained by pyridine silver process
thirty-three days after destruction of spinal cord. <A few spirals could be found
in all the ganglia of the anterior portion of the sympathetic trunk. X 1144.

for complete degeneration of the preganglionic fibers. In order
to remove all doubt on this point, a second lot of frogs was oper-
ated as indicated below.

Second lot of frogs—spinal cords destroyed. ‘This lot of frogs
was received on June 7, and fifty-four were operated in the same
manner as described above. The operated frogs were put into a
large tank and with them was included a small number of normal
frogs for controls. Upon my return to the laboratory after an
absence of three months, I found that all of the frogs had died

COMMISSURAL NEURONES 395

except one operated frog and one normal control specimen.
Both were injected with methylene blue.

The ganglia of the control specimen were well stained and
showed normal histological pictures on sectioning.

Fig. 9 Section of a posterior ganglion from the same specimen (as fig. 8).
Note the absence of spirals. Occasional short sections of darkly stained,
apparently preganglionic, fibers can be seen in these preparations. Pyridine
silver. X 650.

The ganglia of the operated frog were also successfully stained
and showed results which were identical with the results obtained
on frogs of the first lot in which degeneration had continued for
forty-six days or longer. Figure 10 represents a small section
from the fifth or the sixth ganglion of this specimen. In the
more anterior ganglia spirals, baskets, and preganglionic fibers

396 SYDNEY E. JOHNSON

are more in evidence. In the posterior ganglia (9 and 10) no
spirals could be found and only a few broken sections of pregan-
glionie fibers. The spinal cord of this specimen was found to
have been destroyed as far forward as the third vertebra.

This experiment appeared to eliminate the possibility of incom-
plete degeneration, but it also left the origin of a large number of
spiral fibers to be accounted for. Two possibilities presented
themselves: 1) cerebrospinal fibers could still reach the sympa-

Fig. 10 Small section of 5th or 6th ganglion of a specimen injected with
methylene blue three months after destruction of the spinal cord. Many spirals
and pericellular networks were seen in the anterior ganglia of this specimen, but
only a few in the posterior ganglia. X 1144.

thetic trunks through two or three anterior white rami com-
municantes and could pass downward in the trunks, giving off
collaterals to several of the ganglia (Langley and Orbeli, ’11), or
2) they might be the neuraxes or dendrites of commissural neurones
with cell bodies located without the spinal cord.

To exclude the possibility of cerebrospinal fibers reaching
certain of the sympathetic ganglia a double operation was resorted
to with the results reported below.

COMMISSURAL NEURONES 397

3. A third lot of frogs was received on September 21, and fifty-
two were doubly operated, having their spinal cords destroyed and
their sympathetic trunks divided between the seventh and
eighth autonomic ganglia. Thirty-seven survived the operation
and were later stained by one or the other of the two methods
employed. In all but three of the specimens operated in this
manner both sympathetic trunks were severed. The three
specimens referred to (28, 29, 31) will be described separately.

Specimens 1 to 10 of this lot were allowed twenty-eight to
twenty-nine days for degeneration and were then injected with
methylene blue. Specimens 30 to 36 were operated at a later
date, but were allowed about the same length of time (twenty-
seven days) for degeneration. Specimens 11 to 13 were allowed
thirty-six days, and specimens 14 to 29, thirty-one days for degen-
eration. Excepting specimens 28, 29, and 37, the posterior
ganglia of all but the first gave uniform results.

In the posterior ganglia (all mounted on one slide) of the first
specimen, two or three spirals were found, and a few darkly
stained, evidently preganglionic fibers, but no pericellular baskets.

In the posterior ganglia of all the rest there was a striking
and complete dropping out of all spirals and pericellular networks.

The anterior ganglia (1.e., the ganglia of the anterior sections
of the sympathetic trunks) of the same specimens exhibited con-
siderable variation in the number of spirals and pericellular net-
works. In some cases they gave practically normal histological
pictures, in others, only a few spirals and networks could be
found. This variation did not appear to be due to irregularity
of staining and could probably be accounted for by the fact that
the level to which the spinal cord was destroyed varied consider-
ably in different specimens, probably enough to vary the number
of normal white rami joining each sympathetic trunk by one or
two.

Specimen 27 gave results the description and illustration of
which will suffice for all the rest (except 28, 29, 37).

This specimen was operated on October 5, and after an elapse
of thirty-one days was injected with methylene blue. It was found
that the spinal cord had been destroyed to the fourth vertebra,

oe
en ieee

Ce tone

A PO ip.

Rese

Days OA

398 SYDNEY E. JOHNSON

and the sympathetic trunks divided between the seventh and the
eighth ganglia. Immediately after injection both anterior and
posterior sections of the left sympathetic trunk were dissected
out and treated by the pyridine silver process.

Figures 11 and 13 show typical sections of the anterior ganglia
stained by the methylene blue (fig. 11) and the pyridine silver
(fig. 13) method. It should be noted that figure 138 was drawn

‘
, : t
3

om

wwe

arn rere See eT ia

oN

s
ee

Ptah arnanty iit

a Saint te tgs ee

Fig. 11 Section from 5th or 6th ganglion of specimen No. 27. Spirals are
readily found in these sections. This specimen was injected with methylene
blue thirty-one days after section of both sympathetic trunks, between the 7th
and the 8th ganglia of the trunks, and destruction of the spinal cord to the 4th
vertebra. Both sections (i.e., anterior and posterior) of the left sympathetic
trunk were removed and stained by the pyridine silver method (figs. 13 and 14).
x 488.

Fig. 12 Section of a ganglion of the same specimen (No. 27), from posterior
section of the sympathetic trunk. Note total absence of spirals and pericellular
baskets. Methylene blue. X 488.

Fig. 13 From the second ganglion (anterior section) of the left sympathetic
trunk, specimen No. 27. Note the large number of spirals and darkly stained
preganglionic fibers. Pyridine silver. X 488.

Fig. 14. Posterior ganglion of the left trunk of the same specimen (No. 27).
No spirals or networks. Pyridine silver. X 488.

Fig. 15 Interganglionic section of sympathetic trunk showing beaded, ap-
parently degenerating, preganglionic fibers. Methylene blue. X 488.

399

COMMISSURAL NEURONES

Settee pare

Pra S aI,

eee tne Te

400 SYDNEY E. JOHNSON

from the second ganglion of the sympathetic trunk, while figure
11 is from the fifth or sixth.

Figure 12 shows a methylene blue preparation of ganglion nine
or ten (of the same specimen). The autonomic cells and their
neuraxes are faintly stained as in normal ganglia, but there is a
total absence of spirals and pericellular networks. No nerve
endings of any type could be found. ‘

A pyridine silver preparation made from a posterior ganglion of
the left trunk of the same specimen (spec. 27) is shown in figure
14. It supports the results obtained with methylene blue.

Specimens 28, 29, and 37 require a word of explanation.

Dissection, after injection, disclosed the fact that the sympa-
thetic trunks had been divided on one side only in specimens 28
and 29. Spirals and networks were easily demonstrated in the
- ganglia of the trunks which had not been divided, but could not
be found in the posterior ganglia of the divided trunks.

Both sympathetic trunks were missed in specimen 37. The
ganglia were stained, however, and they gave results identical
with the results obtained on the first two lots of frogs in which
the spinal cords only were destroyed, indicating that the devital-
izing effect of the rather severe operation had no detrimental
influence on the staining properties of the nerve terminations.

IV. SUMMARY AND CONCLUSIONS

The results obtained in the three sets of experiments may be
summarized in tabular form as follows:

COMMISSURAL NEURONES 401

i
Ps
Als fa SPIRALS AND | SPIRALS AND
32 DATE OF 04%] sTainiIna | NETWORKSIN | NETWORKS IN ae ee
og OPERATION 209] METHOD ANTERIOR POSTERIOR
By % = Ae GANGLIA GANGLIA

First lot, 72 frogs, received March 20, 1917—42 operated (spinal cords destroyed);
84 survived operation

1} Mar. 29,.1917 9} Meth.-bl.| Many Many Normal _histo-
logical picture
2) Mar. 29, 1917 9| Pyri.-sil. Many Few Evident signs of
degeneration
in the most
posterior
ganglia
Meth.-bl.| Many Several Signs of degen-
eration in the
posterior
ganglia
4| Apr. 5 , 1917 46} Meth.-bl.| Many Few Degeneration
more evident
in posterior
ganglia
5) Apr. 5, 1917 56} Meth.-bl.| ~ Many Few Marked degen-
eration in pos-
terior ganglia
6) Apr. 5, 1917 56| Pyri.-sil. Several Very few | As above
7-10) Apr. 21, 1917 53] Pyri.-sil. Several Very few | As above
11-19} Apr. 21, 1917 |48-54| Meth.-bl.| Several Very few | As above

3} Mar. 29, 1917

bo
(2)

Second lot, 72 frogs, received June 7, 1917—54 operated as described above, all
dying but one during my summer absence of three months

1-54| June 7-14 loz or| 1 frog, Several Few | Marked drop-
more| Meth.-bl. ping out of

| spirals in pos-

| terior ganglia

Third lot, 72 frogs, received Sept. 21, 1917—52 operated (spinal cords destroyed and
and both sympathetic trunks severed unless otherwise noted ); 37 survived
operation

1-10} Sept. 26, 1917 |27-29| Meth.-bl.| Several | A few in| Essentially a

! specimen, complete drop-

1 only ping out of

spirals and

networks in

ganglia poste-

rior to section

of sympathetic
trunks

THE JOURNAL OF COMPARATIVE NEUROLOGY; VOL. 29, No. 4

402 SYDNEY E. JOHNSON

U
a 2
eae & A SPIRALS AND | SPIRALS AND
a8 DATE OF °Z2]| srarnina | NETWORKS IN | NETWORKS IN ies
S a OPERATION a 9 | METHOD ANTERIOR POSTERIOR
Re Aa a GANGLIA GANGLIA

Third lot—Continued

11-13] Sept. 26,1917 36) Meth.-bl.| Several None

14-27) Oct. 5, 1917 31; Meth.-bl.| Several None | Right trunk only
of Spec. 27

28-29! Oct. 5, 1917 31) Meth.-bl. Several | Several in| Dissection
right showed that
trunk,| right trunk
none in had not been

: left | severed

30-36} Oct. 9, 1917 27| Meth.-bl. Several None

27| Oct. 5, 1917 31| Pyri.-sil. Several None _ Left trunk only
37| Oct. 5, 1917 21; Meth.-bl.| Like lots 1 Both trunks
and) 2 missed in op-

above | eration

Destruction of the spinal cord alone (as far cephalad as the
second or third vertebral segment) does not cause degeneration
of all spiral and pericellular endings in the ganglia of the sym-
pathetic trunks, but rather a progressive dropping out of these
elements from the anterior to the posterior ganglia, a large
number of networks appearing in the former and very few or none
in the posterior ganglia.

When all possible routes of entrance of preganglionic fibers to
the sympathetic trunks have been eliminated and sufficient time
allowed for degeneration, there is complete dropping out of all
spiral fibers and pericellular networks. <A few spirals were found
in specimen | (p. 397). These, I think, can be properiy ac-
counted for on the basis of incomplete degeneration, as there
was only the one instance out of a large number of specimens.

Nerve endings of a different origin, if present, should be readily
discovered in those preparations which are well stained and in
which all preganglionic endings have been eliminated by degen-
eration. Such endings have not been found.

The observations presented above appear to me to show con-
clusively, 1) that all of the nerve fibers which end in spirals and

COMMISSURAL NEURONES 403

pericellular baskets in the sympathetic ganglia of the frog are of
cerebrospinal origin (preganglionic fibers), 2) that many of the
spirals and baskets in the posterior ganglia are the endings of
preganglionic fibers which join the sympathetic trunks at a
much higher (more anterior) level (this assumption is necessary
to explain the progressive dropping out of the spirals and net-
works from the anterior to the posterior ganglia after degenera-
tion caused by destruction of the spinal cord); 3) that com-
missural neurones or endings do not occur in the sympathetic
ganglia of the frog.

To what extent the results of the observations reported above
may be applicable to the sympathetic ganglia of higher verte-
brates remains for future investigation to disclose. It has been
asserted that the general scheme (of autonomic relations) is
probably the same in all vertebrates. It is my belief, however,
that this assertion should not be interpreted to exclude com-
missural connections from the sympathetic ganglia of all verte-
brates solely on the basis of findings in the sympathetic ganglia of
Amphibia. Considered, however, in connection with results
obtained on higher vertebrates by Langley, Carpenter and Conel,
Ranson, and others, the evidence here presented appears to me
to afford additional weight to the argument against the om-
missural neurone hypothesis.

404 SYDNEY E. JOHNSON

V. LITERATURE CITED?

Casa, Ramon y 1906 Las ecéllulas del gran simpdtico del hombre adulto.
Trab. del lab. de invest. biol. de la univers. de Madrid, T. 4.

1908 Die Struktur der sensiblen Ganglien des Menschen und der
Thiere. Ergeb. d. Anat. u. Entwick., Bd. 16.

Cannon, W. B. 1912 Peristalsis, segmentation, and the myenteric reflex.
Am. Jour. Physiol., vol. 30. :

CARPENTER, F. W., ano J. L.Conet 1914 A study of ganglion cells in the sym-
pathetic nervous system, with special reference to intrinsic sensory
neurones. Jour. Comp. Neur., vol. 24.

Doatret, A. S. 1986 Zwei Arten sympathischer Nervenzellen. Anat. Anz.,
Bano. 22.

1908 Der Bau der Spinalganglien der Menschen und der Siugethiere.
Jena, 1908.

Enruicu 1886 Uber die Methlenblaureaction der lebenden Nervensubstanz.
Deutsche med. Wochenschrift, Bd. 12, no. 4.

Huser, G. Cart 1913 The morphology of the sympathetic system. XVIIth.
Internat. Congress of Medicine, London.

1899 A contribution on the minute anatomy of the sympathetic
ganglia of the different classes of vertebrates. Jour. Morph., vol. 16.
1897 Lectures on the sympathetic nervous system. Jour. Comp.
Neur., vol. 7.

1896 Spinal ganglia of amphibia. Anat. Anz., Bd. 12.

Lanauey, J. N. 1900 Remarks on the results of degeneration of the upper
thoracic white rami communicantes, chiefly in relatiom to commissural
fibers in the sympathetic system. Jour. of Physiol., vol. 25, pp. 470-
473.

1903 The autonomic nervous system. Brain, vol. 26.

1904 On the question of commissural fibers between nerve-cells having
the same function and situated in the same ganglia, ete. Jour. Phys.,
vol. 31.

Lanatey, J. N. anp L. A. OrsBetr 1911 Some observations on the degeneration

in the sympathetic system and_the sacral autonomic system of am-

phibia, following nerve section. Jour. Phys., vol. 42.

v. LennosséK, M. 1894 Beitriige zur Histologie des Nervensystems und der
Sinnesorgane. Wiesbaden, 1894 (not seen in the original).

Mutter, L. R. 1909 Studien iiber die Anatomie und Histologie des sympath-
ischen Grenzstranges, insbesondere iiber seine Beziehung zu dem
Spinal-Nervensystem. Verhandl. d. Kongresse f. Innere Med., 26
Kkongr., Bergmann.

MicuarLow, Seraius 1911 Der Bau der zentralen sympathischen Ganglien.
Internat. Monat. f. Anat. u. Phys., Bd. 28. |

Rerzius, G. 1889 Zur Kenntniss der Ganglienzellen des Sympathicus. Ver-
handl. d. Biol. Vereins in Stockholm, vol. 2, nos. 1 and 2.

Smrrnow, A. E. 1900 Zur Kenntniss der Morphologie der sympathischen

Ganglienzellen beim Frosche. Anat. Hefte, Bd. 14.

.

?For more extensive bibliographies see Huber (’99, 13) and Ranson (this
number of this Journal).

AUTHOR’S ABSTRACT OF THIS PAPER ISSUED
BY THE BIBLIOGRAPHIC SERVICE, MAY Il

THE THORACIC TRUNCUS SYMPATHICUS, RAMI
COMMUNICANTES AND SPLANCHNIC NERVES
IN, THE ‘CAT

S. W. RANSON anp P. R. BILLINGSLEY
From the Anatomical Laboratory of the Northwestern University Medical School!

NINE FIGURES

In other papers of this series, which appear on the preceding
pages, we have dealt with the cervical portion of the sympathetic
trunk, the superior cervical ganglion, and the branches which it
gives off. We come now to a consideration of the thoracic por-
tion, its rami communicantes and the splanchnic nerves. Our
preparations were obtained from cats because most of Langley’s
observations were made on these animals and we wished to com-
pare our results with his.

The work was started with the hope of throwing some light on
the origin of the various types of fibers in the splanchnic nerves.
Since these fibers are known to belong for the most part to seg-
ments caudad to the fifth thoracic, we began by studying the
rami from the sixth to the thirteenth thoracic nerves and the
corresponding portions of the trunk. It was only after the study
of this material had shown that many significant details con-
cerning this nerve trunk had never been described that we began
the study of it in the first five thoracic segments. Hence the
material representing this part was taken from different cats
than those in which the sixth to the thirteenth thoracic segments
were studied. But in each case a sufficient number of specimens .
was secured to make sure that the peculiarities encountered at
different levels were characteristic for those levels. In all
nearly twenty cats were used, exclusive of those on which opera-
tions were performed to produce the degenerations to be reported
in the following paper.

1 Contribution No. 58, February 15, 1918.
405

406 S. W. RANSON AND P. R. BILLINGSLEY

About half of the material was fixed in osmic acid and the
remainder in ammoniated absolute alcohol for the pyridine
silver stain. The rami communicantes are so small and short
that pyridine silver preparations were made in only a few in-
stances, so that our observations on these are based chiefly on -
osmic acid preparations. For the rest of the work abundant
material was available in which to compare the myelin sheath
and axon content of the various parts of the sympathetic trunk
and the splanchnic nerve.

When small nerves are subjected to the action of the silver
and pyrogallic acid a diffuse precipitate forms throughout the
specimen which renders it useless for microscopic study. In
order to do away with this it is only necessary to subject large
blocks of tissue to the action of the reagents. This can best be
accomplished by imbedding the nerve in the spinal cord. The -
small nerve to be studied is dissected free and a fine silk thread is
tied at either end of the stretch to be removed. With the aid of
a long straight slender needle the thread attached to the end of
the nerve is drawn through a piece of spinal cord and the nerve
drawn in after it. The spinal cord should be prepared before
the nerve is dissected out. The cervical portion of the cat’s cord
freed from dura and split in the median sagittal plane into two
lateral halves makes satisfactory blocks. Each lateral half is
then cut into segments a little longer than the pieces of nerve
to be removed. During these manipulations the nerve and
cord should be protected from drying by the use of normal salt
solution. In drawing the nerve into the cord the needle is run
longitudinally through the anterior gray column and the thread
pulled through until the nerve lies imbedded in the cord. The
segment of the cord is then laid with its lateral convex surface
upon a glass cover-slip and the silk threads attached to either
end of the nerve are tied over the cover-slip so as to put gentle
traction on the nerve. After two hours in ammoniated alcohol
the silk thread can be cut off near the cord, which is then removed
from the cover-slip and pared down with a razor until it forms a
bar, the cross-section of which is not more than 4 mm. square.
This should consist chiefly of the anterior gray column in which
the nerve lies imbedded.

THORACIC TRUNCUS SYMPATHICUS 407

ANATOMY

Truncus sympathicus. In the cat the thoracic portion of the
sympathetic trunk presents an arrangement of its ganglia and
branches somewhat different from that found in man. The
chief differences are in the fusion of the upper thoracic ganglia
to form the ganglion stellatum and in the mode of origin of the
splanchnic nerves. The trunk lies along the sides of the bodies
of the vertebrae ventral to the heads of the ribs, and consists of a
series of ganglia, for the most part segmentally arranged, bound
together by a continuous nerve cord. Each spinal nerve is con-
nected with an adjacent ganglion by a gray ramus. A ganglion
may send a gray ramus to two or more nerves, in which case it
represents a combination of two or more segmental ganglia.
Some compound ganglia are constant in their occurrence, as in
the case of the stellate and the superior cervical ganglia; others
may occur occasionally in any part of the trunk due to the fusion
of two segmental ganglia. Thus the segmental character of the
truncus is indicated by the gray rami, although in some cases
adjacent segments may be fused. The white rami are much more
irregular in their distribution. From all this it will be apparent
that the best method of designating the ganglia is by giving
them the number of the spinal nerve to which they are connected
by their gray ramus. The facts concerning the connections of
the fibers of the gray and white rami, which will be detailed later
in this paper, also bear out this conclusion. Langley (’91 a) has
made use of the same method of designating the ganglia. When
we speak of the twelfth thoracic ganglion we shall have in mind
the ganglion whose gray ramus runs to the twelfth thoracic
nerve, although a glance at figure 1 will show that there are less
than twelve separate ganglia in the thoracic region, and that this
particular ganglion usually receives a white ramus from the
eleventh thoracic nerve. The portion of the continuous nerve
cord which joins two successive ganglia together we shall speak
of as an internodal segment and shall number the successive
segments to correspond to the numbers of the ganglia below which
they lie.

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THORACIC TRUNCUS SYMPATHICUS 409

The ganglion stellatum lies ventral to the first intercostal space
and the angle of the second rib. It receives the gray and white
rami from the first three thoracic nerves and sometimes from the
fourth also. In addition it gives off a gray nerve, the ramus
vertebralis, which follows the vertebral artery and gives off
branches to the lower cervical nerves. According to Langley
(94), it can be traced in the cat as high as the third cervical
nerve. The gray ramus to the eighth cervical nerve may run
by itself. From its connection with the spinal nerves it is obvi-
ous that the stellate ganglion represents a fusion of elements
which in man are found in the middle and inferior cervical and
the first three (and sometimes four) thoracic ganglia. Beginning
with the fourth or fifth thoracic segment, the ganglia are more
regularly arranged. But sometimes a ganglion from which a
gray ramus arises may be very small, and occasionally scattered
ganglion cells or even fairly large ganglionic masses are found
in the internodal segments.

Rami communicantes. While there is a gray ramus for each
spinal nerve the white rami have a more limited distribution.
Gaskell (86) thought that in the dog they were associated
with the second thoracic to the second lumbar nerves only.
But Langley (’92 a) has shown that in the dog, cat, and rabbit,
white rami run from the first thoracic to the fourth lumbar nerves
inclusive. Miller (09) has shown that in man, contrary to the
usual statement, the third and fourth lumbar nerves possess white
rami. The rami communicantes of the first two thoracic nerves
in the cat run directly to the stellate ganglion, those of the third
usually join the trunk a short distance below and ascend in a
common sheath with the trunk to reach this ganglion. The
gray and white rami of the upper two or three thoracic nerves
are commonly fused together, forming one mixed ramus for each
of these nerves. From the fourth to the eighth spinal nerve the

Fig. 1 Diagram of the thoracic portion of the sympathetic trunk in the eat.
Any branches which may run to the pulmonary or aortic plexuses are usually so
fine as to escape notice in a careful dissection carried out with the aid of binocular
lenses of X 2 magnification. In one case we found a branch from the sixth
thoracic ganglion to the pulmonary plexus and one from the tenth to the aorta.

°

410 S. W. RANSON AND P. R. BILLINGSLEY

gray and white rami run close together and join the trunk at the
level of the corresponding ganglion. From the level of the ninth
or tenth thoracic nerve to the fourth lumbar the white rami are
directed caudad and reach the truncus below the level of the
ganglion to which the corresponding gray rami run, often at the
level of the next ganglion below. In some cases a nerve may give
off, in addition to this descending white ramus, a direct one which
accompanies the gray ramus to the segmental ganglion.

A nerve may be connected with the corresponding ganglion by
more than one gray ramus or a nerve may receive gray rami from
two successive ganglia. This is particularly likely to be the
case in the lower thoracic and lumbar regions where, in addition
to the gray ramus from its own segmental ganglion, a nerve may
receive a bundle of unmyelinated fibers from the next more caudal
ganglion, which bundle accompanies the descending white ramus
of the nerve. Langley (’94) has shown that ‘“‘when the white
ramus runs downward to a ganglion, as occurs from the ninth or
tenth thoracic to the fourth or fifth lumbar nerves, the ganglion
may supply pilomotor fibers to the two nerve areas, thus the
fourth lumbar ganglion sends fibers to the fourth lumbar nerve
by its gray ramus, and may also send fibers to the third lumbar
nerve by the white ramus of this nerve.”

Gaskell (86) has shown that when a gray ramus is followed
toward its corresponding spinal nerve it can usually be seen to
give off branches which ramify in the connective tissue overlying
the vertebrae. On these branches accessory ganglia may some-
times be found. In some cases the gray ramus could be seen to
divide on reaching the spinal nerve, part of the fibers passing
centrally, the rest peripherally.

The splanchnic nerves. In the cat the splanchnic fibers leave
the sympathetic trunk in a series of six to ten small nerves.
The first of this series is the largest and corresponds to the greater
splanchnic nerve in man. The level of the trunk at which this
nerve is given off varies. In a total of seventeen dissections it
took origin from the thirteenth thoracic ganglion in six cases,
from the thirteenth internodal segment in three, from the first
lumbar ganglion in four, from the first lumbar internodal

-

THORACIC TRUNCUS SYMPATHICUS 411

segment in three and from the second lumbar ganglion in one.
Since it is well known that fibers of the splanchnic nerve come
from segments as high as the fifth and sixth thoracic, it is obvious
that these fibers must have descended in the sympathetic trunk
to the point of origin of the splanchnic nerve. In man these
same fibers leave the trunk in small bundles from the level of
the fifth or sixth thoracic ganglia downward to the ninth, and
these bundles are then gathered together to form the greater
splanchnic nerve. In the cat other splanchnic nerves are given
off somewhat irregularly from the upper five lumbar ganglia
and internodal segments.

The thoracic rami communicantes. It is not necessary to review
the early literature dealing with the rami communicantes, since
the work of Gaskell (86) may be regarded as the starting point
of modern investigations on this subject. He made a careful
histological examination of the spinal nerves and rami com-
municantes. The gray rami were found to be composed chiefly
of unmyelinated and the white rami chiefly of myelinated fibers.
In the roots of the spinal nerves only myelinated fibers were
found. He argued that, since he found only myelinated fibers in
the roots of the spinal nerves as they left the spinal cord, the
only connection between the spinal cord and sympathetic trunk
must be by way of the myelinated white rami, and that through
them occurred the only possible outflow of visceral efferent fibers
from the spinal cord. The ventral roots of those spinal nerves
which he found associated with white rami, the second thoracic
to the second lumbar inclusive, were seen to contain large num-
bers of fine myelinated fibers like those in the white rami, while
the ventral roots of the other spinal nerves contained very few
such fibers. These he regarded as visceral efferent fibers. <A
gray ramus was found associated with each spinal nerve. On-
reaching the nerve such a ramus was seen to divide, one part
passing centrally, the other peripherally. Most of the unmyelin-
ated fibers which ran centrally were seen to pass into the sheath
of the nerve and become lost in the dense layers of connective
tissue within the intervertebral foramen. Since no unmyelin-
ated fibers could be found in the ventral roots nor in the dorsal

412 S. W. RANSON AND P. R. BILLINGSLEY

roots proximal to the spinal ganglion, Gaskell asserted ‘‘that no
non-medullated nerves leave the central nervous system either
in the posterior or in the anterior roots, any such nerves being in
reality peripheral nerves for the supply of the spinal membranes.”

This was the status of the question when Langley began his
work. In 1892 he said:

It may be regarded as shown that only medullated fibers run from
the spinal cord to the sympathetic chain, and that the white rami con-
tain very many medullated fibers whilst the gray rami contain very few.
The asserted sharp distinction between white and gray rami stands,
however, on a different footing. So far as concerns their histological
characters the difference between them is rather one of degree than of
kind, they both contain medullated fibers of various sizes, and non-
medullated fibers.

On such evidence alone it could not be confidently asserted
that no preganglionic fibers left the cerebrospinal nervous system
by way of the gray rami. This question could best be attacked
by physiological methods, i.e., by stimulating the spinal nerves
within the spinal canal. Langley (’92 a) showed that, while
stimulation of the nerves which were associated with white rami
gave rise to responses in smooth muscles and glands, stimulation
of those which possessed only gray rami produced no noticeable
effect on these structures. He concluded that the myelinated
fibers in the gray rami were either not preganglionic efferent fibers
or were too few to produce any perceptible effect.

Most of Langley’s histological observations were made on
teased nerves, and it has seemed worth while in connection with
the general review of the entire sympathetic nervous system
which is being made in this laboratory to check up his histolog-
ical observations by a careful examination of the rami communi-
cantes of all the spinal nerves in sections stained with osmic
acid. In this paper the rami of only the cervical and thoracic
nerves are considered.

White rami communicantes. The course of the white rami
within the sympathetic trunk will be taken up in connection with
that nerve cord. Our present concern is with the character
of the fibers. The white rami are not always pure, but are often
accompanied by one or more fascicles of unmyelinated fibers

THORACIC TRUNCUS SYMPATHICUS 413

having all the characteristics of small gray rami. Such fascicles
are, however, always sharply defined and do not form a part of
the white ramus proper. These composite rami are especially
frequent in the upper thoracic region where the gray and white
rami are regularly fused. The first two or three thoracic nerves
usually have each a single mixed ramus. Mixed rami are also
not uncommon in the lower thoracic and upper lumbar regions
where the white ramus runs downward.

Osmic acid preparations of the white rami of the cat show that
these contain great numbers of small myelinated fibers with which
are mingled some larger fibers varying in number in the different
rami. In the dog Gaskell found that the small fibers measured
1.8 to 3.6u. He believed that all visceral efferent fibers were of
this size. Langley (’96 a) states that:

In the cat, the medullated fibers of the sympathetic appear to be
somewhat smaller than in the dog. In the dog, I found that most of
the nerve fibers could be classed as belonging to one of three types, viz.,
large fibers about 8 uw in diameter, medium fibers about 5 yu in diameter,
and small fibers about 3 uw in diameter, though all sizes from 2 to 12 u
were present. Inthe cat the corresponding fibers are about 7 uw, 4.5 wand
2.5 u; fibers from 2 to 10 u and occasionally of greater diameter than
10 uw being present.

Our measurements of the medullated fibers in the white rami
of the cat show that the small fibers vary in diameter from 1.5
to 3.5u. Between these two extremes there are fibers of all sizes
and in about equal proportion. There are also fibers of larger
size, but in much smaller proportion. The second thoracic white
ramus contains, however, a great many fibers measuring 4.5 or
5u, as will be seen in figure 2. The larger fibers, which vary in
size from 5 to 13u are not evenly distributed in the white rami
and will be considered more in detail when some of the individual
rami are taken up.

There does not seem to be any reason for grouping the fibers
into three classes as Langley has done. There would be more
reason for making two groups: one less than 4.5y, the other
larger. It is probable that nearly all of the preganglionic efferent
fibers would fall in the first group, but this group would also
contain, as we shall see, some of the smaller sensory fibers. The

414 S. W. RANSON AND P. R. BILLINGSLEY

second group would include the large and medium-sized sensory
fibers.

Are there unmyelinated axons scattered among the myelinated
fibers of the white rami? We must exclude from consideration

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Fig. 2 Second thoracic ramus communicans in the cat consisting of two
fascicles, the larger representing the white and the smaller the gray ramus.
Osmic acid. X 425.

here the bundles of unmyelinated fibers which run as definite
fascicles and represent small gray rami included in the white.
Gaskell (86) found unmyelinated fibers in the white rami and
said that ‘‘there is strong evidence that they arise from the

THORACIC TRUNCUS SYMPATHICUS 415

posterior root ganglia.’’ It is clear from the context that he
believed the spinal ganglia contained autonomic cells and that
the unmyelinated fibers running from these ganglia by way of
the white rami were of the same nature as the unmyelinated
fibers arising from sympathetic ganglia.

We have pyridine silver preparations of the tenth, eleventh,
and twelfth white rami from one cat. While these are not alto-
gether satisfactory, it is possible to see that they contain a con-
siderable number of unmyelinated fibers. In the paper which
follows we shall present evidence to show that these fibers arise
in the spinal ganglia, but we believe that they are to be inter-
preted as afferent, not as postganglionic efferent fibers. If they
belonged to the latter category it would be hard to account for
the negative results of stimulating the splanchnic nerves after
injection of nicotin (p. 436).

There has been some difference of opinion concerning the rami
of the first thoracic nerve. Gaskell (’86) found only a gray ramus
connected with this nerve in the dog. Edgeworth (’92) found
that this ramus in the dog contained unmyelinated, large myelin-
ated, and a few fine myelinated fibers. From this account we
would conclude that there was no clear separation of the fibers
into fascicles representing gray and white rami. Langley (’92 a)
studied the rami of the first thoracie nerve in the cat, dog, and
rabbit, and in every case found the highest white ramus coming
from the first thoracic nerve. In the cat we find the gray and
white rami of the first thoracic nerve united in a mixed ramus in
which they appear as separate fascicles. The white fascicle con-
tains a rather large number of fibers over 6u. It is particularly
in the number of these large fibers that the white rami differ
from one another. In individual white rami the content of large
fibers was found as follows:

First thoracic white ramus, 40 fibers over 6y in diameter, one
of which was much larger than the others and measured 13x.

Second thoracic white ramus, 17 fibers 6u in diameter or larger.
Of these 5 measured 134. There were also a rather large number
of fibers from 4 to 6u in diameter.

416 S. W. RANSON AND P. R. BILLINGSLEY

Third thoracic white ramus, 23 fibers 6u in diameter or larger.
There were no very large fibers like those in the two preceding
rami.

Fourth thoracic white ramus, 10 fibers 6y in diameter or greater.
No very large fibers.

Fifth thoracic white ramus, 24 fibers 6u in diameter or greater,
of these 2 measured 13n.

Sixth thoracic white ramus, 73 fibers 6u in diameter or greater,
the largest of which measured 10x.

Seventh thoracic white ramus, 109 fibers 6u in diameter or
larger. There were no fibers of 10 to 13 diameter.

Eighth thoracic white ramus, 101 fibers 6u in diameter or
greater. None of them very large fibers.

Ninth white ramus, contained 174 large fibers, but many of
them were a little under 6x in diameter.

Tenth white ramus. In this specimen we found a direct ramus
to the tenth thoracic ganglion and a descending ramus to the
eleventh. The direct white ramus contained 130 large fibers,
one of which measured 10u; the descending white ramus in this
case consisted very largely of fibers 6 to 8u in diameter, 106 in
number. The total number of large fibers coming from the tenth
thoracic nerve was thus 236.

Eleventh thoracic white ramus. Here again we found a direct
and a descending white ramus and in both together there were 59
large fibers.

Twelfth thoracic white ramus, 11 large myelinated fibers, of
which the largest was 8x. '

Thirteenth thoracic white ramus, 56 large myelinated fibers.

While these white rami did not all come from a single animal—
the first was from one cat, the second to the fifth from another,
and the sixth to the thirteenth from a third cat—the results
have been checked on a sufficient number of other cats to show
that the larger differences between the rami of the several levels
are significant. The greatest outflow of large fibers occurs
through the seventh to the tenth or eleventh white rami, inclusive.
Figure 3 shows the relatively large number of them in the tenth.

d
THORACIC TRUNCUS SYMPATHICUS 417

There seems also to be a rather large number in the first
thoracic ramus. The upper two thoracic rami are also charac-
terized by the presence of fibers as large as 13, which are usually
absent from the others.

Fig. 3 Tenth thoracic white ramus of the cat with associated gray fascicles.

There was a large separate gray ramus not shown in the figure. Osmic acid.
X 425.

Bidder and Volkman ‘(’42) were the first to consider these
larger fibers as sensory. Langley (’92 a) found difficulty in
correlating the degree of sensitiveness of different parts of the
sympathetic system, as evidenced by the ease with which their
stimulation would produce general reflexes, with the number of

THE JOURNAL OF COMPARATIVE NEUROLOGY, VOL. 29, No. 4

418 sf w. RANSON AND P. R. BILLINGSLEY

large myelinated fibers they contained. He suggested the pos-
sibility that many of the larger fibers mediate some special sense
or subserve special visceral reflexes. ‘Many of them can be traced
to the Pacinian corpuscles (Langley, ’00). Edgeworth (’92)
devoted special attention to the “large-fibered sensory supply
of the thoracic and abdominal viscera” in the dog. According
to him,

It was found that the large medullated sympathetic fibers exist in
the rami communicantes of the nerves from the first dorsal to the third
lumbar inclusive; none were found in the rami aboral to this. The
large sympathetic fibers are found scattered among the other fibers
in the nerve bundles forming the ramus, and not grouped together or
isolated by any septa from the other fibers. In the uppermost dorsal
rami the large sympathetic fibers are fairly plentiful, in the upper and
middorsal rami they are somewhat fewer in number, whilst in the lower
dorsal rami a sudden large increase takes place, which continues as
far as the second lumbar ramus where the outflow practically ceases.
A few however are constantly to be found in the third lumbar ramus—
whilst below this as stated above none are seen.

Edgeworth included among the large fibers those measuring
7.2 to 9u and ignored the even larger number of fibers measuring
less than 7» but still distinctly larger than preganglionic fibers,
so that his results are only in a general way comparable to ours.
He states that the large fibers are as numerous in the gray as in
the white rami. In the cat, as we shall see, they are usually not
present in the gray rami of the cervical and thoracic regions.
Langley (92), working with the cat, found some large fibers, 7.2
uw or upwards, in the gray rami of the lower cervical nerves; in the
white and in the gray ramus of the fourth lumbar nerve, and in the
gray rami of the fifth, sixth, and seventh lumbar nerves. These
were not numerous, but with them were a considerable number of
fibers about 5y in diameter.

It has been assumed that all the large myelinated fibers are
afferent, but are all the visceral afferent fibers large? Added
precision could be given to this question of the myelinated vis-
ceral afferent fibers by the study of the white rami after degen-
eration of the preganglionic fibers resulting from section of the
corresponding spinal nerve roots proximal to the spinal ganglia.
We have examined the white rami of the ninth, tenth, and elev-

THORACIC TRUNCUS SYMPATHICUS 419

enth thoracic nerves after all the preganglionic fibers had been
eliminated. Asis shown in the figure on page 444 of the eleventh
thoracic white ramus, the majority of the fine myelinated fibers
have degenerated, but a considerable number of all sizes remain.
In this particular case the small and medium-sized fibers are more
numerous than the large ones. In some other degenerated
white rami the large ones are relatively more numerous. On
the whole, the sensory fibers of the white rami may be said to be
of all sizes from 1.5 to 8 or 10u, no one size greatly predominating
over the others. In some rami as in the upper thoracic larger
fibers up to 134 may be present.

These sensory myelinated fibers which are found in the white
rami after section of the corresponding nerve roots proximal
to the spinal ganglia take their origin from nerve cells in these
ganglia. In the second paper of this series we have shown that
there was no reason for assuming that there were sensory cells in
the sympathetic ganglia which sent their axons into the dorsal
roots or spinal ganglia (p. 333). Langley has shown that

Section of the inferior splanchnics, the lower lumbar sympathetic
chain, or of a white ramus does not as a rule cause degeneration of any
medullated fibers in the central ends of the nerves. Sometimes a few

degenerated fibers may be followed for a short distance, but these appear
to belong to small gray bundles and to pass off to peripheral tissues.

When we come to the study of the sympathetic trunk we shall
find that while some of the fibers of a white ramus end in the
nearest ganglion, a larger proportion of the fibers run up or down
in the trunk for longer or shorter distances. That is to say, a
white ramus is in no special sense associated with its own seg-
mental ganglion. The gray rami, on the other hand, are in a
_ very special sense the branches of the corresponding ganglia.

Gray rami communicantes. The physiological experiments of
Langley (91 a, 794) on pilomotor, vasomotor, and secretory
fibers show that the majority of these postganglionic fibers take
origin from the cells of that ganglion to which the gray ramus is
attached, but in some cases a minority of the fibers are con-
nected with cells in an immediately adjoining ganglion. On
the histological side this arrangement is indicated by the fact

420 S. W. RANSON AND P. R. BILLINGSLEY

that a gray ramus plunges directly into a ganglion, its fibers being
lost in the fiber complex; while in the case of the white rami it is
easy to see that a large part of the fibers do not enter the ganglion,
but pass along its surface to join the trunk above or below.
While the gray rami are composed in by far the greater part
of unmyelinated fibers, each contains at least a few myelinated
fibers and some contain a very considerable number. Langley
(96 a) has shown that the number of such fibers has been greatly
underestimated. The seventh lumbar gray ramus of the eat -
may contain more than 3800. According to Edgeworth (’92), the
branches from the stellate ganglion to the cervical nerves in the
dog contain a few small myelinated fibers, but no large ones. In
commenting on Edgeworth’s paper Langley (’92) states that he
has always found some large myelinated fibers in the gray rami
of the lower cervical and fourth, fifth, sixth, and seventh lumbar
nerves. The number of small myelinated fibers is in general
proportional to the size of the gray ramus, 1.e., to the number of
unmyelinated fibers it contains (Langley, 96a). He states that
the myelinated fibers range in size from 1.8 to 10u and the varia-
tion in number affects almost entirely the small ones, the most
constant form being the fiber of medium caliber. The number
of myelinated fibers varies considerably in different mammals,
there being many more in the cat than in the rabbit (Langley, ’00).
Miiller (09) demonstrated the presence of myelinated fibers in
the gray rami of man.
In the rami to the first three cervical nerves from the superior
cervical ganglion we found that the number of myelinated fibers
varied greatly in different specimens. Most of these fibers were
less than 3.5u in diameter, although occasionally larger fibers up
to 6 or 7u were found, also in one case a single fiber measuring
10u. We have examined sections of the ramus vertebralis of the
stellate ganglion in one cat and found that it contained about
the same proportion of myelinated fibers as the other gray rami.
There were no fibers as large as 6u. All of the thoracic gray rami
contain a few myelinated fibers. These are for the most part
small, but a few large fibers were found in the upper thoracic
gray rami. We cite some enumerations which may be regarded

THORACIC TRUNCUS SYMPATHICUS 421

as typical. In one cat the sixth thoracic gray ramus contained
one myelinated fiber 6.64 in diameter and three others much
smaller. The seventh was fused with the white ramus, and it
was difficult to be sure which myelinated fibers belong to it. The
eighth contained 3, the ninth 20, the tenth 27, the eleventh 14,
the twelfth 6; and the thirteenth 16, all under 4u in diameter.
What is the function of these myelinated fibers and from what
cells do they arise? Many are postganglionic fibers arising
from the cells of the ganglia of the sympathetic trunk. The
observations to be found in the literature showing that postgan-
glionic fibers in some instances acquire myelin sheaths have been
given qn page 323. As already mentioned, Gaskell showed that
as a gray ramus reaches its spinal nerve it divides into two fas-
cicles, one of which is directed peripherally. This peripheral
branch receives its share of the myelinated fibers. These being
directed toward the periphery can scarcely be other than post-
ganglionic fibers. It is reasonable to suppose that many of those
which turn centrally are of the same nature (Langley, ’92 a).
In 1896 Langley made a careful study of this problem. After
a variety of experimental lesions involving degeneration of fibers
of Various origin in different experiments, he counted and meas-
ured the normal and degenerated fibers in the gray rami of the
lumbar and cervical nerves. We quote his conclusions:

The great majority of these (myelinated) fibers arise from sympa-
thetic nerve cells in the corresponding sympathetic ganglion. In some
cases, but not always, a few arise from sympathetic cells in an adjoining
ganglion. No efferent fibers run from the spinal cord to the sympathetic
by way of the gray rami. In some cases, but not commonly, a few
efferent medullated fibers, passing to the sympathetic by the white
rami, leave the sympathetic by the gray rami. These are to be con-
sidered as fibers on their way to aberrant sympathetic nerve cells lying
in the gray rami before they reach the spinal nerves. The afferent
medullated fibers of the gray rami are of various sizes, 2u, 4u, 6u, and
in some cases 8 to 12u. These are few in number and rapidly diminish
(especially those of more than 4u in diameter) in passing from the lower
lumbar to the coccygeal rami. Most of (these) afferent fibers join the
sympathetic by white rami (only to leave again by the gray), but there
is some evidence that a few, especially the larger ones may run to the
sympathetic by the gray rami.

422 S. W. RANSON AND P. R. BILLINGSLEY

In spite of the presence of a few myelinated sensory fibers in
the gray rami ‘“‘no reflex of any kind has been obtained by stimu-
lating them” (Langley, 00). This may be due to theirsmall
number, or it may be as Langley (92 a) has intimated, to the
fact that these large afferent fibers are not fibers of general
sensibility.

STRUCTURE OF THE THORACIC PORTION OF THE TRUNCUS
SYMPATHICUS

In order to understand the structure of the sympathetic trunk
it is necessary to think of it as a ganglionated nerve which re-
ceives preganglionic myelinated fibers from the various white
rami and through which these fibers are distributed to ganglia
more or less remote from the point where the fibers enter the
trunk (fig. 4). Above the sixth thoracic ganglion the trunks
consist chiefly of ascending preganglionic fibers from the upper
white rami destined to end in the upper thoracic, stellate, and
cervical ganglia. Below the tenth thoracic ganglion it consists
chiefly of descending preganglionic fibers from the lower thoracic
and lumbar white rami to the more caudal ganglia of the trunk
and to the splanchnic nerves. From the sixth to the ninth ganglia
it contains both ascending and descending preganglionic fibers.
The lowest known origin of ascending fibers to the superior cervi-
cal ganglion is from the seventh thoracic white rami and consists
of pilomotor fibers for the face and neck. Fibers ascend to the
stellate ganglion from white rami as low as the ninth. The
highest fibers running to the splanchnic nerve come from the
fifth or possibly the fourth. Fibers from a given white ramus
may be distributed to from five to ten successive ganglia of the
sympathetic trunk, though the branches of an individual pre-
ganglionic nerve fiber would be distributed to a smaller number.
These statements are based on Langley’s (92 a, ’00, 03 a) work
on the cat. In more general terms this distribution of the
fibers of the white rami has been known for many years and
was well stated by Gaskell (’86). According to him, the white
rami from the second to the fifth thoracic nerves, inclusive, in the
dog are directed upward, below the fifth they are directed mainly

10.

Ik

2.

[3.

Fig. 4 Diagram illustrating the course of the fibers from the thoracic white
rami through the sympathetic trunk in the cat. A. The course of the afferent
fibers. B. The course of some of the more important groups of preganglionic
fibers, those terminating in the thoracic ganglia below the stellate are not

indicated.
423

424 S. W. RANSON AND P. R. BILLINGSLEY

TABLE 1

Connections of the spinal nerves with the vertebral ganglia, so far as these supply the skin,
except that of the head and the anogenital region in the cat with an anterior arrange-
ment of the spinal nerves—after Langley-Schafer’s Physiology, vol. 2, p. 634

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downward. This is associated with the course of the fibers
of which they are composed which pass not only into their
segmental ganglia, but also upward into the cervical ganglia,
downward into the lumbar and sacral ganglia and outwards into
the collateral ganglia. Miller (09) has shown that the pregan-
glionic fibers in man havea similar distribution. The connections
of the spinal nerves with the ganglia of the sympathetic trunk so
far as these supply vasomotor, pilomotor, and secretory fibers to
the skin has been worked out in detail by physiological methods
and is expressed in table 1. This shows that these preganglionic
fibers from the nerves above the seventh thoracic are directed
upward from the nerves below the tenth downward and from the
seventh to the tenth, inclusive, both up and down.

With the exception of the cervical and stellate ganglia, which
contain other elements also, the ganglia of the sympathetic
trunk may be regarded as aggregations of postganglionic pilo-
motor, vasomotor, and secretory neurones whose axons are dis-
tributed through the corresponding gray rami and spinal nerves.
As we have stated before, the fibers of a gray ramus arise from
the associated sympathetic ganglion, though a few fibers may

THORACIC TRUNCUS SYMPATHICUS 425

come from the next higher or next lower ganglion. The ganglia
and gray rami are therefore more nearly segmental than the white
rami. As we shall see, few if any postganglionic fibers, arising
in the ganglia of the sympathetic trunk, pass by way of the
splanchnic nerves to the abdominal viscera.

With these facts in mind we are prepared to understand the
observations which follow and which show that the sympathetic
trunk is a well myelinated nerve.

The sympathetic trunk caudad to the sixth thoracic ganglion
has the structure shown in figure 5. It consists like other por-
tions of the thoracic trunk of two fascicles which, though not
sharply separated from each other by connective-tissue septa,
maintain their identity throughout, and in cross-sections of the
stained nerve are easily distinguished from each other because
of their markedly different fiber content. The larger fascicle,
well myelinated, presents in cross-section a round outline and
occupies the greater part of the area of the cross-section. The
other, which makes up but a small part of the area, is composed
almost exclusively of unmyelinated fibers, and is flattened out like
a erescent upon the surface of the larger bundle. For conven-
ience of reference and until its nature is better known we will
speak of this bundle as the crescent. The larger, more rounded,
area will be referred to as the oval.

When followed in serial sections the crescent of unmyelinated
fibers is seen to enter the ganglion at either end of the internodal
segment and become lost in the ganglion. The crescent contains
a very few fine myelinated fibers, and has in fact the structure of a
gray ramus. ‘The fibers of the larger well myelinated bundle, the
oval, run in part into the ganglion at either end of the internodal
segment, but in even larger part pass by along the side of the
ganglion. ‘Every internodal segment of the thoracic sympathetic
trunk presents this separation into two fascicles—and in every
case where serial sections of an internodal segment, including the
ganglia at both ends, were examined the crescent was found to be
continuous from ganglion to ganglion.

The same structure was described as a peripheral fascicle of
unmyelinated fibers in the cervical sympathetic trunk. As

426 S. W. RANSON AND P. R. BILLINGSLEY

the fascicle was followed caudad from the superior cervical
ganglion it was seen to give off very small bundles of fibers which
left the trunk as gray branches, bringing about a gradual reduc-
tion in the size of the fascicle. One set of serial sectioris of the
entire cervical portion of the sympathetic trunk was prepared,

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Fig.5 The sixth thoracic internodal segment of the sympathetic trunk in the
cat. Two fascicles may be recognjzed, one appearing in the cross-section as a
large oval well myelinated field, the other as a crescentic field with few myelinated
fibers. Osmic acid. X 425.

and in this preparation it was found that in tracing the crescent
downward it decreased in size and finally disappeared. It is
obvious, therefore, that in the upper cervical region a fascicle
similar to the crescent consists of postganglionic fibers which
accompany the trunk for a certain distance before being given off

THORACIC TRUNCUS SYMPATHICUS AD

in gray branches. In the thoracic region one cannot often see
this fascicle of the trunk give off branches. It appears rather
to serve as a commissural cord joining two successive ganglia
together.

There are three possibilities concerning the nature of the fibers
of this fascicle: 1. It may consist of commissural fibers arising
from the cells of one ganglion and running to another. Against
this assumption is all the evidence presented by Langley to show
that such commissural neurones do not exist. The most im-
portant evidence in this connection is that based on degeneration
experiments. Langley has shown (’03 b) that after degeneration
of the lower thoracic and lumbar spinal roots, the lower part
of the sympathetic trunk is in the same condition as after injec-
tion of nicotine. Stimulation between the ganglia has either no
effect or only such effect as could be interpreted as due to post-
ganglionic fibers. The literature on this question was con-
sidered at some length in the second paper of this series on page 320.
In the paper by Dr. Johnson this question is again considered,
and what seems to be conclusive evidence is presented that no
commissural fibers exist in the sympathetic trunk of the frog.
In view of these facts, it does not seem probable that the crescent
is composed of commissural fibers.

2. The crescent may consist of fibers belonging to gray rami
which ascend or descend in the trunk for a short distance. From
what has been said about the crescent in the cervical region and ~
from the fact that, as we have already stated, the fibers of a given
gray ramus may come in part from the ganglion next above or
next below, it seems obvious that some at least of the fibers of the
crescent must be of this nature. Since, however, gray ramus
fibers do not ascend or descend in the trunk for more than one
segment and since such fibers are not numerous nor constantly
present, it seems doubtful if they can account for the large number
of fibers constantly present in the crescent.

3. A third possibility is that the crescent is formed by unmyelin-
ated terminal branches of preganglionic fibers. There is some
evidence that these fibers may lose their sheaths before termi-
nating. This evidence has been summarized by Langley (00) as
follows:

428 S. W. RANSON AND P. R. BILLINGSLEY

By the degeneration and by the nicotine method, it can be shown that
in the cat fibers run from the upper lumbar white rami to the sacral
and coceygeal ganglia without passing through nerve cells. In the
rabbit the nicotine method only has been tried; it gives the same results.
We may then conclude that in the rabbit there are preganglionic fibers,
stretching from the upper lumbar white rami to the sacral coccygeal
ganglia. But since the sympathetic in the sacral and coccygeal region
of the rabbit contains very few medullated fibers, it follows that the
preganglionic fibers in this region must be non-medullated, and as they
are medullated in the white rami they must become non-medullated in
passing down the sympathetic chain. In other words, preganglionic
fibers may become non-medullated some distance from their termination
in the vertebral ganglia.

But after all has been said it must be admitted that we are not
in possession of a satisfactory explanation of the bundle of un-
myelinated fibers which we have provisionally called the crescent
and we do not know what the source of its fibers may be.

As seen in figure 5, the myelinated fibers which constitute the
larger oval field are of various sizes. The small fibers 1.5 to 3.5u
in diameter are by far the most numerous. They have the size
and appearance of white rami fibers with somewhat thicker
sheaths than is usual on postganglionic fibers of the same caliber.
The larger fibers are rather conspicuous but are not present in
great numbers. They will be recognized as the large fibers of the
white rami which, as we have seen, take their origin from the
dorsal root ganglia.

Sections stained with osmic acid through successive internodal
segments from the sixth thoracic downward to the origin of the
first splanchnic nerve show no great change in structure. There
is obvious a rather considerable increase in area of the oval myelin-
ated fascicle without any regular increase in the area of the
crescent. The most noticeable feature is, however, the absolute
and relative increase in the number of large myelinated fibers. A
comparison of figures 5 and 6 will show that they are relatively
much more numerous in the eleventh thoracic internodal segment
than in the sixth. And the area of the cross-section at the
eleventh is much greater than at the sixth. This increase in
area is caused by the large number of fibers descending in the
trunk to enter the splanchnic nerves. All of the large fibers of

THORACIC TRUNCUS SYMPATHICUS 429

the lower eight thoracic white rami turn downward toward the
splanchnic nerves, and accumulate in the trunk. It is probable
that many of them branch on their way down. Langley (’00)
states that the large fibers of the sympathetic system occasionally
divide. In this case the branches are of somewhat less diameter
than the parent fibers. He does not state how these observations
were made, but most of his histological observations were made
on teased preparations. As evidence that division of the large

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Fig. 6 A small part of a section of the eleventh thoracic internodal segment
in the cat. Osmic acid. X 425.

fibers occurs in the sympathetic trunk we may mention the results
of the enumeration of the large fibers in the lower thoracic white
rami and in the trunk just above the origin of the first splanchnic
nerve. Only fibers 6u or greater were counted. The total num- :
ber of large fibers in the lower eight thoracic white rami was
864. In the trunk just above the origin of the first splanchnic
nerve there were 464, i.e., a little more than half'as many as in
the rami. Since, as we shall see, all or practically all of- the
large fibers from these rami turn downward in the trunk, and
since none or almost none are given off in any of the other

430 S. W. RANSON AND P. R. BILLINGSLEY

branches of the truncus, and since being sensory fibers, it is not
likely that they terminate in the ganglia, the simplest expla-
nation of these numerical results would be that through branch-
ing about half of them became reduced in size below a diameter
of 6u.

In serial sections of the sympathetic trunk with the white
rami attached it is easy to trace the course of the myelinated
fibers from the latter. In one cat longitudinal serial sections of
the trunk at the level of the entrance of the sixth white ramus
were prepared from osmic acid material, also similar sections of
the trunk at the level of the seventh white ramus. These rami
joined the trunk at the level of the lower end of the corresponding
ganglia and could be seen to divide into two bundles, a smaller
ascending and a larger descending bundle. The majority of the
fibers do not plunge directly into the ganglion, but seem to run by
on its surface. This is especially evident in case of the descending
bundle which can be followed into the trunk below the ganglion.
It is very easy to follow the large medullated fibers and to see that
practically all of these in the sixth and seventh white rami turn
downward past the ganglion into the internodal segment.

An instructive set of preparations was obtained from another
cat in which the seventh thoracic ganglion and the associated
rami were cut into transverse serial sections. The white ramus
on reaching the ganglion divided into two parts: the smaller of the
two joined the myelinated portion of the truncus on the surface
of the ganglion; the other part turned downward in a well-
defined fascicle separated from the ganglion by a connective-
tissue septum and could be traced downard for a considerable
distance along the side of the seventh thoracic internodal seg-
ment before it joined with the trunk. So far as could be de-
termined all the large fibers of this white ramus turned downward
in this fascicle. Such a separate-descending fascicle is of course
atypical, but this ramus serves to indicate in a diagrammatic
way the course taken by the fibers of the white rami on enter-
ing the trunk. Of course the corresponding fibers of the upper
thoracic white rami turn upward instead of downward.

THORACIC TRUNCUS SYMPATHICUS 431

At the point where the first and largest splanchnic nerve
is given off, which is usually near the thirteenth thoracic ganglion,
the size of the trunk becomes abruptly reduced, and it is ob-
vious, when serial sections are studied, that a large part of its
myelinated fibers run into this nerve.

The sympathetic trunk cephalad to the sixth thoracic ganglion
is characterized by the small number of large myelinated fibers
which it contains. The peripheral crescent-like bundle of un-
myelinated fibers is seen here as well as in lower segments and
can be traced continuously from one ganglion into another.
Above the fourth thoracic ganglion the trunk sometimes breaks
up into two or three fascicles which run parallel to one another to

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Fig.7 One of three fascicles composing the sympathetic trunk above the level
of the fourth thoracic ganglion in the cat. Osmic acid. X 425.

reach the stellate ganglion. A cross-section of such a fascicle
just above the level of the fourth thoracic ganglion is seen in
figure 7. The crescent of unmyelinated fibers was joined with
one of the other two fascicles of which the trunk was composed.
The fascicle which is seen in cross-section in figure 7 contained
no bundle of unmyelinated fibers large enough to be recognized
in osmic acid preparations. With the exception of two larger
fibers, it was composed of myelinated fibers of uniformly small
size. The other fascicles of the trunk were also characterized by
the paucity of large and medium-sized myelinated fibers.

432 S. W. RANSON AND P. R. BILLINGSLEY

In studying the white rami we have found reason for believing
that the large and medium-sized fibers of the sympathetic system
are afferent. There are also small myelinated afferent fibers,
but these are not readily distinguished from the preganglionic
efferent fibers. It will be evident from what has been said
that the large and medium-sized myelinated afferent fibers are
present in varying numbers in different parts of the thoracic
sympathetic trunk. Between the stellate ganglion and the
sixth thoracic ganglion they are few in number. Caudal to the
sixth ganglion there is a steady increase in these fibers with the
accession of each successive white ramus until the point of origin
of the greater splanchnic nerve is reached through which nerve
a large part of these fibers run toward the viscera (fig. 4 B).
We shall now see that unmyelinated afferent fibers from the white
rami are distributed in the same way as these myelinated sensory
fibers which we have been studying.

Above the level of the fourth thoracic ganglion there are very
few unmyelinated fibers in the trunk except for the well-defined
bundle which we have referred to as the crescent. The fine
myelinated fibers of which the rest of the cross-section is com-
posed are almost free from an admixture of unmyelinated fibers.
These are also not very numerous in the oval of the seventh
internodal segment. In the lower thoracic segments the oval
well myelinated portion of the section does not consist entirely
of myelinated fibers, but, as is shown in figure 8, it contains also
very large numbers of unmyelinated axons. These are grouped
in small bundles which lie among the myelinated fibers. The
distribution of the three kinds of fibers, large myelinated, small
myelinated, and unmyelinated, is not uniform throughout the
cross-section. The large myelinated fibers are much more nu-
merous in some parts of the field than in others (fig. 5). They also
show a tendency to be arranged in bundles which are separated
from each other by the small myelinated fibers. Now it is in
and about these bundles of large myelinated fibers that the
greatest number of the unmyelinated axons are found. The
grouping of these with the large myelinated sensory fibers sug-
gests that they also may be afferent in function. The data thus

THORACIC TRUNCUS SYMPATHICUS 433

far presented would not exclude the possibility that these unmye-
linated fibers might be preganglionic fibers that had lost their
myelin sheaths, but in the paper which follows we will present
evidence to show that they are afferent fibers and arise from the
cells in the spinal ganglia.

Since there are few large myelinated and unmyelinated fibers

Fig.8 Apart of asection through the tenth thoracic internodal segment in the
cat. Pyridine silver. X 425.

in the sympathetic trunk below the stellate ganglion and prac-
tically none in the cervical part of the trunk, we must conclude
that the sensory fibers which reach the stellate ganglion by way
of the first three white rami run out again through the branches
of the stellate or the inferior cervical ganglion. These branches
have been studied in only one cat. The cardiac branch of the
stellate ganglion, while consisting chiefly of unmyelinated fibers,
contained a somewhat larger number of myelinated fibers than

THE JOURNAL OF COMPARATIVE NEUROLOGY, VOL. 29, No. 4

434 S. W. RANSON AND P. R. BILLINGSLEY

the internal carotid nerve. These were all under 4.54 except
two, which measured 6y. Large myelinated fibers were found
in both limbs of the subclavian ansa which joined to form a single
trunk just below the middle cervical ganglon. <A cardiac
branch given off by the trunk in this position contained a con-
siderable number of fibers between 4.5 and 7u. We counted
forty-eight that measured approximately 6. Aside from the
presence of these larger fibers, this nerve had the same structure
as the cardiac branch of the stellate ganglion. These observa-
tions indicate that the large myelinated fibers pass through the
stellate ganglion, run in both limbs of the ansa, and leave through
the cardiac branch coming from the middle cervical ganglion or
from the ansa subelavia. This is in keeping with the work of
Edgeworth (92), who found that the large myelinated fibers in
the dog could be followed in the stellate ganglion through the ansa
subelavia and middle cervical ganglion, whence they were dis-
tributed to the heart and lungs. This question deserves thor-
ough study. As is indicated in figure 4 B, the sensory fibers
from the lower eight thoracic rami run downward in the trunk
and out through the splanchnic nerve. In the segments Just be-
low the stellate ganglion there are few large myelinated and un-
myelinated sensory fibers, as is indicated in the diagram by the
dotted line.
THE GREATER SPLANCHNIC NERVE

At another time we expect to take up the more detailed con-
sideration of all the splanchnic nerves of the cat, but the present
paper would not be complete without some account of the struc-
ture of the first and largest of the series, the greater splanchnic
nerve. <A study of serial sections through the trunk at the point
of origin of this nerve shows clearly that it is formed by the
separation of a large part of the oval well myelinated fascicle
from the rest of the trunk. The nerve has the same structure
as this oval fascicle and consists of large and small myelinated
and unmyelinated fibers in the same proportion and with the same
arrangement as in that fascicle.

THORACIC TRUNCUS SYMPATHICUS 435

Usually in pyridine silver preparations it is possible to see that
there are somewhat larger accumulations of unmyelinated fibers
near the periphery or directly under the perineurium. These
do not constitute well-defined fascicles such as one would expect
to find if any large number of postganglionic fibers were present.
They are probably of the same nature as those scattered through
the nerve.

In two out of ten normal greater splanchnic nerves examined
we found evidence of postganglionic fibers in the form of a well-
defined and fairly good-sized fascicle composed chiefly of un-
myelinated fibers. Preparations of the first lumbar segment of
the sympathetic trunk and the greater splanchnic nerve taken

xm Ww LG.

G

I.L.Gang.

ILL Gano.
ie NM splaneh.min.

Mspla nch.ma}.

Fig.9 Diagram of the upper lumbar portion of the sympathetic trunk of a cat
in which there was an accessory ganglion at the origin of the greater splanchnic
nerve. XIII. W., white ramus to the XIII thoracic nerve; I. G., gray ramus
to the I lumbar nerve; I. W., white ramus of the I lumbar nerve; II. G., gray
ramus to the II lumbar nerve.

from Cat 8 were especially instructive. Figure 9 shows that in
the first lumbar segment of the trunk there was a ganglion, not
connected with the spinal nerves by rami, located at the point of
origin of the greater splanchnic nerve. The entire portion of the
sympathetic trunk shown in the figure was cut in serial sections.
A study of these sections shows that no branches, even of micro-
scopic size, are given off from the trunk at the level of this gan-
glion except the splanchnic nerve. As this nerve leaves the trunk
it carries with it a rather large bundle of peripherally placed
unmyelinated fibers which closely resembles the crescentic area
described in the trunk. It seems probable that this unusual
bundle of fibers takes origin from the cells in this aberrant
ganglion.

The observations so far recorded lead one to conclude that the
greater splanchnic nerve is composed chiefly of preganglionic

436 S. W. RANSON AND P. R. BILLINGSLEY

autonomic fibers and visceral afferent fibers. In the majority
of the specimens studied (eight out of ten) it was not possible to
demonstrate any group of fibers that could be identified as post-
ganglionic. We shall see that these conclusions agree with those
of Langley. The statements which appear in the citation below
will be found scattered through several pages of text (Schiéfer’s
Physiology, vol. 2, pp. 644, 646, 648):

By dissection, it is easy to see that a large proportion of the splanchni¢
nerve fibers arise from the white rami communicantes, running in the
sympathetic chain for a variable distance. In the cat and dog the fibers
of the great splanchnic nerve can be traced upwards in the sympathetic
chain as far as the sixth thoracic ganglion. And there is good reason
to believe that all the splanchnic fibers are the direct continuation of the
fibers of the white rami. It can easily be shown in the rabbit that the
very great majority of the fibers running from the spinal cord to the
abdominal viscera end in the prevertebral ganglia. After injection of a
small amount of nicotine in the rabbit, the nerve roots, the splanchnies
proper, and the inferior splanchnics have either no effect or a mere trace
on the blood vessels or abdominal and pelvic viscera; but all the normal
effects can be readily obtained by stimulating the fibers given off by the
prevertelral ganglion. It has long been known that the major splanch-
nic contains a considerable number of non-medullated fibers, and it is in
large part this fact which has led to the unquestioned belief that the
ganglia of the sympathetic chain send fibers to the solar ganglia or to
the abdominal viscera. If, then, the view which I have given above be
accepted, namely, that very few if any fibers pass from the cells of the
vertebral ganglia to the splanchnic nerves, we must take the non-
medullated fibers to be preganglionic fibers which have lost their medulla.

According to Langley, the majority of the efferent fibers of
the greater splanchnic terminate in the solar ganglion, though
a few may pass on to more distal ganglia. He also admits the
possibility that occasionally a few postganglionic fibers arising
from cells in the ganglia of the trunk may run through the
splanchnic to the coeliac plexus. The physiological experiments
on which his conclusions are based are found in the papers by
Langley and Dickinson (’89), Langley (’96 b), and Bunch (’97).

It will be seen that our histological results are in agreement
with those obtained by physiological experimentation. We have
seen reason to believe that the unmyelinated fibers in the splanch-
nic which Langley thought might be preganglionic fibers that had
lost their sheaths, are instead afferent fibers. More convincing

THORACIC TRUNCUS SYMPATHICUS 437

evidence on some of these points will be presented in the paper
which follows.
CONCLUSIONS

We shall make no attempt to summarize the detailed observa-
tions presented in the preceding pages, but will merely state a
few general conclusions that seem warranted by the facts already
given.

The segmental character of the sympathetic trunk is evident
in its ganglia and gray rami. The fibers of each gray ramus arise
chiefly, and sometimes exclusively, from the cells of its own seg-
mental ganglion and are distributed through its associated spinal
nerve. When two or more segmental ganglia are fused together
the resulting compound ganglion gives rise to gray rami running
to the corresponding spinal nerves. Except for compound
ganglia like the cervical and stellate, the ganglia of the trunk
are best designated by the number of the spinal nerve with
which their gray rami are associated. The white rami have
a restricted origin from the first thoracic to the fourth lumbar
spinal nerves, inclusive, and their fibers are distributed through
the sympathetic trunk to ganglia at higher and lower levels.
A white ramus is in no special sense associated with its own
segmental ganglion.

The gray rami contain in addition to the unmyelinated also a
few, mostly fine, myelinated fibers. The latter are for the
most part postganglionic. No preganglionic fibers run from the
spinal cord to the sympathetic ganglia by way of these rami.

The white rami consist of myelinated fibers ranging from
1.5 to 13u, though fibers of more than 10u are rare except in the
first two white rami and most of the large fibers have a diameter
of about 6 or 7u. The majority of the myelinated fibers are small,
measuring 1.5 to 3.54. Most of these are preganglionic. The
afferent components include myelinated fibers of all sizes, some
of the very smallest as well as those of medium and large size,
and also unmyelinated axons. The number of the large myelin-
ated fibers varies greatly in the different white rami. They
were found to be most numerous in the seventh to the tenth,

438 S. W. RANSON AND P. R. BILLINGSLEY

from which they run through the sympathetic trunk and the
splanchnic nerves to the viscera.

The sympathetic trunk is to be looked upon as a series of more
or less segmentally arranged ganglia bound together by fibers
frcm the white rami. Above the sixth thoracic ganglion these
fibers are chiefly ascending, below the tenth descending, but
between the sixth and tenth both ascending and descending
fibers are present. In addition to these fibers from the white
rami, which make up the larger part of the cross-section of the
trunk in the form of a large well myelinated oval field, there is
also present throughout the thoracic sympathetic trunk a small
well-defined bundle consisting chiefly of unmyelinated fibers.
This in cross-sections appears flattened out like a crescent against
the larger oval well myelinated field. Some of the fibers in the
crescentic field are postganglionic, ascending or descending to
reach adjacent gray rami. Others may be preganglionic fibers
that have passed through one or more ganglia, giving off collaterals
end losing their myelin sheaths.

In the upper part of the thoracic sympathetic trunk the oval
well myelinated field is composed almost exclusively of fine myelin-
ated preganglionic fibers, with very few large myelinated and
unmyelinated afferent fibers. In the lower thoracic segments
there are in addition to the preganglionic components also affer-
ent fibers, both myelinated and unmyelinated, which increase
steadily in number from the sixth internodal segment toward the
origin of the greater splanchnic nerve.

The greater splanchnic nerve of the cat usually leaves the trunk
at or just below the level of the thirteenth thoracic ganglion.
It is formed by the separation of a large part of the oval well
myelinated fascicle from the rest of the sympathetic trunk and
is composed of fine myelinated preganglionic fibers, destined to
end in the coeliac ganglion, and of both myelinated and unmyelin-
ated afferent fibers. Occasionally it also contains a bundle of
postganglionic fibers arising from cells in ganglia of the sympa-
thetic trunk.

THORACIC TRUNCUS SYMPATHICUS 439

LITERATURE CITED

BippER AND VOLKMAN 1842 Die Selbstiindigkeit des sympathischen Nerven-
systems. Leipzig, 1842.

Buncu, J. L. 1898 On the origin, course and cell-connections of the viscero-
motor nerves of the small intestine. Jour. Physiol., vol. 22, p. 357.

Epagewortn, F. H. 1892 Ona large-fibered sensory supply of the thoracic and
abdominal viscera. Jour. of Physiol., vol. 13, p. 261.

GASKELL, W.H. 1886 On the structure, distribution and function of the nerves
which innervate the visceral and vascular systems. Jour. Physiol.,
volk.7, ps Ie

LANGLEY, J. N., AND Dickinson, W.L. 1889 On the local paralysis of peripheral
ganglia, and on the connection of different classes of nerve fibers with
them. Proc. Roy. Soc. London, vol. 46, p. 423.

Lanetey, J. N. 1891a On the course and connections of the secretory fibers
supplying the sweat glands of the feet of the cat. Jour. of Physiol.,
vol. 12, p. 347.

1891 b Note on the connection with nerve-cells of the vasomotor
nerves for the feet. Jour. of Physiol., vol. 12, p. 375.

1892 a The origin from the spinal cord of the cervical and upper
thoracic sympathetic fibers, with some observations on white and gray
rami communicantes. Phil. Trans. Roy. Soc. London, vol. 183, p. 114.
1892 b On the larger medullated fibers of the sympathetic system.
Jour. of Physiol., vol. 13, p. 786.

1894. The arrangement of the sympathetic nervous system, based
chiefly on observations upon pilo-motor nerves. Jour. of Physiol.,
vol. 15, p. 176.

1896 a Observations on the medullated fibers of the sympathetic
system and chiefly on those of the gray rami communicantes. Jour.
of Physiol., vol. 20, p. 55.

1896 b On the nerve cell connection of the splanchnic nerve fibers.
Jour. of Physiol., vol. 20, p. 223.

1900 The sympathetic and other related systems of nerves. Schiifer’s
Physiology, vol. 2, p. 616.

1903 a The autonomic nervous system. Brain, vol. 26, p. 1.

1903 b Das sympathische und verwandte nervése Systeme der Wir-
beltiere. Ergebn. d. Physiol., vol. 2, p. 818.

Mier, R. L. 1909 Studien tiber die Anatomie und Histologie des sympathi-
schen Grenzstranges, insbesondere iiber seine Beziehungen zu den
spinalen Nervensysteme. 26. Kongr. innere Med., Wiesbaden, p. 658.
Ref.-in Jahres. Anat. u. Entwick., vol. 15, III, p. 731.

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AUTHOR'S ABSTRACT OF THIS PAPER ISSUED
BY THE BIBLIOGRAPHIC SERVICE, MAY ll

AN EXPERIMENTAL ANALYSIS OF THE SYMPATHETIC
TRUNK AND GREATER SPLANCHNIC NERVE
IN THE CAT

S. W. RANSON anv P. R. BILLINGSLEY

Anatomical Laboratory of the Northwestern University Medical School!

TEN FIGURES

A consideration of the facts presented in the preceding paper
makes it clear that much could be learned through the study of
the sympathetic trunk and splanchnic nerves after a variety
of experimental lesions leading to the degeneration of nerve
fibers arising from the spinal cord and spinal ganglia. We have
five experiments to record, and since no two were just alike it
will be best to consider each separately. The operations were
performed under rigid asepsis. The general technique of expos-
ing the spinal cord and nerve roots has been given in another
place (Ranson and v. Hess, 715). After time had been allowed
for degeneration, the lesion was verified at autopsy and the
affected portion of the sympathetic trunk with its rami com-
municantes and the greater splanchnic nerve was removed and
prepared for microscopic examination by fixation in osmic acid
or by the pyridine silver technique. So far as was possible the
material was cut into serial sections. The details of the five
experiments follow.

Cat XI. Died seven days after the left sympathetic trunk was
cut below the ninth thoracic ganglion and the ninth thoracic to
the first lumbar spinal nerve roots cut proximal to the spinal
ganglia as shown in figure 1. Examination of the gray rami of
the tenth, eleventh, and twelfth thoracic nerves, showed that
the few fine myelinated fibers which they normally contain were
not in the process of degeneration. That is to say, these are not

1 Contribution No. 59, February 15, 1918.

441

442 S. W. RANSON AND P, R. BILLINGSLEY

preganglionic efferent fibers coming from the spinal cord (page
421). The white rami of these three nerves showed marked
changes. Most of the small myelinated fibers were undergoing
degeneration, but there were a few which in cross-section appeared
as sharply contoured black rings. These were apparently normal
as were also all of the large myelinated fibers. In the trunk

Fig. 1 Diagram of the thoracic sympathetic trunk with the corresponding
spinal nerves and rami communicantes to illustrate lesions produced in cats IX
and XII. The course of the degenerated fibers is indicated in black. N.S.M. =
N. splanchnicus major.

Fig. 2 Diagram of the thoracic sympathetic trunk with the corresponding
spinal nerves and rami communicantes to illustrate the lesions produced in cat
VII. The course of the degenerated fibers is indicated in black. N.S.M. = N.
splanchnicus major.

above the level of the tenth ganglion, i.e., between the lesion
and the next lower ganglion, the oval field described in the
preceding paper (fig. 5, page 426), was largely degenerated.
Nearly all of the fine myelinated fibers were represented by

ANALYSIS OF THE SYMPATHETIC TRUNK 443

myelin globules, though a very few of them retained a normal
appearance. There was very little degeneration of the large
fibers, and, since the fibers present at this pot must nearly all
have been cut away from their cells of origin, we must interpret
this result as showing that sufficient time had not elapsed for
the degeneratiou of the large fibers. It has been shown by Van
Gehuchten and Molhant (’10) that the speed of degeneration in
myelinated fibers is inversely proportional to their size. In
parts of the crescentic field the scattered fine myelinated fibers
were normal, in other parts of this same field they were all
degenerated.

A cross-section of the trunk below the tenth ganglion showed
most of the scattered fine myelinated fibers in the crescentic
field to be normal in appearance, indicating that few of them took
origin above the cut. The oval field had the same appearance
as in the section described above. The tenth white ramus could
be seen in longitudinal section as it entered the trunk. The
majority of its fine myelinated fibers had their myelin broken up
into globules, giving them a beaded appearance. Its large
fibers and a few of the small ones were normal.

Sections of the greater and lesser splanchnic nerves showed
that most of the fine myelinated fibers were degenerated, while
the large fibers were all or nearly all normal. These results were
confirmed by a study of teased preparations of the twelfth inter-
nodal segment of the trunk and the greater splanchnic nerve.
In these teased preparations it was possible to see that a few
large fibers were also in the early stages of degeneration.

Cat VII, killed thirty-three days after section of the roots of
the left tenth, eleventh, twelfth, and thirteenth thoracic and first
lumbar nerves proximal to the spinal ganglia as indicated in
figure 2.

Sections of the trunk below the entrance of the tenth white
ramus showed a circumscribed area of degeneration at the surface
of the trunk. In this area there were two large and a consider-
able number of small normal myelinated fibers. This degenerated
area was taken to represent the tenth white ramus, although
enough sections were lost from the series at this level to prevent
our tracing that ramus directly into the degenerated area.

444 S. W. RANSON AND P. R. BILLINGSLEY

The white ramus of the eleventh thoracic nerve contained
myelinated fibers of all sizes in about equal proportions. These
were scattered fairly evenly throughout the cross-section and
were separated by a large amount of degenerative material (fig.
3). It was obvious that the preganglionic fibers had degen-
erated as the result of the section of the ventral root. The fibers
which remained were afferent and arose from the cells in the
spinal ganglia. These afferent myelinated fibers were of all

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the preganglionic efferent fibers. All of the remaining fibers are afferent. Osmic
acid. X 425.

sizes, as is shown in the illustration, but as a rule there are rela-
tively more large ones than in this ramus.

In the serial sections the degenerated eleventh white ramus
could be traced into the trunk above the level of the twelfth
thoracic ganglion (fig. 4 a). Here it occupied a position super-
ficial to that occupied by the degenerated fibers from the tenth
(fig. 4b). The rest of the oval field was occupied by large and
small myelinated fibers and was normal in appearance. Only
a small part of this is shown in the illustration.

ANALYSIS OF THE SYMPATHETIC TRUNK 445

A little farther down in the trunk the fibers derived from the
tenth and eleventh white rami formed a single well-defined
bundle which because of the degeneration was easily distinguished
from the normal part of the trunk. This degenerated bundle
could be traced through the trunk beyond the origin of the first
splanchnic nerve. None of the degenerated fibers seemed to go

Fig. 4 From the eleventh thoracic internodal segment of the sympathetic
trunk of cat VII, showing the partially degenerated fascicles derived from a) the
eleventh and b) the tenth white ramus. Osmic acid. X 260.

into the greater splanchnic nerve, which was normal in appear-
ance and seemed to receive all or nearly all of the undegenerated
oval well myelinated portion of the trunk. In this case all of
the fibers of the greater splanchnic nerve came from the white
rami above the tenth. In one instance it received a few fibers
from the tenth white ramus (Cat XIV) in another (Cat XVI) all
of its fibers came from above the ninth.

446 S. W. RANSON AND P. R. BILLINGSLEY

Above the level of the eleventh ganglion there was some evi-
dence of degeneration, and this could be followed up as far as the
tenth. The evidence of an ascending degeneration was, how-
ever, by no means as clear as that for a descending degeneration.

The gray rami of the eleventh, twelfth, and thirteenth thoracic
nerves were normal, containing a few fine myelinated fibers.
No axon stain was made. ‘The white ramus of the tenth nerve
was not well stained, that of the eleventh nerve has already been
described and figured. The twelfth white ramus contained a
fair number of medium and small-sized fibers, but no large ones.
Most of the normal fibers in the thirteenth white ramus were
also of medium and small size. It is clear that in these rami
of this cat the afferent fibers were for the most part of medium
and small size. We regard the paucity of large fibers as some-
what atypical.

The point which stands out most clearly as a result of this
experiment is that the majority of the fibers of the tenth and
eleventh white rami turn downward in the trunk, forming a well-
defined fascicle near its surface which can be traced in the trunk
beyond the origin of. the great splanchnic nerve. At least in the
upper part of this course the fibers from the two rami remain
separate, those from the eleventh lying superficial to those of the
tenth. This lamination of the fibers in the trunk in flattened
bundles, corresponding to the white rami from which they come,
explains why it is easy to follow these fibers by dissection through
the trunk to the splanchnic nerve, as is claimed by Langley
(00).

The degeneration of the preganglionic fibers in the lower
thoracic white rami enables us to isolate the myelinated sensory
fibers and to see that these include fibers of all sizes. These
can be seen not only in the rami themselves, but also in the
degenerated fascicles representing these rami in the trunk.

Cat XII. The sympathetic trunk was cut on the left side at
the level of the ninth internodal segment and the roots of the left
ninth, tenth, eleventh, twelfth, and thirteenth thoracic and first
lumbar nerves were cut proximal to the spinal ganglia, as shown
in figure 1. The cat was killed thirteen days after the operation.

ANALYSIS OF THE SYMPATHETIC TRUNK 447

The gray rami of the tenth, eleventh, twelfth, and thirteenth
thoracic nerves were normal, containing the usual small number
of fine myelinated fibers, except that in the tenth there were four
or five fine fibers which did not appear normal. The white rami of
these nerves were in large part degenerated, although scattered
through each there were a considerable number of myelinated
fibers of all sizes. The proportion of large and small fibers did
not seem to be constant. These undegenerated fibers might, so
far as the data given by this experiment is concerned, have had
their cells of origin in the spinal ganglia or in the ganglia of the
sympathetic trunk. Other experiments will show that the cells
were located in the spinal ganglia.

The part of the trunk including the tenth thoracic ganglion
and internodal segment was fixed in osmic acid and cut into serial
sections. Just below the tenth ganglion all the fibers in the
trunk were degenerated. Many of the larger myelinated fibers
were still seen in process of degeneration. <A little lower down a
very small branch was seen entering the trunk, probably an
accessory white ramus from the tenth nerve, which contained
eleven myelinated fibers chiefly of medium size. These could
be followed down in the trunk as a small compact fascicle for
some distance, but became lost just above the point where the
tenth white ramus entered the trunk, at which point the serial
sections were imperfect, but it probably joined with the fibers
from this ramus as it was not recognizable as a separate fascicle
below the point where this ramus entered. Below the point of
entrance of the tenth white ramus there was a well-defined
fascicle of about the size of the ramus, composed of myelinated
fibers of all sizes rather widely separated from each other. This
fascicle from which the bulk of the fine myelinated fibers had
disappeared could be followed downward at the surface of the
trunk throughout the series of sections which did not include the
entrance of the eleventh ramus.

The twelfth thoracic ganglion and adjacent portions of the
trunk were prepared by the pyridine silver technique. Most of
the fibers in the trunk were degenerated, but the crescent could
be recognized and contained a great many normal fibers, the

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ANALYSIS OF THE SYMPATHETIC TRUNK 449

staining of these fibers was not very satisfactory, however.
On one side of the trunk there was a rather large area containing
scattered normal myelinated fibers, many of which were of large
size. This area represented the contribution of the tenth and
eleventh white rami, and the myelinated fibers in this area were
the afferent fibers from these rami. Among these normal myelin-
ated afferent fibers were considerable numbers of unmyelinated
fibers, also of normal appearance and showing a marked tendency
to arrange themselves in groups, as seen in figure 5.. Through-
out the rest of the trunk all the fibers, both myelinated and unmy-
elinated, were degenerated. The fibers in this completely degen-
erated area had their cells of origin located above the point
of section of the trunk, and from what has already been said in
this and the preceding paper we know that they entered the trunk
by way of the white rami above the tenth. The tenth and
eleventh white rami contributed the fibers found in the area which
is only partly degenerated, and since the roots of the corresponding
spinal nerves were cut proximal to the spinal ganglia the only
normal fibers which these rami could contribute would be afferent
with cell bodies located in the spinal ganglia. We are therefore
justified in interpreting as afferent all the fibers in this area, in-
cluding large and small myelinated and unmyelinated fibers.

We have both osmic acid and pyridine silver preparations of
the greater splanchnic nerve. This was almost completely
degenerated. There was, however, at one side a small group of
normal myelinated fibers. These could be seen in both osmic
acid and pyridine silver preparations. In the latter, as shown in
figure 6, there were also some normal unmyelinated fibers to be
seen iia gldd with the others. The rest of the splanchnic was
completely degenerated except for a very small bundle of unmye-
linated fibers on the other side of the cross-section. In con-
nection with this bundle there were some nerve cells and the
fibers of this group were probably to be regarded as postganglionic,
arising from the cells of a small ganglion in the course of thé
splanchnic. The bundle of myelinated and unmyelinated fibers
was clearly a continuation of a part of that found in the trunk
and illustrated in figure 5.

THE JOURNAL OF COMPARATIVE NEUROLOGY, VOL. 29, No. 4

A450 S. W. RANSON AND P. R. BILLINGSLEY

Serial sections of the trunk including the first lumbar ganglia
and the origin of the second splanchnic nerve, stained with osmic
acid, were examined. In the trunk below the thirteenth thoracic
ganglion and the origin of the greater splanchnic nerve the major-
ity of the fine myelinated fibers had degenerated. There were
present, however, normal myelinated fibers of all sizes rather
widely separated from each other by degenerated material.
These were the afferent fibers of the tenth, eleventh, and twelfth
white rami. The lesser splanchnic had the same structure as the
thirteenth thoracic internodal segment.

Cat XIV. Killed thirty-two days after section of the roots
of the tenth distal, and those of the eleventh thoracic nerve
proximal, to the spinal ganglia (fig. 7). In osmic acid prepara-
tions of the trunk including the tenth, eleventh, and twelfth
thoracic ganglia, the tenth white ramus could be seen entering
the trunk. It contained six or eight normal fine myelinated
fibers, but except for these was completely degenerated. It
could be traced down the trunk as a sharply defined fascicle
occupying a superficial position. In addition to the half-dozen
fine myelinated fibers that could be traced in along with the
tenth ramus this degenerated area became invaded by a few fine
myelinated fibers that worked their way into it from the normal
part of the trunk.

The white ramus of the eleventh nerve could also be traced
into the trunk. It contained a small number of large fibers and
a somewhat greater number of medium-sized and small fibers.
These normal fibers were separated by a considerable amount of
unstained material representing the degenerated preganglionic
fibers. These normal and degenerated fibers of the eleventh
white ramus could be followed down the trunk where they could
be seen to occupy a position adjacent and partially superficial
to the fibers from the tenth ramus.

The bundles from the two degenerated rami presented a marked
contrast. That of the tenth contained only a few fine myelin-
ated fibers, that of the eleventh a much greater number of all
sizes. The latter are easily accounted for as afferent fibers with
their cells of origin in the eleventh thoracic spinal ganglion.

ANALYSIS OF THE SYMPATHETIC TRUNK 451

The half-dozen fine fibers traced from the tenth ramus are more
difficult to understand. It must be admitted that such fibers
are just what one would find if sensory fibers arising in the
sympathetic ganglia pass back along the white rami to end in
the spinal ganglia (p. 333-334). They might also be accounted
for as postganglionic fibers accompanying the white ‘ramus
(p. 412-418).

Fig. 7 Diagram of the thoracic sympathetic trunk with the corresponding
spinal nerves and rami communicantes to illustrate the lesions produced in cat
XIV. N.S.M. = N. splanchnicus major.

Fig. 8 Diagram of the thoracic sympathetic trunk with the corresponding
spinal nerves and rami communicantes to illustrate the lesions produced in cat
XVI. N.S.M. = N. splanchnicus major.

Osmic acid preparations of the greater splanchnic nerve showed
a very restricted area of degeneration, almost the entire nerve
being of normal appearance.

Cat XVI. Killed twenty-two days after section of the roots
of the ninth and tenth thoracic nerves proximal to the spinal
ganglia (fig. 8). The trunk including the ninth, tenth, and

RANSON AND P. R. BILLINGSLEY

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ANALYSIS OF THE SYMPATHETIC TRUNK 453

eleventh thoracic ganglia, stained with osmic acid, was cut into
serial sections. In these it was possible to identify the ninth
white ramus which contained a considerable number of normal
myelinated fibers, of which the greater number were large. The
fibers from this ramus could be followed as a superficial bundle
down the trunk to the point where the tenth ramus entered.
This contained in addition to the degenerated preganglionic fibers
a considerable number of normal myelinated fibers, and of these
there were rather more small than large ones. As each ramus
entered it lay close to the crescentic field of unmyelinated fibers
and the area of the tenth was immediately adjacent to that of the
ninth. A little farther caudad it was no longer possible to sep-
arate the two areas, the two together being spread out over nearly
half the circumference of the trunk as shown in figure 9. In this
figure the degenerated bundles are indicated by the stippled
background. The myelinated fibers in these bundles are affer-
ent, and it will be seen that they are of all sizes and there are about
as many of one size as of another.

Pyridine silver preparations of the twelfth thoracic internodal
segment were especially instructive (fig. 10). The greater part
of the trunk was normal and was characterized by the presence
of great numbers of small myelinated fibers. Large myelinated
and unmyelinated fibers were also in evidence. On one side
there was seen a condensation of the unmyelinated fibers which
represents the crescentic field normally present at all levels of
the thoracic sympathetic trunk. Another area, rather sharply
limited, from which the majority of the fine myelinated fibers
had disappeared, contained myelinated fibers of all sizes in about
equal proportion and also unmyelinated axons. The _ back-
ground presented a peculiar reddish-yellow tone which we have
found characteristic of degenerated fascicles stained by this
method. It is obvious that the fine myelinated fibers had de-
generated and that this is the same fascicle that is seen in figure
9. A comparison of the two figures will show that the areas
occupied by the degenerated fibers have undergone great shrink-
age in passing through the steps of the pyridine silver technique,
and because of this the large myelinated and unmyelinated fibers

RANSON AND P. R. BILLINGSLEY

Si Wo

454

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ANALYSIS OF THE SYMPATHETIC TRUNK 4595

are more closely grouped together in figure 10. Since this
partially degenerated fascicle could be traced to the white rami
of the ninth and tenth thoracic nerves, the roots of which had
been cut proximal to the spinal ganglia, it is clear that the normal
fibers remaining in this fascicle were not preganglionic autonomic
fibers. They must either have been afferent, with their cells
of origin in the spinal ganglia, or they must have been directed
from the sympathetic ganglia toward the spinal ganglia or spinal
cord. The complete degeneration of the greater part of the trunk
at the level of the twelfth thoracic internodal segment after sec-
tion of the trunk below the ninth thoracic ganglion in Cat XII,
as illustrated in figure 5, shows that these fibers do not take origin
from the sympathetic gangha.

The partially degenerated fascicle from the ninth and tenth
white rami made no contribution to the greater splanchnic nerve,
but was continued along the trunk into the lesser splanchnic.
Osmiec acid and silver preparations of the greater splanchnic
showed that this nerve was entirely normal, while similar prepa-
rations of the lesser splanchnic showed that it had the same
structure as the partially degenerated fascicle in the trunk.

SUMMARY

Section of the thoracic spinal nerve roots proximal to the spinal
ganglia results in a degeneration of all of the preganglionic auto-
nomic fibers in the corresponding white rami, but leaves the
afferent fibers intact. The white rami studied were the ninth,
tenth, and eleventh. The fibers from these partially degenerated
rami could be traced caudad in the trunk, those from each ramus
forming a well-defined fascicle. It is this arrangement which
makes it possible to trace the fibers of the splanchnic nerve by
dissection to the white rami as high as the sixth. The afferent
fibers, which alone remained in these partially degenerated rami
and the corresponding fascicles of the trunk, included myelinated
fibers of all sizes and many that were unmyelinated. They
took origin from the cells of the spinal ganglia. In one case after
section of the tenth thoracic nerve distal to the spinal ganglion
we found a half-dozen normal myelinated fibers in the corre-

456 S. W. RANSON AND P. R. BILLINGSLEY

spending white ramus, but these may have belonged to a small
eray ramus accompanying it.

When the sympathetic trunk was cut caudad to the ninth
thoracic ganglion all the fibers degenerated in the oval well
myelinated field in the twelfth thoracic internodal segment,
except in a fascicle derived from the tenth and eleventh white
rami, which entered the trunk caudad to the cut. The fibers
in this oval field, therefore, come from the spinal cord and spinal
ganglia by way of the white rami; at least this experiment proves
that none of them in the twelfth thoracic internodal segment
come from the ganglia of the sympathetic trunk below the ninth,
and under the circumstances there is no reason to suppose that
they might come from those situated farther cephalad. In
this experiment the greater splanchnic nerve was degenerated
except for a small bundle of fibers that could be traced into it
from the fascicle representing the white rami of the tenth and
eleventh nerves, and a very small number of unmyelinated fibers
obviously associated with a small group of ganglion cells located
in the course of the nerve. It is clear that in this case the
splanchnic nerve received no fibers from the ganglia of the sym-
pathetic trunk below the ninth, and there is every reason to
believe that all of its fibers, except those arising from the small
ganglion located in its course, came from the spinal cord and
spinal ganglia (p. 4384-4386). Exclusive of an occasional well-
defined bundle of obviously postganglionic fibers found in two
out of ten normal specimens of the greater splanchnic nerve,
the unmyelinated fibers of this nerve are derived from spinal
ganglia by way of the white rami. The number of rami from
which this nerve may receive fibers seems to vary, but it usually
does not contain any from those below the ninth.

LITERATURE CITED

Lanauey, J. N. 1900 The sympathetic and other related systems of nerves.
Schiifer’s text-book of physiology, vol. 2.

2aNSON, S. W., anp v. Hess, C. L. 1915 The conduction within the spinal
cord of the afferent impulses producing pain and the vasomotor reflexes.
Am. Jour. Physiol., vol. 38, p. 128.

Van GeuucuTen, A., AND Motyant, M. 1910 Les lois de la dégénérescence
wallérienne directe. Le Névraxe, vol. 11, p. 75.

AUTHOR’S ABSTRACT OF THIS PAPER IsSUED
BY THE BIBLIOGRAPHIC SERVICE, JULY 19

THE OLFACTORY ORGANS OF DIPTERA

N. E. McINDOO
Bureau of Entomology, Washington, D. C.

FIFTY-FIVE FIGURES

CONTENTS

introductionrandamethods:. 44ers ses eel ea ese eA chee Sh eh. ae cae 457
PUB eLOMACLOn YA DORCUIN S| pati Mn iil etre Ae S EN 205. sparaiis ind sols olde Seacuehs wpa ble heed 460
Disposition) of pores In MuscandOmestica. .: 2.5002. .ci.c. os ceuie a ous 460

GAME ORESUOMCICES He eae MES Pe eats icla eicleic e Giaie a aisha MM eek aR 460

Gs ORES OnaWwani gs Mayahees eee tise ee kta oak, PAG) DEL 2 em 460
CROTESLONS Hal TERESA tas teeta MMe at wen oy seec Poy 6 Sze orb A Lcenedbeepate oe Steve ike oe 461
Disposition, of pores in. OLHEr SPECIESt...,..5 - ts:<%)0- sey om es ces aee lee hed 463

QP ONES OME LS mmr oe Re ig Se eae Fikes Aied oee eed oie nena ee TAOS
CHORES OUR WEES ty ts 3s As NERS Somes eo ae RIE AL SRLS OO Te le eS 464

ee ores| on haljeres20 shih vdeo SA Foe ALAS de dtd ee <da0 Oe 464
Gmvonresconyapnormaluspecres ane imse e eck chic races er eee: 465

e. Generic, specific, individual, and sexual variations................ 468
Senucture of poressn Musca’ domestica... 22: ..0. Vso. ee ae ek 471

GuaE XGenmalysonWe tures ey aaah eee ahh euc.c icles Bias kd ot eM 471
Daalindernalestructunes: tercsy i creases est hd chauyscia o> oad hoes otekee «teens 473
SLENCCUre. Of Pores In ObMEr SPECIES... cldsckicssis- 00s peaks sees snd saan 478

GUE RIE EN AISEEUeUUNCAee ye ossene ae Hen ass ok eels ovis vid ae ae hatte: 478

Ome imeernel ShrueuUnreye ato. 25% RULES ELL Ne RR 479

Reem bering com SARIN eho AES. V2. epee erm Het alae bat da ck dss « ose eget 481
SUUUTEITIE AS a ed chine oe ae RNR tone Sie Ee Se am 2 Se 482
UT UH STRE ela Ds OUI 0 RR IR US 9 8 I gi 8 aR am HUE oN 484

INTRODUCTION AND METHODS

The results herein recorded are a continuation of the writer’s
investigation concerning the morphology of the olfactory pores.
Up to date, including the present results, these organs have been
carefully studied in Hymenoptera, Coleoptera, Lepidoptera, and
Diptera. The chief object of the present investigation is to
determine whether the olfactory pores are better adapted ana-
tomically than the antennal organs to receive olfactory stimuli.

457

THE JOURNAL OF COMPARATIVE NEUROLOGY, VOL. 29, NO. 5
OCTOBER, 1918

458 N. E. McINDOO

The investigators who have performed experiments on flies
with mutilated antennae have concluded that these appendages
bear the olfactory organs, regardless of whether or not the anten-
nal organs are anatomically fitted to receive olfactory stimuli.
Since these investigators failed to study sufficiently the behavior
of the insects investigated, it is possible that the responses
observed misled them in determining the seat of the olfactory
organs.

In 1857 Hicks discovered porelike organs on the wings and
halteres of flies, and claims that they are similar in structure and
probably have the same function, that of smell. He was able
to trace a nerve to each group of organs, the one going to the
halter being the larger. The same author (’59) found these
organs in Hippobosca equina and Tipula olerocea, and in 1860
discovered them on the legs of various insects, including Diptera.
In the same year Leydig described and figured the same organs
on the halteres of Calliphora (Musca) vomitoria and Eristalis
tenax. Each one of the foregoing authors was able to trace nerves
to these pores, but they could not understand the internal anat-
omy of them.

Graber (’82) described and figured these organs on the wings
and halteres of several Diptera, and called them chordotonal
organs, because he thought the peripheral ends of the sense cells
were sensory chords.

Lee (’85) described and figured in detail these structures on
the halteres of Calliphora vomitoria, but he, like the preceding
authors, failed to understand their internal anatomy.

The paper of Weinland (’90) is the most comprehensive one
dealing with the sense organs found on the halteres, and as a
whole it is the best, although he did not clearly understand the
anatomy of these structures. He gives a good review of the
literature pertaining to the halteres, and according to him the
earliest writers (beginning in 1711) said that these appendages
served in maintaining the equilibrium of the insect while flying;
hence the Latin name, halferes and the English translation,
balanciers. About a century later experiments proved that
flies with amputated halteres could fly, although not as well,

THE OLFACTORY ORGANS OF DIPTERA 459

and consequently the preceding view has long since been aban-
doned. Another old view was that the halteres aid in respiration
Hicks and Lee regarded the structures as olfactory organs, while
Leydig and Graber thought they were auditory in function.
Weinland determined that the halteres in vibrating rapidly
perform a number of different movements, and chiefly for this
reason he thinks that the organs borne by them bring about the
perception of movements, thereby steering the flight of the insect.
He asserts that since the antennae bear the olfactory organs, the
organs on the halteres certainly do not perform the same function.

Nagel (’94), in commenting on the probable function of the
halteres, thinks that the first four preceding views have been
abandoned, but he is a strong advocate of Weinland’s view.

The paper of Prashad (16) seems to be the most recent one
concerning the sense organs on the halteres, and this author
studied only the halteres of the mosquito, Ochlerotatus pseudo-
taeniatus Giles. He evidently did not have access to most of
the literature on this subject and consequently has added little
knowledge concerning these organs. He thinks that each organ
has an external opening’ and found two scalpel groups of pores
on each halter, while the present writer found only one scalpel
group on each halter of mosquitoes belonging to other genera.

McEwen (18) has just recently observed the sense organs on
the wings of Drosophila ampelophila. He determined “that
these organs had nothing to do with the response to light’’ (pp.
85 to 87), but performed no experiments using odor stimuli.

To obtain material for the study of the disposition of the
olfactory pores, dried museum specimens were largely used.
These specimens were obtained of Messrs. C. T. Greene and C. H.
Popenoe through the courtesy of Dr. L. O. Howard. Mr.
Greene is furthermore to be thanked for verifying the identifi-
cation of all the species used. Fresh material was fixed in the
modified Carnoy’s fluid, and was embedded in eelloidin and
paraffin. The sections were cut three and five microns in thick-
ness, and weré stained in Ehrlich’s hematoxylin and eosin. All
the drawings were made by the writer and all are original except
figures 50 to 55; these represent the antennal organs of flies

460 N. E. McINDOO

and mosquitoes, and were copied from Hauser, vom Rath, and
Nagel. The drawings were made at the base of the microscope
with the aid of a camera lucida.

THE OLFACTORY PORES

Before making a study of the anatomy of the organs, called the
olfactory pores by the writer (’14 a), the distribution and number
of them were first investigated.

Disposition of pores in Musca domestica

Owing to an abundance of material and to the economic im-
portance of the house fly, the olfactory pores of this insect have
been studied and drawn in detail, and it is hoped that such work
will encourage experimentation along practical lines.

a. Pores on legs. Seven groups of pores lie on each leg and
the disposition of them is as follows: nos. 1 to 4 on the inner
surface of the leg (fig. 1) and nos. 5 to 7 on the outer surface;
nos. 1, 2, and 5 being on the trochanter, nos. 3 and 6 on the femur,
and nos. 4 and 7 on the tibia. Nos. 1 and 2, consisting of 5 and
8 pores, respectively, always lie on the anterior margin of the leg,
while no. 3, composed of 11 pores, lies on the posterior margin.
Nos. 4 and 7, when present, may lie on either or both margins of
the leg and the number of pores in each group varies from one to
three. No. 5, consisting of 3 pores, usually lies near the poste-
rior margin, while no. 6, composed of 1 pore, lies near the anterior
margin.

b. Pores on wings. Six groups and several scattered pores lie
on each wing and the disposition of them is as follows: Nos. 8 to
11 and scattered pores a to ¢ lie on the dorsal surface of the wing
(fig. 2), while nos. 12 and 13 and the seattered pores d and e lie
on the ventral surface. No. 8, consisting of about 24 pores, lies
at the proximal end of the propterygium (Pr), while nos. 9 to 13
lie on the subcostal (Sc) vein in about the positions as indicated
by the numbers in figure 2. The number of pores‘in each of these
groups varies slightly, but the average number in each is about as
follows: no. 9 has 50 pores; no. 10, 12 pores; no. 11, 10 pores;

THE OLFACTORY ORGANS OF DIPTERA 461

No. 12, 9 pores, and no. 13, 18 pores. The scattered pores vary
considerably in number and position and they are located about
as follows: 1 at a on the base of the humeral vein; 2 always
present at b on the distal end of the first radial vein; 1 at c on the
radiomedial vein; 1 at d on the proximal end of the first radial
vein; and 1 at e on the fourth radial vein.

Fig. 1 Portions of legs of house fly (Musca domestica co”), showing location of
groups nos. 1 to 7 of olfactory pores. The drawings at the right represent the
inner surface and those at the left the outer surface. AntM and PostM stand for
anterior and posterior margins. X 20.

c. Pores on halieres. Five groups and 1 isolated pore lie on the.
base of each halter (fig. 3); nos. 14 to 16 and the isolated pore
at f being found on the dorsal surface and nos. 17 and 18 on the
ventral surface. The pores lie on plates whose outlines are simi-
lar in shape to the contours of the groups of pores themselves;

462 N. E. McINDOO

hence, the pores in nos. 14 and 18 have been called scalpel organs
because each group lies on a plate shaped like a scalpel. No. 15
lies on the basal plate, consequently its pores have been called
basal organs. No. 16 lies on the anterior end of the basal plate,
while no. 17 on the opposite side of the halter lies on the proximal
end of the scalpel plate; the pores in these two groups are like
in structure, and since their structure is like that of those on the
wings they have been called Hicks’ organs. In the following
pages it is shown that the scalpel and basal organs are unlike in
structure and also neither one of these two types is exactly like
the Hicks’ organs. The isolated pore at f is found on only about

Fig.2 Portion of left wing of Musca domestica o’, showing location of groups
nos. 8 to 13 of olfactory pores on propterygium (Pr) and on subcostal vein (Sc) and
the scattered pores at points marked a toe. The drawing at the left represents
the dorsal surface and the one at the right the ventral surface. X 20.

one-half of the halteres of the house fly, and it has been called
an undetermined type by Weinland.

Considering the twenty halteres belonging to five males and
five females, the numbers of pores in the groups are as follows:
In no. 14 they vary from 74 to 110 with 92 as an average; In no.
15, from 70 to 96 with 88 as an average; in no. 16, from 10 to 11
with almost 11 as an average; in no. 17, from 3 to 8 with 7 as an
average, and in no. 18, from 74 to 110 with 93 as an average.

THE OLFACTORY ORGANS OF DIPTERA 463

Disposition of pores in other species

In making a comparative study of the disposition of the ol-
factory pores in Diptera, 47 species, belonging to 38 genera and
representing 21 families, were used. In most cases only one
specimen of each species was employed, and whenever a portion
of an appendage or an entire appendage was missing or was
badly mutilated in being prepared for study, the supposed number

Fig. 3 Right halter of Musca domestica o’, showing location of scalpel pores
(nos. 14 and 18), basal pores (no. 15), Hicks’ pores (nos. 16 and 17) and the unde-
termined type (f). The upper drawing represents the dorsal surface and the
lower one the ventral surface. The upper margin of each drawing represents
the anterior surface and the lower margin the posterior surface. F, one of the
folds caused during preparation of halter. > 100.

of pores on this portion or entire appendage was regarded the
same as the number found on the corresponding portion or entire
appendage on the opposite side of the body. Since the pores on
only one specimen for each species were counted, the total
number of pores recorded cannot be a fair average. Besides
this error, there is also another small probable error for each
species, because a few of the pores were probably overlooked,
and often, as on the tibiae, it was impossible to distinguish the

464 N. E. McINDOO

olfactory pores from hair sockets. As a rule, only the legs, wings,
and halteres were examined, although in several instances the
chitinous parts of the reproductive organs and the mouth parts
were also examined, but usually no olfactory pores were seen
on them. The sex of the species, except in a few cases, was not
determined.

a. Pores on legs. The disposition of the pores on the legs is
more similar to that of those on the legs of Hymenoptera (Mc-
Indoo, ’14 b) than to those on the legs of Lepidoptera or Coleop-
tera (McIndoo, 715, 717). Pores were found on each trochanter
and femur examined, but sometimes none was seen on a tibia and
not one was ever observed on a tarsus. The distribution of them
is similar to that of the house fly, already described. The total
number of them varies considerably, depending on the number of
groups present and the size of the species. The groups are usu-
ally conspicuous and the one on the femur is quite characteristic ;
it consists of two or three rows of pores variously arranged,
depending on the genus examined.

b. Pores on wings. The disposition of the pores on the wings
is more similar to that of those on the wings of Lepidoptera than
to those on the wings of Hymenoptera or Coleoptera. In Lepi-
doptera the pores are well grouped, while in Diptera they are poorly
grouped and consequently not much reliance can be placed upon
the number of groups recorded; for this reason the variation in
the number of groups need not be discussed. Lepidoptera have
more isolated pores than have Diptera, and in the former order
they may extend along the full length of the veins, while in
Diptera they are never found farther than two-thirds the dis-
tance from the base of the wing. The propterygium (fig. 2,
Pr.) was often lost during the preparation of the integument,
but group No. 8, was usually found on it whenever this part of the
wing was present. This is the first time for this group to be
reported.

c. Pores on halteres. As already mentioned on page 462, there
are four types of pores on the halteres, although the undeterminde
type, consisting of large isolated pores, should be called isolated
Hicks’ pores. The groups of Hicks’ pores are seen only with

THE OLFACTORY ORGANS OF DIPTERA 465

much difficulty and doubtless many of them were overlooked.
The writer is the only observer who has seen a group of them on
either side of the halter. Since the number of pores on the hal-
teres has never been tabulated, the following table is presented.
A reference to this table will show the minor variations in these
pores better than a description of them, therefore only the more
important variations need be pointed out. The Hicks’ groups
were found on 75 per cent of the halteres; a basal group on each
halter, except in one species (no. 2); one or two scalpel groups
on each halter; and the undetermined pores on 45 per cent of the
halteres examined. One basal group (excepting no. 2) was
invariably present on each halter, while two scalpel groups were
observed on each halter examined, except in the three mosquitoes
(nos. 3 to 5) and two of the wingless forms (nos. 13 and 48);
only one scalpel group was seen on each halter of these five
species.

d. Pores on abnormal species. To determine what effect en-
vironmental conditions has had upon the disposition of the ol-
factory pores, seven species were selected for this purpose.
Table 3 (p. 470) shows to what families they belong and the
number of their olfactory pores in comparison with the pores of
the normal species. In table 2 they are arranged according to
the degree of degeneracy of the wings and halteres and they shall
be described accordingly.

The sheep tick (45 Melophagus ovinus) is much compressed;
has no signs of wings and halteres; its legs are short and the
segments are wide; the entire integument is thick and tough.
Olfactory pores were found only on the trochanters and femora;
their distribution is normal, but their number is reduced. The
bat tick (48 Nycteribia bellardii) is also much compressed and
has no compound eyes; its wings are totally wanting and its
halteres are unusually small. The disposition of the pores on
its legs is normal, but on the halteres the pores are comparatively
few; the scalpel type being reduced to only one group per halter
(table 1). The so-called wingless female of the snow-fly (2
Chionea valga) copulates on the surface of the snow and it
seems to be abnormal in four ways; 1) The number of pores on

466

N. E. McINDOO

TABLE 1
Number of organs in the four types of olfactery pores found on the halteres of
Diptera
TYPE
*Nos. Nos. Total
NUMBER AND NAMES OF SPECIES 6 hod ty Basal eaoal une
pores
Num-| Num-| Num-} Num-| Num-| Num-
ber of|ber of|ber of|ber of|ber of|ber of|ber of
groups] pores |groups| pores |groups| pores | pores
WAL ipalaso AOE Maa SRT. 8 2 90 | 4 | 1384] 6 | 230
2. ~Chiones, Wal gan Qi icteric Gave 4 26.) 2 28
3. Culex pipienssesets oda ene Dee SOE 2520 | e286
4, Aédes vexans..... Steet UE 2 °'| 156 | 2 1-188} 4° 1298
5. Corethralcinebipes..-..+-. 456s. 2) | LEONE S2F8 1324 eG" e208
6. Mycetophila punctata......... 2 | 158} 4 | 189) 3 | 350
Los claniagnconstanstsee ee ccc 2 1O))| 2) 3 1405) 4 764) AS e380
8. Macrosargus decorus.......... 3 Ad 2s We2i2. |) 42 lnooZn |) laniEeaO
OF Rachydromianspsass dese eee 2 Gnlez 72) 4 | 200) 4 1282
10. Rhamphomyia abdita........ 2 | 152) 4 -|384 536
i SRslopusisp emer cera eee 2 20752) 4 ASs0a a 438 588
12, Aphiochaeta Spe sles oucie fc; 2 65 | 4 | 209| 4 | 278
13. Pulicifora borinquensis @..... 2 64 | 2 72 | 4 | 140
14. Calobata antennipes........... 2 OG 2a 2S |e a2 2 430
15; Biophila; caset:} jys.ss ahacs dete 2 18 | 2 | 140| 4 | 231 389
1G; diritoxa fexage pce. ; Oh ete aar 4 16) 2 65 | 4 | 191 272
17. Anacampta latiuscuta......... + Of) 2) ls 4s e301 |) (Gra lkaso
(SaHuxesta notatasesso ee eee oe eee 2F 82 L450) 4 200 434
19. Dacus cucurbitae.............. 2 14] 2 | 168 | 4..} 332 514
20. Milichiella lacteipennis...... 2 20) 1.426 f 140. | 4) SIT 471
21. Drosophila busckit.:: 324... 3: 2 | 108) 47 180 288
22. Drosophila amoena............ 2 D2 SZ LOO Paes Zi 324
23. Drosophila funebris........... 2 12°) 26 /' 1089), v4y 19286. |e Qe S58
24..Paralimna decipier............. 2 4) 2 96 | 4 | 209 309
25. Paralimna appendiculata...... 2 A 2 P20. 45 e216. cae
26:-Ephydra eracilis:....2.c....---|) 2 1B ee) | LOOT As LOZ SZ sa tsOG
272‘Chilorops coxendixe i.e.) 0.25. 2 74) 4 |:182 256
28: Tetanocera, plumos: 2). 4. .402 + 36 | 2 | 194| 4 | 358 588
2Oe Helomyzaghinet aes saeco 4 222 GON eA lnosO 522
30. Scatophaga stercoraria........ 2 180] 27 150") A 3802 470
3! Seatophaga furcata...0°.05.2.| 4 22) 2) -|) 150'| 4.) 300 472
32. Homalomyia canicularis....... Deis 20) 2) 664 S06 492
30. Eiylemyia simple: yo ety eae 2 24] 2 | 166| 4° | 276 466
SA BE NOLNI a, DEASSICAe wy Een aericr ete 39 | 2 | 144!) 4 | 319 502
35. SPhorbia fussiceps:..:..4......: 2 22) 2° 1140 | 418340 502
SOIC OeENORIAUSD sec hiaes date ae ee cilliee 16 | 2 | 140] 4 | 248 404

THE OLFACTORY ORGANS OF DIPTERA 467

TABLE 1—Continued

TYPE

*Nos. Nos. 33 Total
NUMBER AND NAMES OF SPECIES ene Basal Seealecl 34 anak
Py pores
Num-| Num-| Num-| Num-} Num-} Num-| Num-
ber of|ber of|ber of|ber of|ber of|ber of|ber of
groups} pores |groups| pores |groups} pores | pores
37. Musca domestica o’........... 4 SON LSS! Ih AsealeSes ih en GOOG
38. Musca domestica 9........... 4 Sol te) G6l | 48 lS oOr alee aoe
39. Sarcophaga plinthopyga....... 2 18; )'2) |:140.) 4) le3k6 A74
40. Sarcophaga lambens...........| 2 32 | 2 |168] 4 | 334 534
41. Sarcophaga helicis.............| 4 48} 2 | 186) 4 | 826| 4 | 564
42 warcophaga sp:ss.. 440. 4: Sees SR + 36 | 2 | 146) 4 | 292 474
43. Sarcophaga.sp.....¢.2.... 0048 4 34] 2 | 150] 4 | 334 518
44. Olfersia americana c.....‘....| 2 605) Ame) 2425 | 25 e304
45. Melophagus ovinus 9......... ij
46. Lipoptena depressa o..‘...... 2 LOS ee 68 | 4 | 122 200
47. Hippoboscea struthinionis o...| 2 TGS Zo 120 ra 3045 2 442
48. Nycteribia bellardii o........ 2 6 2 3G) | 2 44°
A eres LO 0) 0 O=) 2) 26) 6-|os—
SVL en nennetetics onan RSet dees 4g| 2 |272| 4 | 552!1 6 | 870

* These numbers refer to those in figure 3, showing the same types on the halteres
of the house fly.
+ Halteres totally wanting.

the legs is slightly more than might be expected; 2) the wing is
nothing more than a little pad, about as long as the base of the
halter, but it bears no pores; 3) the halteres seem normal in size,
but the pores on them are comparatively few in number, the
Hicks’ and basal groups being absent; 4) the ovipositor seems to
bear 21 small.pores, but they are not recorded in the tables.
The chitinous parts of the genital organs of all the abnormal
species and of a few of the normal species were examined, but no
olfactory pores were observed on them except as above stated.
The so-called wingless female phorid (13 Pulicifora borinquensis)
is the smallest specimen examined. The wing is padlike, about
the size of the halter and it bears 7 pores. The number of pores
on the halter appears to be reduced. The deer tick (46 Lipop-
tena depressa) has vestigial wings which are unusually thick

468 N. E. McINDOO

at the base. The number of pores on them is greatly reduced.
The two remaining parasitic species, the fowl tick (44 Olfersia
americana) and the ostrich tick (47 Hippobosca struthinionis),
are winged and apparently are normal, unless one considers the
number of their pores slightly reduced.

TABLE 2
Number of olfactory pores found on abnormal species

NUMBER OF PORES ON Total

NUMBER AND NAME OF SPECIES number of
Legs Wings Halteres pores
45’ Melophagus ovinugs 9. .....24-).5.5.8: 162 A EK 162
48. Nycteribia bellardii o7............... 178 A F44 222
Dimi @hione aval gaso kanes Gere prcleceer 391 B 28 419
13. Pulicifora borinquensis @........... 168 C14 140 322
46. Lipoptena depressa o’............... 144 D75 200 419
44. Olfersia americana o..... Date wera 168 154 304 626
47. Hippobosea struthinionis o’......... 180 167 442 789
NES Tiere Yay Wao Arete EW (RP nek eae { a Ls Lu —
391 167 442 789

The following is an explanation of letters A to F in the above table: A, totally
wingless; B, wing about as long as base of halter; C, wing about size of halter;
D, wing much reduced, about same length as that of the short tarsus; HZ, halteres
totally wanting; and F, halteres unusually small and peduncles threadlike.

e. Generic, specific, individual, and sexual variations. As
already stated, the variations between the olfactory pores of
Hymenoptera, Coleoptera, Lepidoptera, and Diptera are large
and in regard to both disposition and structure of the pores they
are characteristic for each order. The variations among the
families depend upon the families compared; for example, the
disposition of the pores in Tipulidae and Muscidae is very differ-
ent, but in Muscidae and Sarcophagidae only slightly different.
The generic characteristics are slight variations in the disposition
of the pores, while the specific variations are based almost solely
upon the total number of pores present. The individual and
sexual variations are distinguishable only by comparing the total
number of pores present.

A reference to tables 1 and 3 shows that the variations found
pertain to the number of groups on the halteres and to the varia-
tions in number of pores on the legs, wings, and halteres. Exclud-

THE OLFACTORY ORGANS OF DIPTERA 469

ing the wingless forms (nos. 13 and 48), the mosquitoes (nos. 3
to 5) differ from all the other Diptera examined in that each
halter bears only one scalpel group instead of two. While the
legs and wings of these mosquitoes are long and slender, the
halteres are short and stout; relative to the other species exam-
ined, the reverse is generally true. The number of pores on the
halteres of mosquitoes is considerably less than the average
number on the halteres of flies, but they appear to be consid-
erably larger. Tipulidae is the only family which bears more
pores on the legs than on either the wings or halteres. As a
rule, the smaller species bear fewer pores than the larger ones,
but there are many exceptions; for example, Tritoxa flexa (no.
16) is one of the largest specimens examined, yet its total number
of pores is among the lowest recorded. Among the genera the
total number of pores may vary slightly, as in the mosquitoes
(nos. 3 to 5) and in Anthomyidae, or considerably, as in Myce-
tophilidae and Empididae; but among the species the total num-
ber usually varies only slightly, as in nos. 24 and 25, 30 and 31,
34 and 35, but occasionally a larger variation may be found, as in
nos. 21 to 23 and 39 to 43.

The olfactory pores on five females and five males of Musca
domestica were carefully counted to determine the individual
and sexua! variations. For the females the number of pores
on the legs vary from 165 to 175 with 186 as an average; on the
wings, from 219 to 274 with 252 as an average; on the halteres,
from 530 to 570 with 552 as an average. For the males the
number of pores on the legs vary from 168 to 180 with 172 as an
average; on the wings, from 232 to 257 with 248 as an average;
on the halteres, from 564 to 625 with 606 as an average. Thus,
as an average a female bears 972 pores and a male 1026 pores.

The mouth parts and antennae of many specimens were ex-
amined, but no olfactory pores were seen on them. Other
parts of the integuments besides those discussed were also often
examined, although no olfactory pores were found on them,
except on the ovipositor already mentioned (p. 467) and occa-
sionally two or three pores on the thorax near the base of the
wing. These were not carefully recorded and do not appear in
the tables.

470

N. E. McINDOO

TABLE 3

Number of olfactory pores on legs, wings, and halteres of Diptera

FAMILY

Tipulidae......

Culitcidse.23.. &

Stratiomyidae...

Empididae.....
Dolichopodidae. .
Phoridae.......

sl
|
Mycetophilidae. {
:
{

Micropezidae...
Sepsidac? ssh.

Ortalidae.......

Agromyzidae...

Ephydridae....

|
Drosophilidae... |):
[
|

Chloropidae....
Sciomyzidae......
Helomyzidae......

Scatophagidae. .

Anthomyidae...

Muscidae.......

SOON OOP WH Ee

—

NUMBER AND NAME OF SPECIES

SO pula sense epee Seite a aaaene
. Chionea valga 9 Harr...........
PE Culex pipiens Uis.cse sk woyde ote eek
. Aédes vexans Meig................
. Corethra cinctipes Coq..........
. Mycetophila punctata Meig.......
. Sciaria inconstans Fitch.........
. Macrosargus decorus Say........
seRachydromia, spay -nerem asco
. Rhamphomyia abdita Coq.......
SE SILOPUSIND, 426 cA& cit aveeyte aeraee
, Mphiochaeta sp. oe 4. 05 Se
. Pulicifora boringuensis 2 Wheeler
. Calobata antennipes Say.........
~ Biophila cases ae. cients
OW TIPOxXa HeXA WiCGsn. eset: eee
. Anacampta latiuscuta Loew.....
- Huxesta notata, Wied:...@6s.¢e)
.Dacus cucurbitae Coqi.«..% 2)...
. Milichiella lacteipennis Loew.....
. Drosophila busckii Coq...........
22. Drosophila amoena Loew.........
. Drosophila funebris Fabr........
. Paralimna decipier Loew........
. Paralimna appendiculata Loew...
. Ephydra gracilis Pack...........
. Chlorops coxendix Fitch.........
. Tetanocera plumos Loew........
. Helomyza tincta Walk............
. Scatophaga stercoraria L..........
. Scatophaga surcata Say.........
. Homalomyia ecanicularis L.......
- Hylemyia simplarCoq...=55 2 «ssc <
. Phorbia brassicae Bouche........
5. Phorbia fussiceps Zett...........
“Cornosia, Sp... 4. Gh ae
. Musca emeenice a side SA aomeanea
Muscardomestican 2) litas meses.

NUMBER OF PORES
ON

Legs

Total
num-
ber of
Hal- | pores

Wings} teres

252 | 230 | 862
Bt 28 | 419
170 | 286 | 664
192 | 298 | 684
160 | 298 | 678
343 | 350 | 918
138 | 330 | 628
408 | 870 |1550

60 | 282 | 528
192 | 536 | 876
163 | 588 | 919

74 | 278 | 511
C14 | 140 | 322
161 | 430 | 729
154 | 389 | 667
111 | 272 | 478
222 | 485 | 858
184 | 434 | 784
192 | 514 | 888
124 | 471 | 723
98 | 288 | 546
110 | 324 | 607
117 | 358 | 655
138 | 309 | 615
126 | 342 | 641
183 | 306 | 653
138 | 256 | 571
202 | 588 | 964
197 | 522 | 891
214 | 470 | 854
208 | 472 | 853
198 | 492 | 885
241 | 466 | 885
236 | 502 | 912
240 | 502 | 919
223 | 404 | 805
248 | 606 |1026
252 | 552 | 972

THE OLFACTORY ORGANS OF DIPTERA 471

TABLE 3—Continued

NUMBER OF PORES

teres

ON dots
FAMILY NUMBER AND NAME OF SPECIES Lariat
Legs | Wings ats | Pores

39. Sarcophaga plinthopyga Wied.....} 174 | 198 | 474 | 846

40. Sarcophaga lambens Wied..?......| 170 | 204 | 534 | 908

Sarcophagidae.. {| 41. Sarcophaga helicis Towns....‘....| 179 | 218 | 564 | 961
ADE SALE OP NASA SP ces sys woo, succd. siaielack + = 180 | 194 | 474 | 848

eds eSarcophaga: SPs). 5.) y02s a yeSseo ton 186 | 202 | 518 | 906

(| 44. Olfersia americana © Leach...... 168 154 | 304 | 626

Hipnoeectae 45. Melophagus ovinus 9 L.......... 162) |) Avs set, 162
‘* || 46. Lipoptena depressa o Say........| 144 | D75} 200 | 419

|| 47. Hippobosea struthinionis Jansen! 180 | 167 | 442 | 789

Nycteribiidae..... 48. Nycteribia bellardii ~ Rondani..| 178) A | F44 | 222

Variation J 90— 00—| 00—| 162—
Pais Ot ry OA ERC Re ey CaCl ED, Ca Ch 'S Dutt CHOI OH an Se Ee REM eat od \ 391 408 | 871 (1550

* For explanation of letters A to F, see p. 468.

Structure of pores in Musca domestica

The preceding pages deal with the disposition of the olfactory
pores, and now a discussion of their anatomy will be given.

a. Kxternal structure. As already stated, the pores in groups
nos. 16 and 17 on the halteres (fig. 3) have been called Hicks’
organs, and since their structure is like that of those on the legs
and wings, all of these pores may be regarded as belonging to the
Hicks’ type. Since their anatomy does not differ materially
from that of those in the other orders of insects, discussed in
other papers by the writer, a reference to figures 4 to 15 may
suffice at this place. t

Under a high-power lens the scalpel groups (nos. 14 and 18)
and the basal group (no. 15) look somewhat as shown in figures
16 and 17. They may be compared with the Hicks’ type (nos.
16 and 17). It is to be noted that the scalpel group no. 14
consists of 11 rows and no. 18 of 10 rows. From a superficial
view the rows appear to be flat, but sections will show that the
pores are linked together and stand in ridges, projecting far
above the surrounding integument. The summit of each ridge is
beautifully sculptured, and’ a row of stout hairs (fig. 16, Hr')

472 N. E. McINDOO

arises between each two rows of pores. These rows of hairs are
only prolongations of the chitin and therefore should be called
pseudohairs; their only function is probably to protect the rows
of pores. The apertures (PorAp) of the pores are invariably
long, narrow slits, while sculptured markings replace the pore
walls and pore borders in the Hicks’ type. The two halves

| /®
leas | ©©6 / 20
' {@) l vA / 0)
Plat BENET Hip Phigate
oo) OQ © v, @®
! 5 / 0)
SSS EEE Sey @
Oo © @ © @ /Q @ 9 »®
tS eae iy AOE Di ON Midd 6 0
@ © © © oe (6) @
© RSL 6)
2 © Et o 9
Sep Po espe Gers
OHYSY QO -/
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Pee ! 9

Ge © J 0090 9069 0 8

Figs.4to15 External view of olfactory pores in Musca domestica o’, showing
variation in size. Fig. 4, groups nos. 1 and 2 (fig. 1); fig. 5, group no. 3; fig. 6,
group no. 4; fig. 7, group no. 5; fig. 8, group no. 6; fig. 9, group no. 8 (fig. 2); fig.
10, group no. 9; fig. 11, 10 of 12 pores in group no. 10; fig. 12, 9 of 10 pores in group
no. 11; fig. 13, group no. 12; fig. 14, 6 of 18 pores in group no. 13; fig. 15, scattered
pores at b. XX 500.

(PorR), surrounding the aperture, are similar in position to the
pore wall, but do not correspond to it; this structure may be
called the pore ridge. The portion, marked PorL, may be called
the pore link, because it unites the pore ridges; in position it is
similar to the pore border, but it is quite different in structure.
The structure of the basal type of pores is similar to that of the
Hicks’ type, excepting pore borders are not present and a row of

THE OLFACTORY ORGANS OF DIPTERA 473

pseudohairs arises between each two rows of pores. Each basal
group consists of about eight rows of pores which are usually
smaller than the scalpel pores; the pseudohairs in this group
are also smaller than those in the scalpel group. The Hicks’
pores are never protected by pseudohairs.

ND SDSS EE
ISSN WOOL SS ~
SSS SOS SSS

ST ee aN aN eas ee

SO ad

yh, 44
I
Ns YG

Figs. 16 and 17 External view of scalpel pores (nos. 14 and 18), basal pores
(no. 15), Hicks’ pores (nos. 16 and 17), and the undetermined type (f) on base of
right halter of Musca domestica o (fig. 3). All of the pseudohairs (Hr!) in group
no. 15 are represented, but only a few of those in groups nos. 14 and 18 are shown,
the bases of the remainder being represented by black dots. X 500.

b. Internal structure. As in Lepidoptera, the olfactory pores
of Diptera may be called dome-shaped structures. All of the
pores on the legs (fig. 18) and most of those on the wings (fig.
19) are typical dome-shaped structures, while the remainder on
the wings (figs. 20 and 21) and all of those on the halteres (figs.
23 to 27) are modifications of the typical structure. It will be
noted that the internal structure of each type of pore is identical
to that of any other type and it is also similar to that of the

THE JOURNAL OF COMPARATIVE NEUROLOGY, VOL. 29, NO. 5

A7T4 N. E. McINDOO

olfactory pores in other orders of insects; therefore, it is the ex-
ternal structure that really determines the various types.

A hypodermal strand (figs. 23, 26, and 28, HypS), running ~
from the hypodermis (fig. 25, Hyp) to the chitinous cone (fig.
26, Con), is always present. In this strand may be observed the

Figs. 18 to 28 Sections showing internal anatomy of olfactory pores of Musca
domestica. Fig. 18, from trochanter; figs. 19 to 21, 3 variations on wing; fig. 22,
portion of cross-section of wing (X 500); fig. 23, largest Hicks’ pores; fig. 24,
smallest, and fig. 25, largest basal pores, both rows being cut lengthwise; fig.
26, 4 rows of largest scalpel pores cut crosswise and 1 cut lengthwise; fig. 27, a row
of smallest scalpel pores cut lengthwise; and fig. 28, from an oblique section of a
scalpel row of pores, only their external view and nervous connection having been
drawn. The sense fiber (SF) and hypodermal strand (HypS) are taken from a
deeper focus. Attention is called to the sense fiber ending at the center of the
pore aperture. Con, chitinous cone; Hr!, pseudohair; Hyp, hypodermis; N, nerve;
PorAp, pore aperture; PorlL, pore link; PorR, pore ridge; SC, sense cell, and
Tr, trachea. X 1000.

sense fiber (figs. 23, 25, and 28, SF), but it is easily overlooked
owing to the minute size of these organs. The sense cells in the
legs and wings (fig. 22, SC) are spindle-shaped as usual, but in
the halteres (fig. 25, SC) they are more than spindle-shaped
and assume almost a spherical shape (fig. 29, SC). <A pore
aperture (figs. 19 and 26, PorAp) was seen only occasionally

THE OLFACTORY ORGANS OF DIPTERA 475

and then never distinctly; it would never have been regarded as
an opening had not the writer seen many good examples of it in
the olfactory pores of other insects. These pores are the smallest
ones ever examined by the writer, and this fact easily explains
why other observers have never seen the pore apertures. The
sections were studied under a magnification of 1900 diameters,
and with the aid of a camera lucida the drawings made represent
a magnification of 3000 diameters before reduction; and they
were reduced to 1000 diameters.

As already stated, the pores on the legs, wings and groups
nos. 16 and 17 on the halteres belong to the Hicks’ type, while
group no. 15 belongs to the basal type and nos. 14 and 18 to the
scalpel type. A glance at figures 19 to 25 shows that the struc-
ture of the basal type (figs. 24 and 25) is like that of the Hicks’
type (figs. 20 and 23), and the only difference (not shown in these
figures) between these two types is that a row of pseudohairs
(fig. 16) lies between each two rows of pores in the basal group.
Pseudohairs (figs. 19 and 20, Hr!) also protect some of the pores
on the wings, but they are never arranged in rows as they are on
the halteres.

The size of the pores in any type varies considerably. This is
shown by comparing the smallest and largest basal pores (figs.
24 and 25) and the largest and smallest scalpel pores (figs. 26 and
27). The scalpel type differs from the other types in the follow-
ing three particulars: 1) The domes lie totally above the sur-
rounding chitin; 2) the bottoms of the domes are considerably
constricted, while in the basal and Hicks’ types on the halteres
the domes are projected about one-half their height above the
surrounding integument and their bases are constricted little
or not at all, and 3) the tops of the domes are beautifully sculp-
tured and assume a more or less flat surface. One pore (fig. 21)
on the wing, resembling a scalpel pore, was found, while several
(fig. 20) on the wing are identical to those in the Hicks’ and basal
groups on the halteres.

Sections passing longitudinally through the rows of basal pores
show the pores as drawn in figures 25 and 29 (6Por,), while sec-
tions passing transversely through the rows show the pores as

476 N. E. McINDOO

drawn in figure 29 (BPor.). Figure 26 represents a section pass-
ing transversely through four rows and longitudinally through
one row of scalpel pores. In the latter pore, as well as in figures
27, 28, and 29 (SPor:), the pore ridge (PorR) and pore link
(PorL) can be identified. Figure 29 represents an oblique longi-
tudinal section through the base of the halter in the direction. of
AA in figure 3. The large nerve (N) is very conspicuous; it
spreads out fanlike and connects with the masses of sense cells

Fig. 29 Longitudinal section (} diagrammatic), cut in direction of line AA in
figure 3, through base of halter of Musca domestica, showing internal anatomy,
sealpel pores (nos. 14 and 18), basal pores (no. 15) and Hicks’ pores (no. 16).
The chordotonal organ (ChO) is only in its approximate position and was copied
from Lee (’85). One row each of basal pores (BPor,) and scalpel pores (SPor,)
cut lengthwise, and 3 rows of basal pores (BPor:) and 5 rows of scalpel pores (no.
18) were cut crosswise. Ch, internal view of chitin; Ch2, external view of chitin;
M, muscle; N, nerve; SC, sense cell, and Tr, trachea. X 500.

(SC). A trachea (7'r), muscles (/) and a chordotonal organ
(ChO) are also present. Both Lee and Weinland have studied
the chorodotonal organ, but the present writer has paid little
attention to it, hoping later to make a special study of this type
of sense organ. In figure 29 it is represented in only its approxi-
mate position as drawn by Lee.

Figures 30 and 31 are schematic drawings of a portion of a row
in a scalpel group, showing the pores both in perspective and in

THE OLFACTORY ORGANS OF DIPTERA 477

section. In figure 30 the row was cut crosswise, passing longi-
tudinally through the shtlike aperture, whereas in figure 31 the
row was cut lengthwise, passing transversely through the slitlike
aperture.

Figure 32 is a drawing, showing a portion of the base of the
halter in perspective and in section, it was cut crosswise in the
direction of line BB in figure 3. The muscle (MV) and chordotonal
organ (ChO) are drawn in only their approximate positions as
represented by Weinland; their points of attachments are incor-
rect. The scalpel pores (nos. 14 and 18) and a few basal
pores (no. 15), shown both in perspective and in section, lie on

Figs. 30 and 31 Schematic drawings of a portion of a scalpel row on halter of
Musca domestica, showing the row in perspective and in section. In figure 30,
the row was cut crosswise, longitudinally through the slitlike aperture, while in
figure 31 the row was cut lengthwise. Thenerve (N) is drawnin perspective, and
gtrong pseudohairs (Hr!) bend over the pores, protecting them well.

curved plates, and it is noted that the surface of the base of the
halter is very rough, being made up of minute hills and hollows.

In Weinland’s drawings it is noted that the nerve does not run
beyond the olfactory pores on the halter, but the trachea runs
into the peduncle and stops there. <A cross-section of the knob
of a halter somewhat resembles a double convex lens; it contains
masses of cells which are certainly not sensory, but probably they
are the remains of the early hypodermis. The surfaces of the
knobs of prepared halteres bear a few true hairs, and they are
generally smooth excepting the folds (fig. 3, 7), caused by pre-
paring the specimens.

478 N. E. McINDOO

Structure of pores in other species

Since the structure of the pores in the house fly has been de-
seribed in detail, only the more important variations concerning
the structure of the pores in other Diptera will be mentioned
and attention will be called to the various figures.

a. External structure. On the legs of one or two specimens the
pore walls are diamond-shaped instead of being round and oblong,

Fig. 32 Portion of base of right halter of Musca domestica, cut across in direc-
tion of line BB in figure 3, showing halter, scalpel pores (nos. 14 and 18), and@&
basal pores (no. 15) in perspective and in section. The chordotonal organ (ChO)
and muscle (7) were copied from Weinland (’90) and were drawn in only their
approximate positions.

and the pore apertures in several instances are long, more or less
slit-shaped, and resemble the slits in the lyriform organs of
spiders (MecIndoo, ’11); such is particularly true on the tro-
chanters of Tipula (fig. 33). The pores on the tibiae of Sarco-
phaga (fig. 34) are very large and striking. The pore wall is
surrounded by three areas of differently colored chitin; the inner
one is real light in color; the middle one is a little darker, and
the outer one, having a soft appearance, is still darker.

THE OLFACTORY ORGANS OF DIPTERA 479

b. Internal structure. A reference to figures 35 to 49 shows
that the size of the pores usually varies according to the size
of the insect studied; thus the average size of the pores in the
robber fly (figs. 39 to 43) is greater than that of the pores in the
flesh fly (figs. 44 to 49), although the pores on the halters of
both flies are about equal in size. While the pores on the legs
are always dome-shaped, many of those on the wings (figs. 42
and 46) and a few on the halteres (fig. 47) are not dome-shaped.
Many of those on the wings (fig. 45) of Sarcophaga project far
above the surrounding chitin and their tops slightly resemble
those of the scalpel pores on the halteres. A study of these pores
shows a complete series of variations, ranging from the Hicks’
type to the scalpel type, and perhaps each type is still in the trans-

Figs. 33 and 34 External views of olfactory pores of other flies. Fig. 33, a
group from trochanter of Tipula, showing slitlike pore apertures, and fig. 34, a
group from tibia of Sarcophaga plinthopyga, showing 3 areas of chitin around pore
wall. X 500.

itional stage. . Morphologically the scalpel type is the most highly
developed, but physiologically it is probably little or no better
developed than any other type of pores. -

All of these results indicate that while the hind wings of
Diptera have been gradually reduced in size, consequently
gradually diminishing their flying ability, their sensory function
has been greatly increased, and now they bear the highest type
of olfactory pore yet found. The latter statement is supported
by the fact that in Hymenoptera, the hind wings bear about one-
half as many pores as do the front wings; in Lepidoptera’ the
hind wings do not bear quite as many pores as do the front
wings, while in Diptera the halteres bear about as many pores as
do the wings and legs combined, or close to one-half the total
number of pores found.

480 N. E. McINDOO

Figs. 35 to 49 Sections showing variations in internal anatomy of olfactory
pores of other flies. Figs. 35 to 38, from crane fly (Brachypremna dispellens
Walk.); fig. 35, from trochanter; fig. 36, from wing; and figs. 37 and 38, from
halter, fig. 37 being basal type and fig. 38 being scalpel type. Figs. 39 to 48, from
robber fly (Erax «stuans L.); fig. 39, from trochanter; fig. 40, from femur; figs.
41 and 42, from wing, and fig. 48, scalpel type from halter. Figs. 44 to 49, from
flesh fly (Sarcophaga sp.); fig. 44, from trochanter; figs. 45 and 46, from wing,
and figs. 47 to 49, from halter. > 1000.

THE OLFACTORY ORGANS OF DIPTERA 481

THE ANTENNAL ORGANS

Several investigators have studied the morphology of the
antennal organs in Diptera, but since certain drawings of Hauser
(80), vom Rath (’88), and Nagel (94) best illustrate the various
types of antennal organs, the following discussion will be taken
only from these three works.

The antennae of Diptera are usually short, generally consist-
ing of only a few segments, which bear so-called olfactory pits.

Hr
fad
bgt

53

Figs. 50 to 55. Structure of antennal organs of Diptera; figs. 50 to 52, copied
from Hauser (’80); figs. 53 and 54, from vom Roth (’88); and fig. 55, from Nagel
(94). Fig. 50, longitudinal section through third or last antennal segment of
Cyrtoneura stabulans FIll., showing internal anatomy of segment and the com-
pound olfactory pits (C) in section. X75. The tip of the segment is not sec-
tioned, thus showing the simple (A) and compound olfactory pits (B) from a super-
ficial view. Fig. 51, section of a simple olfactory pit, and fig. 52, part of a section
of a compound olfactory pit; X 750. Fig. 53, section of simple olfactory pit with
projecting hair; X 150. Fig. 54, section of compound olfactory pit on palpus;
100. Fig. 55, 2 olfactory hairs (Hr) on antenna of a mosquito (Culex pipiens ”);
x 500.

Not all of the segments bear such pits, but the distal or last one
is usually well provided with them. Sometimes, however, ol-
factory pits are never present on any segment, as in the mos-
quitoes. The olfactory pits are divided into simple and com-

482 N. E. McINDOO

pound ones. From a superficial view, a simple pit looks like a
small circle (fig. 50, a) with a dot at its center, while a compound
pit resembles a large circle (8) which contains radiating lines and
two or more dots. Sections through these pits show that a single
hair (fig. 51, Br) arises from the bottom of a simple pit and two
or more hairs (fig. 52, Hr) from the bottom of a compound pit
(fig. 50, C).. The mouth and sides of each pit are well protected
by pseudohairs (Hr'!). A sense cell (SC) lies directly beneath
each sense hair and a nerve fiber runs from each sense cell to the
nerve (figs. 50 and 52, NV). An idea of how well the distal seg-
ment is innervated may be had by looking at figure 50.

Sometimes the hair in a simple pit projects out of the mouth
of the pit (fig. 53), indicating that the primary function of such a
hair is that of touch. All types of transitional forms of simple
and compound pits have been found, and besides being present
on the antennae, the compound pits are sometimes found on
the palpi (fig. 54). Mosquitoes do not seem to have olfactory
pits; Nagel has found two types of hairs on their antennae, and
he calls the short, stout ones (fig. 55, Hr) olfactory organs. A
male mosquito has only a few of these hairs, while a female has
many. All flies seem to have olfactory pits, but some of them
do not have the compound ones, and a few of the latter flies bear
only one simple pit on each antennal segment.

SUMMARY

The disposition of the olfactory pores on the legs of Diptera is
more similar to that of those on the legs of Hymenoptera than
to those on the legs of Lepidoptera or Coleoptera, but those on
the wings of Diptera are more similar to those on the wings of
Lepidoptera than to those on the wings of the other two orders.
The disposition of the pores on the halteres is entirely different
from that of those on the hind wings of the other orders examined.
In Hymenoptera the hind wings bear about one-half as many
pores as do the front wings; in Lepidoptera the hind wings do not
bear quite as many pores as do the front wings; while in Diptera
the halteres bear almost one-half the total number of pores
found. Excluding the abnormal forms, the total number of

THE OLFACTORY ORGANS OF DIPTERA 483

pores found in the four orders examined varies as follows: For
Hymenoptera, from 463 to 2608 with 1286 pores as an average;
for Lepidoptera, from 514 to 1422 with 850 pores as an average;
for Diptera, from 473 to 1550 with 772 as an average; and for
Coleoptera, from 273 to 1268 with 724 pores as an average.

As in Lepidoptera, the olfactory pores of Diptera are dome-
shaped and their internal anatomy is very similar to that of those
in the other three orders, but the sense cells in the halteres are
more spherical than usual.

For description the pores have been divided into four types as
follows: The Hicks’ type includes all of those on the legs, wings,
and a few of those on the bases of the halteres. This type also
includes all of those found in the other three orders examined.
The other three types are found on the bases of the halteres.
The undetermined type really belongs to the Hicks’ type, while
the basal type is very similar to the Hicks’ type; nevertheless,
the basal and scalpel types are quite unique and are found only
on the halteres. While the basal pores stand in rows resembling
the shape of mountain ranges, each row of the scalpel pores may
be likened to an inverted urn-shaped ridge whose summit is
more or less flat and is beautifully sculptured. Deep depressions
lie between the rows in each type and a row of strong, protective
pseudohairs stands in each depression. Morphologically, the
scalpel type is the most highly developed, but physiologically
it is probably little or no better developed than any other type of
pore.

This study indicates that while the hind wings of Diptera have
been gradually reduced in size, consequently diminishing their
flying ability, their sensory function has been greatly increased.

Compared with the antennal organs, the olfactory pores are
better adapted anatomically to receive olfactory stimuli, because
the peripheral ends of their sense fibers come in direct contact
with the external air, while those in the antennal organs are cov-
ered with hard chitin.

484 é N. E. McINDOO

LITERATURE CITED -

GRABER, Virus 1882 Die chordotonalen Sinnesorgane und das Gehér der
Insecten. Arch. f. mikr. Anat., Bd. 20, pp. 506-640, 6 pl.
Hauser, Gustav 1880 Physiologische und histologische Untersuchungen iiber
das Geruchsorgan der Insekten. Zeitsch. f. wiss. Zool., Bd. 34,
Heft 3, pp. 367-403, 2 pl.
Hicks, J. B. 1857 Ona new organ in insects. Jour. Linn. Soe. London, Zool.,
v. 1, pp. 1386-140, 1 pl.
1859 Further remarks on the organs found on the bases of the halteres
and wings of insects. Trans. Linn. Soc. London, Zool., v. 22, pp.
141-145, 2 pl.
1860 On certain sensory organs in insects, hitherto undescribed.
Ibidem, v. 23, pp. 139-153, 2 pl.
Ler, A. B. 1885 Les balanciers des diptéres leurs organes sensiféres et leur
histologie. Rec. Zool. Suisse, T. 2, pp. 363-392, 1 pl.
-Leypia, Franz 1860 Uber Geruchs- und Gehérorgane der Krebs und Insecten.
Arch. f. Anat. u. Phys., pp. 265-314, 3 pl.
McEwen, R. 8. 1918 The reactions to light and to gravity in Drosophila and
its mutants. Jour. Exp. Zodél., v. 25, no. 1, Feb., pp. 49-106.
McInvoo, N. E. 1911 The lyriform organs and tactile hairs of araneads. Proc.
Phila. Acad. Nat. Sci., v. 63, pp. 375-418, 4 pl.
1914 a The olfactory sense of the honey bee. Jour. Exp. Zodl., v.
16, no. 3, pp. 265-346, 24 figs.
1914b The olfactory sense of Hymenoptera. Proc. Phila. Acad. Nat.
Sci., v. 66, pp. 294-841, 3 figs. and 2 pl.
1915 The olfactory sense of Coleoptera. Biol. Bul., v. 28, no. 6,
pp. 407-460, 3 figs. and 2 pl.
1917 The olfactory organs of Lepidoptera. Jour. Morph., v. 29, no. 1,
pp. 33-54, 10 figs. ,
Nace, W. A. 1894 Vergleichend phys. und anat. Untersuchungen tiber den
Geruchs- und Geschmacksinn und ihre Organe. Bibliotheca Zool.,
Heft 18, 207 pp. 7 pl. Diptera, pp. 116-117.
PrasHap, Barnt 1916 The halteres of the mosquito and theirfunction. Indian
Jour. Med. Research, v. 3, no. 3, pp. 503-509, 1 pl.
Vom Ratu, Orro 1888 Uber die Hautsinnesorgane der Insekten, Zeitsch. f.
wiss. Zool., Bd. 46, pp. 413-454, 2 pl. Diptera, p. 427..
WEINLAND, Ernest 1890 Uber die Schwinger (Halteren) der Dipteren. Zeitsch.
f. wiss. Zool., Bd. 51, pp. 55-166, 5 pl.

AUTHOR'S ABSTRACT OF THIS PAPER ISSUED
BY THE BIBLIOGRAPHIC SERVICE, JULY 19

REMARKS ON VON MONAKOW’S “DIE LOKALISATION |
IM GROSSHIRN””!

REPKE

Department of Physiology, Columbia University

Every now and again a work appears which lays the axe at
the root of some of our ancient and honorable scientific assump-
tions which have survived so long and for years have been so
often and so vehemently repeated that they have acquired a
certain sacredness and become a part of the dogmatic and un-
critical part of our teaching. Verily, the axe hath other uses
than those to which it is put by politicians or administrators,
and it would seem a pity that a notable work in which certain
long-cherished assumptions are put to the test of modern knowl-
edge should escape being brought to public notice. My object
is not to give a formal review of the book, but to discourse in-
formally upon some of its unusual features, and particularly
those which have to do with the fundamental conceptions of
the function of the central nervous system.

One point in which von Monakow departs from the traditional
views is his attitude toward the segmental theory of the nervous
system and its necessary attendant hypothesis of shock. With-
out pausing just here. to give a detailed discussion of his views,
we may say that he rejects the segmental theory and limits
the effects of shock in so far as they are incompatible with the
theory of cerebral localization. It will conduce to the clear-
ness of the discussion to give first a brief account of the older
view of the segmental theory of the central nervous system and

1 Die Lokalisation im Grosshirn und der Abbau der Funktion durch kortikale
Herde, von Dr. med. C. von Monakow, Professor der Neurologie und Direktor
des hirnanatomischen Institutes sowie der Nerven-Poliklinik aus der Universitat
in Ziirich. Mit 268 Abbildungen im Text und 2 Tafeln. Wiesbaden. Verlag
von J. F. Bergmann, 1914.

485

486 F. H. PIKE

then take up more in detail the examination of von Monakow’s
argument against these views and in favor of cerebral
localization.

, The classical statement of the segmental theory and of the
general hypothesis of shock is due largely to Goltz. I made
this statement from the point of view of the physiologist rather
than that of the anatomist. I should perhaps utter a warning
here that the phenomena of shock, as Goltz and others have
described it, and as the term is used in this paper, are not to be
confused with other phenomena of uncertain nature which have
come to be included under the somewhat obscure but widely in-
clusive term shock as it is used by the surgeon or the clinician.
A perusal of the first chapter of von Monakow’s work will be
sufficient to show the error that may arise from failure to differ-
entiate several different kinds of shock.

Goltz assumed that all reflexes occurred through the lower
levels of the central nervous system and especially through the
spinal cord. This view has been restated many times. Per-
haps its most concise statement in modern anatomical terms is
that by Edinger (’08):

Since it is certain that the palaeencephalon persists quite unchanged
even after a well developed neencephalon has been added to it, there is
no ground for regarding those activities which we recognize as ‘palacen-
cephalic in one class of animals as anythmeg else or as otherwise local-
ized in higher animals. Furthermore we may regard an entire series
of activities as common to all vertebrates and we may then seek to
ascertain how other activities are added to these when a new structure
is added to the palaeencephalon. All sense impressions and movement
combinations belong to the palaeencephalon. It is able to establish
simple new relations between the two, but it is not able to form asso-
ciations, to construct memory images out of sever: fh components. It 7s
the bearer of all reflexes and instincts.

This has generally been regarded as a certainty, and despite
the fact that he adduces no independent proof, Edinger’s italies
leave little doubt as to his own views on the subject. But
Goltz himself regarded it as an assumption, and no actual proof
of its general truth has been forthcoming in the four decades
and more since its enunciation. In view of the wide currency

“DIE LOKALISATION IM GROSSHIRN”’ 487

of the general idea of shock as applied to the central nervous
system it may not be out of place to give here Goltz’s statement
in his own words, as translated by Loeb (’00):

No one will assume, that that piece of the spinal cord which is
separated from the brain in so short a time (i.e., afew days or weeks)
acquires entirely new powers as a reflex organ; we must assume that
these powers were only suppressed or inhibited temporarily by the
lesion of the spinal cord.

Goltz’s statement of the segmental theory was that each level
or division of the central nervous system had essentially the
same functions in all vertebrates (Goltz, ’92). The reason why
a man or a dog will not recover as completely as a frog or a turtle
after loss of the cerebral hemispheres is not because the cerebral
hemispheres have any more highly developed motor function in
the higher forms, but because the effects of shock are so much
more permanent and more severe in the higher forms than in the
lower.

It may be remarked in passing that Magendie (1816), many
years before Edinger, had with great clearness stated the mechan-
ism of instincts in neurological terms. An abstract of his views
follows:

We may distinguish, in those attitudes and movements which are
intended to express our intellectual and instinctive acts, and which are
included under the generic term ‘gestes,’ between those which are
bound up with organization and, as a consequence, are present in all
men, in whatever condition, and those which have arisen and reached
their perfection in a social state.

The former are intended to express the most simple condition, the
internal sensations as joy, pain, grief and the like, as well as the animal
passions, through cries and the voice. One may observe them in the
idiot, the savage, the blind from birth, as well as in the civilized man
enjoying all moral and physical advantages. These are native or in-
stinctive responses.

But while Edinger’s statement of the relations was probably
at variance with the known facts at the time it was made, and
certainly is at variance now, the generality of Magendie’s expres-
sion made it conform, not only to the facts of his time, but also
gave it a lease of life which endures to the present day.

A488 F. H. PIKE

Von Monakow’s views on cerebral localization and on the dura-
tion and severity of the effects of shock are at variance with
those of Goltz, perhaps more widely than he realizes. For the
substantiation of Goltz’s views depends upon either, 1) the direct
proof of the activity of the spinal cord in the reflexes in the
manner which Goltz supposed it to act in the uninjured animal
or, 2) the independent proof that the reflex or other activities of
the regions of the nervous system lying below the level of the
transection or the injury are merely depressed for days or years,
as the case may be, and that no quantitative change occurs in
the impulses passing over any given synapse in the lower regions
of the nervous system leading to increased activity after the
injury, as compared with the amount of activity before the
injury occurred. The experimental evidence now available
does not substantiate Goltz’s conclusions on either of these
points.

Von Monakow recognizes that, if Goltz’s view of shock is to
be accepted, the idea of cerebral localization must be abandoned,
just as Goltz insisted. And if localization is true, one must set
some limits to the effects of shock. This he does in his theory
of diaschisis, which will be discussed a little later. But if we
set any limits to the omnipotence of shock, we raise the question
whether shock is a necessary conception in the explanation of
the phenomena following injury to any portion of the central
nervous system; and, considering shock as a purely depressive
effect, whether the limits set may not become vanishingly small.
If the limits do become small, the gap between von Monakow’s
position and Goltz’s position must become even wider than
it now is.

It is still necessary to make some assumptions in discussing the
organization of the nervous system. Aside from the assumption
that the effect of shock is merely temporary and that the cells in
the levels below the lesion regain all their former functions in
time, von Monakow (10) makes certain others concerning the
organization of the mechanisms of the spinal cord as well as
those of higher levels. The account is best given in his own
words.

“DIE LOKALISATION IM GROSSHIRN”’ 489

From the experiments of Sherrington and others as described, it
follows that in the spinal cord of higher mammals and, as my own
observations show, apparently even of man, there must be present
elements other than the direct receptor and effector cells themselves
which retain a stimulus for a longer period than these (i.e., than the
direct receptors and effectors). Included therein are found nerve cell
elements which are excited by individual incoming fibers, facilitated
through the summation of stimuli by others and again inhibited by
still others. Single nerve cells in the spinal cord apparently return to
a condition of rest after a short period of excitation, immediately after
the completion of the specialized function assigned to their neurone
complex, and again become receptive to new stimuli. Other cells,
however, undoubtedly remain in a condition of excitation for a longer
period—minutes or more—after the stimulus coming to them has
been interrupted. In other words, we find in the spinal cord elements
extremely variable in their duration of charge, both positively and
negatively (mnestic elements) such as I have long postulated in the
brain, with brief, intermediate or long duration of charge (Ladung).
There must also be present here well organized groups of neurones
which are effective, that is, which can discharge, only by means of a
complex summation of stimuli each (action) in a qualitatively different
manner and a different duration; and among them are groups which
form the connecting links of a chain of acts released in succession,
and which remain functional throughout the course of a reflex move-
ment; they carry the ‘kinetic melody’ as the notes of a chord accom-
panying the tune.?

Von Monakow’s views represent the growth of years. We
may take as one starting point the view expressed in 1895 that,
in a series of vertebrates, essentially similar nervous reactions
involve more numerous and more widely scattered groups of
cells and fiber tracts in the higher animals than in the lower.
The logical development of this idea means abandoning the
notion of sharply circumscribed centers particularly in the
cerebrum, for various acts, which he does.

The issue is squarely joined, therefore, with two other oppos-
ing camps. There is, on the one hand, the issue between the
adherents of the Goltzian view that the effects of shock may
persist, undiminished if need be, for months or years, with its
consequent negative view of cerebral localization, and the ad-
herents of the view that shock, if present at all, is more or less

2T am indebted to Mrs. C. S. Winkin for assistance in the translation.

THE JOURNAL OF COMPARATIVE NEUROLOGY, VOL. 29, NO. 5

490 F. H. PIKE

transient as one must hold if cerebral localization is to be sub-
stantiated. On the other hand, von Monakow opposes those
who insist on ‘‘all the so-called centers in the bulb and cord
(and particularly the cerebrum) with which the perverse inge-
nuity of nvestigators and systematic writers has encumbered
the archives and text books of physiology.’ (Stewart, ’00.)

A complete presentation of the evidence for and against the
current ideas of shock and of the omnipotence of the circum-
scribed centers would require many pages, but some statement
is necessary as a basis for a comparison of the various hypotheses
and a general estimate of their validity

As already mentioned, Goltz’s view, either in its original form
or as restated by Edinger, that reflexes occur through the lower
levels of the brain and the spinal cord exclusively, rests upon an
assumption. Explicitly or implicitly, Goltz and his school
assume that the cells and synapses of the isolated portion of
the spinal cord never convey any greater quantity of energy, to”
use Hughlings Jackson’s term, after isolation than they did
before. Changes in isolated cells have been mentioned in the
literature, e.g., Munk’s term ‘Tsolationsinderung,’ but those
changes have more commonly been supposed to be retrogressive
than otherwise. Sherrington’s term ‘isolation dystrophy,’
although applied to a somewhat different condition of affairs, is
an instance in point.

Senator (98), however, admits that reflexes may be per-
manently absent in the human subject in cases in which no
degeneration of, or damage to, the neurones of the supposed
reflex ares can be shown histologically. Basing his first con-
clusion, then, upon the fact that some of the reflexes return after
a time in the isolated portion of the spinal cord, Goltz as previ-
ously indicated, found it necessary to make another assumption,
to the effect that the reflexes were only temporarily suppressed
or inhibited by the operation of transection of the spinal cord.
This temporary failure of the reflexes had been called ‘shock’
by Marshall Hall, and Goltz spoke of ‘Shockwirkung’ in this
connection. Goltz did not know what shock was, but was in-
clined to regard it as an ‘Inhibitorische Fernwirkung’ due to the

“DIE LOKALISATION IM GROSSHIRN”’ 491

anatomical transection of the cord. And despite the fact that
cutting a nerve produces but a relatively small and transient
effect as compared with the effects of electrical stimulation,
anatomical transection of the spinal cord is commonly said to
be a terrific stimulus. Sherrington, however, shows that the
effect of anatomical transection can be exerted but once, and
concludes that the view of trauma qua trauma as the cause of
spinal shock is not really tenable. It has been shown also that
shock in the lower levels of the spinal cord may be produced by
anaemia of its higher portion and of the brain without interrup-
tion of the circulation to the lower portion of the cord (Stewart
et al., ’06) or by freezing a segment of the spinal cord without
excitation of the efferent motor pathway. Sherrington’s view
that the interruption of certain conduction pathways in the
spinal cord favors the production of spinal shock derives much
support from these results. The recent work of Ranson (’16)
shows that the rupture of certain orally conducting pathways is
effective in abolishing responses and that the rupture of the
aborally conducting pathways may not be necessary, as Sher-
rington believed it to be. Ranson’s results confirm, in a measure
at least, my view that the shock effect is exerted upon the affer-
ent pathway, since the efferent pathway is so obviously open,
as judged by all the tests which one may apply.

The segmental theory of the central nervous system, as Goltz
formulated it, does not accord with the facts of organic evolu-
tion, inasmuch as it makes no allowance for a change in function
of the various levels of the system to correspond with the ana-
tomical changes occurring in phylogenetic development. The
argument for a shifting of function toward the anterior end of
the central nervous axis (Steiner) and the development of cerebral
localization is met by the statement on the part of the segmen-
talists that, if the effects of shock in the higher forms were not
so severe, the lower levels of the nervous system of a man would
manifest just as complete a recovery after injury to the higher
levels as those of a frog. The increasing severity and perma-
nence of the shock effects in higher animals, while freely ad-
mitted by Goltz, and even made a supporting point of his

492 F. H. PIKE

hypothesis, are without any explanation on the basis of such
an hypothesis. Goltz and his followers conclude that a cell in
the lower levels of the central nervous system may never regain
all its normal function after the injury to the higher levels.
Von Monakow departs from the fundamental assumption of
the segmental theory—that all levels or segments have essen-
tially the same function in all types of vertebrates—in his state-
ment that more numerous and more widely separated groups of
nerve cells and fibers are necessary for the successful execution
of essentially similar movements in successively higher types of
animals. This statement, as already noted, dates back to 1895.
The anatomical and pathological evidence available twenty
years and more ago was sufficient to shake his faith in the seg-
mental hypothesis. To some of us it seems that all the addi-
tional anatomical, pathological, and experimental evidence
which has accumulated since that time points toward cerebral
localization as the logical and final development of the processes
of evolution in the central nervous system. But, as I have
already mentioned, and as I would particularly emphasize
now, cerebral localization is an untenable view if all Goltz’s
postulates concerning spinal shock are to be granted. The
emphasis is the more necessary since this part of Goltz’s argu-
ment, which is essentially sound if his premises be granted, has
been so frequently neglected or overlooked. Goltz considered
the argument against cerebral localization to be just as cogent
as his argument for the spinal cord as the great reflex mechan-
ism, as a careful reading of his papers will show. He was much
too careful and accurate a thinker to overlook any serious defects
in the logic of his argument. Indeed it must be confessed that
he was a far clearer and more logical thinker than many who
have essayed this field since his day, or than many who have
accepted his argument in part while rejecting the remainder of
it. The task of these latter authors is more difficult than was
Goltz’s, for they must show, not only that one part of his argu-
ment is correct, but why the remainder, which is founded on
exactly the same assumption as the other part and upon facts
of exactly the same nature, is incorrect. I will freely admit

‘“‘DIE LOKALISATION IM GROSSHIRN”’ 493

that intellectual evolutions of this sort are much too difficult for
me to follow and, a fortiori, to execute. I cannot do less than
to accord to Goltz here, from whom I differ on matters of inter-
pretation, the same tribute he accorded to Le Gallois, from whom
he differed on matters of interpretation. I do not question
Goltz’s facts any more than he questioned those of Le Gallois.
And I should say of him, as he said of Le Gallois, that he was
one of the clearest thinkers among the physiologists of his day.
But just as the discovery of new facts compelled the revision of
Le Gallois’ interpretation, so I now believe that the discovery of
new facts has compelled a revision of Goltz’s interpretation.
The limitation of the effect of shock to a degree which may in
some measure be based upon anatomical or functional considera-
tions is necessary. Whereas Goltz supposed that the cells in
the regions below the level of injury might never regain all their
former degree of activity, but might be permanently depressed
or inhibited for the remainder of the life of the animal, von
Monakow, while allowing a possible depression of function of the
cells below the level of the lesion at the time of its occurrence,
supposes that this depression is transient, and that, in time, the
isolated cells may regain all their former functions. The minimal
deficiencies of function remaining after some weeks or months
subsequent to the injury afford a measure of the function of the
injured or lost portions, particularly of the upper levels of the
nervous system. In no case, so far as I have observed, does
von Monakow suppose that the quantity of nervous energy, to
use Hughlings Jackson’s expression, flowing through any one of
the remaining tracis is any greater after an animal’s recovery
from the injury than it was before the injury.

In his hypothesis of diaschisis, von Monakow comes back to
the view that it is the rupture of the aborally conducting, or
efferent, paths which is the essential factor in: shock. The
lower lying neurone, after its separation from the higher, or
after failure of the impulses which normally come down from
the higher, supposedly suffers a temporary depression of function.

Von Monakow also attacks the idea of a vicarious assumption
of the function of the injured portion of the central nervous

494 F. H. PIKE

system by any remaining intact portion, declaring that it is not
a useful conception in the explanation of the action of the nerv-
ous system normally or of the processes occurring in its recovery
from injury.

If, by vicarious assumption, one means that some other cells
and fibers which were never concerned directly or indirectly
with the processes carried out by a second group when intact,
assume a part of the function of the second group when the latter
is injured, vicarious assumption becomes a mischievous as well
as a useless hypothesis in the explanation of nervous processes.
For, if one group of cells may take over a function with which it
has had no previous connection, there is no localization of func-
tion in the proper sense of the term. If such be its meaning, the
term vicarious assumption of function should be dropped from
neurology.

The idea of compensation in the nervous system for injury
to any of its parts should not, however, be disposed of so sum-
marily. In order to show how such a compensation is susceptible
of explanation in terms of nerve cells and fiber tracts without
violating any of the postulates either of cerebral localization or of
localization in the nervous system generally, I will ask leave to
introduce here some conclusions to which I have been led from
a study of certain processes of compensation for loss of partic-
ular afferent channels or central cells and fibers. To state the
case intelligibly, it is necessary to give something of the general
physiological basis of normal responses.

I have stated elsewhere my belief that the reactions of an
animal generally occur in response to gvoups of afferent impulses
of different kinds rather than to one single kind of afferent im-
pulse. Jn looking over the field generally. I am more and more
impressed with the number of responses in which afferent im-
pulses from more than one source can be shown to participate.
I am doubtful whether any single reflex response, particularly a
response of the skeletal muscles, can be shown to involve affer-
ent impulses from one source only.

In making these statements, I am fully aware that in the
elicitation of certain reflexes under experimental conditions, one

‘‘DIE LOKALISATION IM GROSSHIRN”’ 495

nerve trunk only may be stimulated, and it may be urged that
the reflex response occurs without the access of any other affer-
ent impulses. Stimulation of a particular afferent nerve under
constant conditions generally elicits a particular reflex response.
Hermann embodied these facts in his statement of the law of
specific response to stimulation. But the reflex response of a
skeletal muscle involves other afferent impulses than those
arising from stimulation of a given afferent nerve in a given
manner, which may be regarded as the particular afferent im-
pulses which elicit the response. Tschiriew showed that even
the form of the curve of a single muscle twitch elicited by stim-
ulation of the motor nerve to the muscle is modified by section
of the afferent nerves from the muscle. Afferent impulses from
the muscle itself are involved in its reflex response arising from
stimulation of any other afferent nerve. And if the muscle is in
situ, other, antagonistic, muscles are involved as well as the
prime mover. The deportment of the antagonists is controlled
by afferent impulses, arising in part in the antagonists them-
selves, and in part in other regions, such as the joints. The
analysis of even the simplest reflex response in an intact animal
shows that it is far from simple in the mechanism involved.
One should not lose sight of all the other phenomena following
the application of the one form of stimulus to a given limited
area or location which is said to elicit the reflex. To lose sight
of what follows is to get a very imperfect idea of even the sim-
plest reflex response of a skeletal muscle. In general, it is the
accessory afferent impulses, if one may so speak of them—the
impulses arising from sensory fields other than the limited one
to which a given stimulus is applied—which makes the reflex
response biologically adequate, to use Edinger’s phrase. That
a reflex response may occur in the absence of some of the affer-
ent impulses normally entering into its control does not affect
the main statement. It is possible that under experimental
conditions a reflex could be elicited which would involve affer-
ent impulses from one and only one sensory field. But it is
extremely doubtful whether such a condition ever arises in the
intact animal. When we consider the liberation of one reflex

496 F. H. PIKE

response by one preceding it, and when we consider also the
considerable number of afferent impulses which may be in-
volved in such a reflex response as the maintenance of an atti-
tude of the body or a part of it, or in the maintenance of equi-
librium, the actions become bewildering in their complexity.

The study of the specific reflex response to stimulation of a
given afferent nerve and of the modifications of any given re-
sponse which occur when any particular component of the affer-
ent group is lacking are of importance not only from the point
of view of the physiologist, but from the point of view of the
clinician as well. One aid in diagnosis which the clinician
employs is the study of the modification of typical’ motor re-
sponses which occurs when any particular afferent channel or
channels are blocked. Considerably more precision of facts
and ideas is necessary before this particular aid attains to its
maximum usefulness to the clinician.

Other writers have also recognized this dependence of the
normal response upon afferent impulses from various sources.
Upon some such basis, if I get its significance correctly, must the
idea of the integrative action,—a summing up of afferent im-
pulses within the central system—of the nervous system be
founded. I have expressed elsewhere the belief that the idea of
the integrative action of the nervous system is one of the great
principles of the physiology of the nervous system. It under-
lies all the work of Pawloff on conditioned reflexes. And all
the work of Pawloff goes to show that it is in the cerebrum that
the summing up of the afferent impulses so necessary for the
finer sensory discriminations occurs. Instead of being an
argument against cerebral localization, as I have once or twice
seen intimated, it seems to me that Pawloff’s work is an argu-
ment in favor of localization. The description in physiological
terms of any response occurring through the nervous system
must include an account of all the afferent impulses which enter
into its inception and control, the central mechanism of this
integration, and the efferent pathway. The relationships of the
various afferent impulses concerned are not always obvious
from the anatomical relations. Most of the instances in which

“DIE LOKALISATION IM GROSSHIRN”’ 497

groups of afferent impulses from different sources are said to be
concerned have involved more or less of a subjective element in
the demonstration. It is, however, possible to get a purely
objective demonstration of the fact that afferent impulses from
at least two different sources are involved in postural activity,
to use Sherrington’s terminology, of the muscles which maintain
the position of the head. If one otic labyrinth of a cat is ex-
tirpated, there is torsion of the head, the occiput being turned
‘toward the injured side and the nose toward the sound side.
If, after an interval varying from one hour to several months,
the dorsal roots of the cervical nerves of the opposite side are
divided, the torsion of the head disappears (Prince, 716). Sub-
sequent experiments have shown that the processes of compensa-
tion are related to a considerable degree to the cerebral hemi-
spheres (Prince, 717). There is a strong presumption, at least,
that afferent impulses from divers peripheral sources are nor-
mally involved in the control of any motor reaction. All of these
impulses of various kinds are necessary for the normal perform-
ance of such a motor act. There is also a strong presumption
that when one of these afferent channels is blocked by accident
or disease, certain of the other channels may, by an increase in
the quantity of energy which passes over them, compensate, in
part at least, for the loss of the impulses which formerly came in
over the damaged pathway. What is commonly called vicari-
ous assumption of function may be a reality in this sense and
in this degree. But it is not necessary to postulate the partici-
pation in this process of compensation of any system or group of
fibers which is not normally concerned in the control of the
reactions in some degree. A more detailed account of this
phase of the question will be presented in a forthcoming dis-
cussion of some unpublished experiments on the otic labyrinth.
(See also Wilson and Pike, °12.)

I wish to say here, however, that the minimal deficiency of
function would be an incorrect index of the actual function of
such an organ as the otic labyrinth, as the index would be too
low. I may remark in passing that Prince’s results effectually
dispose of the italicized portions of Edinger’s remarks on the

498 F. H. PIKE

localization of all reflexes. As the matter appears to me now, I
would say that the loss of or injury to any given region of the
brain may be compensated for, in part at least, by an increase
in the quantity (without any change in the quality), to use a
suggestion of Hughlings Jackson’s, of the nervous energy pass-
ing over the other afferent pathways or through other central
stations which are normally involved in the functions of the
injured part. Compensatory processes of this general nature
should be considered in arriving at an estimate of the normal
function of any injured or lost portion of the central nervous
system. And if, as I believe has now been definitely shown,
these processes do enter into the problem of the interpretation
of cerebral function, the minimal deficiency of function observa-
ble after a long period of recovery will be too low to serve as an
accurate index of the normal function of the injured or lost part.
Such a view is not in any way destructive of or antagonistic to
von Monakow’s argument for cerebral localization. As I see the
problem, it strengthens von Monakow’s general position inas-
much as it shows that normal cerebral function may be even
greater than he imagines.

The view that more numerous and more widely separated
groups of nerve cells and fibers are necessary for essentially the
same sort of movement in higher animals than in lower and the
view that afferent impulses from different sources are concerned
in most of our neuromuscular reactions have a certain bearing
on the hypothesis of circumscribed centers each having a definite
and particular function. Von Monakow has taken the speech
center as a test case and adduces evidence that the cerebral
speech mechanism cannot be such a circumscribed center.
Space does not permit a consideration of the evidence against
such circumscribed centers urged by other physiologists (Leonard
Hill).

There are other systems or mechanisms in which the hypoth-
esis of a definite circumscribed center is no longer satisfactory.
One would expect to find such a definite circumscribed region in
the lower levels of the nervous system in the portions which
have become highly organized, as Hughlings Jackson expresses it,

‘“‘DIE LOKALISATION IM GROSSHIRN”’ 499

and whose responses to excitation occur in a definite regular
manner time after time. The group of cells in the medulla
oblongata which responds to increase in the concentration of
the hydrogen ions in the blood by a respiratory impulse may be
taken as a case in point. Probably there is such a definite
group of cells from which arise impulses leading to movements
of the respiratory muscles, and it is probable also that such
impulses do not arise from any other group of cells. The evi-
dence in favor of the normal participation in respiratory move-
ments of accessory respiratory centers in the spinal cord does
not appear to me to be conclusive. To this extent and in this
sense, the respiratory center is a definite circumscribed center.
But the question does not end here. ‘The experimental evidence
now at hand on respiratory movements alone is incompatible
with the idea of such a circumscribed center as the complete
controlling mechanism. Anatomically, the central respiratory
mechanism is not very thoroughly known. Experimentally, it
is a system of great neurological interest. This interest is
heightened for the student of the speech mechanism by the
fact that every afferent impulse involved in the control of respi-
ration is involved also in the control of speech. And when we
consider that speech involves respiratory movements, most
certainly under cortical control, the idea of a circumscribed
respiratory center becomes hopelessly inadequate to account for
all respiratory movements that are possible in man. A complex
mechanism consisting of groups of nerve cells more numerous
and more widely separated in man than in the turtle becomes a
necessary postulate.

The argument on shock may be summarized by saying that
von Monakow in his theory of diaschisis has granted all that
could reasonably be asked for shock, i.e., it is a temporary effect
from which the cells recover fully, but never assume any greater
function than their normal function in an intact nervous system.

One may be pardoned, perhaps, for suggesting that, before
any hypothesis of shock as a consideration influencing our inter-
pretation of the function of any level of the central nervous
system is accepted, we find out just how necessary any such

500 F. H. PIKE

hypothesis is. For any compensatory increase in the activity
of the lower neurones must be subtracted from the supposed
shock effect, and a corresponding amount must be added to
the supposed function of the cerebral cortex, as determined by
the criterion of a minimal deficiency of function. Asthe problem
stands at present, there are three unknown quantities: 1) the
exact function of the lower neurones, motor, sensory, com-
missural or association; 2) the amount of change of a progressive
nature rather than retrogressive, which the lower motor neurones
undergo after separation from the higher, and, 3) the exact
function of the higher neurones. None of the quantities has
been measured independently and directly, and the number of
equations so far proposed is less than the number of unknown
quantities. It seems idle, therefore, to introduce a fourth
unknown quantity—the shock effect—or even a fifth, such as
vicarious assumption of function, and to ascribe arbitrary limits
to it, when the determination of its real value must await either
a demonstration of its actual extent and potency or the solu-
tion of the equations involving the three other unknowns.
Certain considerations other than those already adduced may
be brought forward in connection with the discussion of von
Monakow’s views. Diaschisis, or shock, or whatever other
name one may apply to the change which occurs in the lower
levels of the central nervous system when they are separated
from the higher, isa reversible change. I have already referred
to Sherrington’s statement that, when the shock effect has once
been induced in the spinal cord by anatomical transection, a
second transection below the first has no further effect. In this
case the anatomical separation of one portion of the central
nervous system once for all from the remaining portions would
preclude any reciprocal action of one part upon the other. No
possibility of a reversible reaction dependent upon a connection
of the lower levels with the higher exists under such conditions.
But when the function of the higher levels of the central nervous
system is temporarily abolished, by tying off the arteries to the
head, the lower part exhibits at first signs of shock similar to
those seen after anatomical transection. There is, however, a

“DIE LOKALISATION IM GROSSHIRN”’ 501

return of the reflex responses of the structures lying below the
anaemic region of the spinal cord within a period of half an
hour or an hour. Anatomical transection at this time is not
attended by cessation of the reflexes. Just as in Sherrington’s
experiments, trauma qua trauma is not the necessary antecedent
condition for the onset of spinal shock. But if the circulation
to the head is restored and the animal is allowed to recover, a
more or less normal deportment gradually returns. If anatomi-
cal transection of the cord is done on the following day, or even
a few hours after re-establishment of the cerebral circulation,
signs of shock appear immediately. The changes which oc-
curred in the spinal cord leading to the return of the reflexes
while the circulation to the head was interrupted were reversible,
since, to all our tests, they did not greatly outlast the period of
failure of cerebral and bulbar function.

There is one other point on which the doctrine of minimal
deficiency of function comes into conflict with the conclusions
drawn from the results of more acute experiments. Francois
Franck and Pitres taught that in mammals tonic movements of
the skeletal muscles originated from the lower motor cells (e.g.,
basal ganglia) and that the clonic movements originated from
the higher motor neurones. Epilepsy and epileptiform con-
vulsions (Hughlings Jackson) are of cortical origin. Gowers
taught that a spastic paralysis indicated a lesion of the higher
motor neurones, while a flaccid paralysis indicated a lesion of
the lower motor neurones. Decerebrate rigidity (Sherrington)
is due to the activity of lower motor neurones. Horseley reported
some experiments from his laboratory in which absinthe was
used to induce convulsions in cats. If the cerebral hemispheres
were present along with the rest of the central nervous system,
absinthe produced: clonic convulsions. If the cerebral hemi-
spheres were removed, absinthe produced tonic convulsions.
If one cerebral hemisphere was removed and the other left
intact, clonic convulsions appeared on the opposite side. So
general has the belief in this hypothesis of the origin of tonic
and clonic movements become that many have insisted that
the pyramidal fibers exert an inhibitory action upon the lower

502 F. H. PIKE

motor neurones. Concerning the truth of this latter statement,
I must confess to a deep and enduring skepticism. Complica-
tions arise in such a scheme. If we follow out the types of move-
ment that are present in various representatives of the verte-
brate phylum, we find that even in such forms as the chimaeroid
fishes in which higher motor neurones, as we know them in
mammals, are lacking, clonic as well as tonic movements are
possible. Moreover, in such forms, there is no sustained rigidity
of the skeletal muscles: even without the supposed inhibitory
action of the pyramidal fibers, the lower motor neurones do not
normally develop any activity which results in a prolonged
spastic condition of the muscles. If in the higher type of ani-
mals the pyramidal fibers exert an inhibitory influence, it seems
equally clear that in the course of the evolution of vertebrates a
change has occurred in the lower motor neurones, resulting in
the development of some activity which must be inhibited.
One must therefore admit a change in the function of the lower
motor neurones in phylogenetic development if the hypothesis of
the tonic inhibitory action of the pyramidal fibers is to be sub-
stantiated. Such a change in the function of the lower motor
neurones seems improbable. It appears simpler to assume that
as evolution has progressed there has been a separation in the
types of movement represented by higher and lower motor
neurones; and that in the higher animals, when the higher
motor neurones are injured or destroyed, there may be a change
in the amount of energy passing through—a quantitative but
not a qualitative change—in the function of the lower motor
neurones. As Dejerine (714) shows, man is the only form in
which a permanent spasticity of the skeletal muscles results
from. a purely cortical lesion. Goltz’s decerebrated dog, in which
although decerebration was not complete, no part of the motor
area remained, did not exhibit any permanent spasticity. Com-
plete decerebration in a dog is followed, usually within an hour,
by marked decerebrate rigidity (Sherrington). The particular
nerve cells which it is necessary to rupture in order to produce
permanent spasticity have a different anatomical location in
man as compared with the dog. Some change in the anatomical

“DIE LOKALISATION IM GROSSHIRN”’ 503

site of the cells whose removal is necessary for the genesis of
spasticity by the remaining cells of the central nervous system
has occurred in the course of evolution from lower to higher
vertebrates. The pyramidal fibers in a dog do not apparently
exert the inhibitory effect on the lower motor neurones which
they are said to exert in man.

Spinal shock, while of little direct interest to the present-day
internist, has appealed to the clinical neurologists in days past,
and from them has come the clinical counterpart of the labor-
atory expressions. That the necessity for some hypothesis or
theory of shock is still felt among clinicians is shown by the fact
that Mott (16) has applied von Monakow’s views in the attempt
to explain some of the conditions arising in cases of shell shock.
It is my opinion that the importance of a conception of the
changes occurring in the nervous system as the result of injury
will meet with more general recognition as the effects of war
conditions are more generally and more critically studied. Two
of the earlier attempts of clinicians to explain the effects of
injury to or disease of the higher motor neurones are those of
Gowers and Hughlings Jackson. Gowers formulated his ideas
in terms of inhibition, but, in the opinion of some clinical neu-
rologists, his hypothesis is unsatisfactory. Hughlings Jackson
phrased his conceptions in terms of energy. He thought that if
one level of the nervous system was damaged by disease about
the same quantity of energy as passed through the whole central
system before the injury passed through the remaining levels
after the injury. Although he does not expressly say so, Jack-
son’s view, particularly in the form in which it was expressed by
Horsley (07), postulates a quantitative change in the number
or intensity of impulses going through the remaining nervous
pathways. I can hardly see how the change in the amount of
energy in the remaining levels of the central nervous system
which he imagines to occur after the shutting out of one level
can occur without such a quantitative change as has been shown
to occur in some levels of the central nervous system. To all
intents and purposes, the idea of a quantitative change in func-
tion must have been present in Jackson’s mind. I do not

504 F. H. PIKE

remember, either, that he used the term vicarious assumption of
function. It is true that Jackson was not an experimentalist,
but his powers of observation and of deducing from his facts a
generalization which would hold them all together were extra-
ordinary. In the matter of cerebral localization, he anticipated
by several years the experimental work of Fritsch and Hitzig.
The idea of a change of energy in the remaining levels of the
central nervous system should, from its authorship, command at
least a careful scrutiny. But aside from some of the fruitful
suggestions of Luciani, I have seen little or no use made of the
hypothesis by experimentalists, despite the fact that such a
hypothesis might be given the rank of a fundamental assumption.
I am strongly of the opinion at present that we have experi-
mental proof that a given conduction pathway may carry a
greater quantity of nervous energy after injury to another path
way associated with it in the control of a given response than it
carries under the usual conditions.*

3 Prof. W. M. Bayliss, who has read the manuscript, has asked me just what
the earlier statement of Jackson about the change in the quantity of nerve energy
passing over a given pathway might mean in terms of the recent work of Lucas
and Adrian on the nerve impulse. One may take as an example of such a change
the crossing over of efferent impulses from the respiratory center at the phrenic
nuclei. (Porter, Journal of Physiology, 1894-5, 17, p. 455). The reader must
consult the original paper for the full description of the phenomena, as it is too
long to give here in detail. When the spinal cord is hemisected above the level
of origin of the phrenic nerve, we will say on the right side, the movements of
the half of the diaphragm on that side cease. If the phrenic nerve of the oppo-
site (uninjured or left) side is divided, the movements of the right half of the
diaphragm begin again. The impulses which were passing down the left side of
the cord now cross to the right side. As I see it, there is a change in the quan-
tity of nervous energy passing over the commissural fibers and synapses from the
left phrenic nucleus to the right. It is possible, even probable, that the increas-
ing asphyxial condition which comes on after section of the left phrenic nerve
leads to the excitation of more cells in the bulbar respiratory center and to the
sending out of impulses over more efferent fibers than before. It is not necessary
to postulate any increase in the intensity of the impulses coming over any
one fiber. In view of Stirling’s demonstration that the synapses have the power
of summation of impulses, and Sherrington’s experiments, as well as observations
by G. N. Stewart and myself, pointing to the same conclusion, I think it probable
that the principal change occurs in the passability of the synapses. In the com-
pensations occurring after loss of the otic labyrinth, it does not seem possible
that either more fibers are excited in any of the afferent systems entering

“DIE LOKALISATION IM GROSSHIRN”’ 505

One reason for the neglect of Jackson’s hypothesis may be
that Jackson’s conception is distinctly that of a physiologist,
while clinicians generally have tried to interpret the nervous
system without much reference to purely physiological data.
The physiologist has generally given too little consideration to
well established clinical data, and has often exercised too little
critical discrimination with regard to widely current beliefs
which were not necessarily in accordance with the facts. I
find Jackson’s views in general better suited to constructive
work than Goltz’s.

The odds in favor of any hypothesis of shock and against
cerebral localization could scarcely be greater than von Monakow
has granted. He has understated rather than overstated his
case. To my mind, therefore, one of the fundamental questions
in the physiology of the nervous system, and in fact the question
that underlies practically all of our interpretation of the effects
of lesions of the central nervous system today, is whether or not
a nerve cell, or group of cells, perhaps forming a potential reflex
are, IN any way increases quantitatively, after injury to a system
connected with it, the work which it has been doing while all its
connections are intact. Unless the possibility of such a quanti-
tative change can be excluded, the whole hypothesis of shock
must be modified. And if such a quantitative change can be
shown in such an isolated (speaking relatively, of course) group
of nerve cells, even von Monakow’s conclusions must be modified
in favor of a stricter view of cerebral localization than the one
he now holds.

If von Monakow is right in his conclusions from anatomical
data, and, as I have insisted elswhere, they derive great support
from the experimental data, Edinger’s dictum becomes definitely
obsolete, and takes with it all the obscurity and vagueness of
the shock hypothesis, as well as, let us hope, some of its acrimony.

into the process of compensation or that impulses passing over these fibers are
any more intense than before. There may be an increased sensitivity of some
of the receptors, but it seems probable that the main thing is the change of re-
sistance at the synapses.

On the basis of the all or none law, it is difficult to see how such a severe effect
as has sometimes been supposed to result from transection of the spinal cord is
possible.

THE JOURNAL OF COMPARATIVE NEUROLOGY, VOL. 29, NO. 5

506 F. H. PIKE

But, if the rigid conceptions of the segmental system are to be
substantiated and shock in all its pristine vigor is to remain with
us, then must it be conceded that von Monakow has been pur-
suing a mirage and that the inferences from the great amount of
fact collected in his volume are largely untrue. This I am loath
to admit, since my own interpretations of experimental findings
would be swept away with it. I may repeat that it is necessary
to choose between the hypothesis of spinal shock and the seg-
mental theory, on the one hand, and the theory of cerebral
localization, on the other. The adherent of the theory of cere-
bral localization need not be unduly troubled by misgivings as to
the security of his position until it has been shown beyond mere
assumption that the things supposed to occur in shock actually
do occur. So far as the experimental evidence goes at present,
it is against Goltz’s position rather than in favor of it. What-
ever objections I may urge against von Monakow’s position are
to be regarded as constructive rather than destructive. Neither
of us doubts the transient effect of shock nor the general truth
of cerebral localization. I believe that the available evidence
justifies a stricter view, a more rigid localization than the one
he has propounded in his volume.

The doctrine of cerebral localization must be regarded as
established, and the hypothesis of shock as Goltz formulated it
must be discarded. Not only has there been no direct proof of
the hypothesis of shock, but there is experimental proof of the
main tenets of the theory of cerebral localization. There must
be a corresponding revision of many of the chapters in our texts
of physiology as they stand today.

The establishment of the theory of cerebral localization will
bring us a step nearer to the realization of the prophetic vision of
Magendie (’16b), which has been obscured for so many decades
by the mass of detail accumulated by anatomists and experi-
mentalists alike, both of whom have so. far failed to accept the
interpretation of the great French experimentalist.

One means by the term brain (cerveau), the organ which fills the

cavity of the cranium and that of the spinal canal. To facilitate the
study, the anatomists have divided it into three parts, the cei veau

“DIE LOKALISATION IM GROSSHIRN’”’ 507

(brain) properly speaking, the cerebellum, and the spinal cord. This
division is purely scholastic. In reality the three parts form one and
the same organ.

It is only when we regard the cerebrum as the great sensory
and motor mechanism to which all the other parts contribute
and from which they receive that we can rid ourselves of the
idea—eminently fallacious, as I view it—of independent sensory
or motor activities of other portions of the nervous system and
begin to see all parts of the system acting as one system.

We are hearing much of the clearness of French thought in
relation to scientific subjects at the present time. It is well
that we are beginning to accord it the somewhat tardy recogni-
tion which it so nobly deserves. I am minded to emphasize the
value of clear thinking in science and particularly in physiology,
by a quotation from another source. In the German edition of
Luciani (’07), but unfortunately omitted from the English
edition, there is a fine sentence concerning another very prev-
alent fallacy—the view that the otic labyrinth has its main
functional pathway through the cerebellum—but which is
equally applicable to the popular status of shock to-day.

One cannot deny that the clearness and consistency of the book
py . . . . leave something more to be desired, and its following
among many clinicians and surgeons would be difficult for me to explain
if I did not remember that great is the number of uncritical people
among whom words of uncertain meaning have more weight than
positive facts and clear, well considered explanations.

The plausibility of the words of uncertain meaning may be
greater than that of the other type of exposition. How else
may one account for the amazing vogue of fakirs and quacks?
It may be remarked in passing that von Monakow inclines to
the view that there is a cortical station for laybyrinthine fibers
in the cerebrum.

More recently, Luciani (16), has warned against the con-
fusion in thought which inevitably follows when one fails to
recognize the essential unity of action of the central nervous
system, but clings instead to the idea of separate, independent,
and sharply localized centers in various divisions of the central

508 F. H. PIKE

nervous system. As I have indicated elsewhere, some concep-
tion of a quantitative change in the amount of energy passing
over a given nerve pathway after injury to another may have
been present in Luciani’s mind years ago.

Von Monakow’s work will take its rank along with other
classical monographs on the nervous system—Francois-Franck’s
“‘Lecons sur les Fonctions Motrices du Cerveau,’’ Luciani’s
‘‘Cervelletto” and Soury’s ‘‘Le systeme nerveux centrale.”
It is to be hoped also that the various illuminating addresses
and lectures which were published during the years when the
larger volume was in preparation will be continued long after
its publication.

The objection sometimes urged against works in the German
language that American work does not receive proper consider-
ation can scarcely be urged against von Monakow’s volume.
American anatomists, psychologists, clinical neurologists, and
surgeons are mentioned in the index of authors. The small
number of American physiologists whose work is cited may
perhaps be taken as index of the lack of interest in this phase of
physiology which has been manifested by American workers.

“DIE LOKALISATION IM GROSSHIRN”’ 509

BIBLIOGRAPHY

DEJERINE, J. 1914 Semiologie des Affections du Systeme Nerveux. Paris, p.

Epincer, L. 1908 The relations of comparative anatomy to comparative
psychology. Jour. Comp. Neur., 18, p. 444.

Goutz, F. 1892 Der Hund ohne Grosshirn. Archiv fiir die Gesammte Physi-
ologie, 51, p. 614.

Horstry 1907 Dr. Hughlings Jackson’s views of the function of the cere-
bellum, as illustrated by recent research. Brit. Med. Jour., April, p.

803
Lorn, J. 1900 Comparative physiology of the brain. New York and London,
pp. 273-4.

Lucranr, L. 1907 Physiologie des Menschen. Jena. Bd 3, p. 488.
1916 La questione del moto e del commino in ordine alla dottrina del
cervelletto. Archivio di Fisiologia 14. pp. 147-156.

MaGeEnpIE, F. 1816a Precis Elelmentaire de Physiologie. Paris; T. 1, pp.
302, 303.
b Ibid, p. 162

Monaxkow, C. von 1895 Experimentelle und pathologisch-antomische Unter-
suchungen iiber die Haubenregion, den Sehhiigel und die Regio sub-
thalamica, ete. Archiv fiir Psychiatrie, 27, pp. 1, 386.
1910 Aufbau und Lokalisation der Bewegungen beim Menschen.
Leipzig. p. 12.

Mort, F. W. 1916 The effects of high explosives upon the central nervous
system. Lancet, 1, pp. 331, 441, 545. ? :

Pixs, F. H. 1909 The genera’ phenomena of spinal shock. Amer. Jour.
Physiol. 24, pp. 139-142.

Prince, A. L. 1916 The position of the head after experimental removal of
the otic labyrinth. Pro. Soc. Exper. Biol. and Med., 13, p. 156.
1917 On the compensation of the ocular and equilibrium disturbances
which follow unilateral removal of the otic labyrinth Ibid, 14, p. 138,
and unpublished results. See also Aronovitch, B., and Pike, F. H.,
1918 The factors influencing the attitude of the head in animals with
injury to one otic labyrinth. Science, N. 8.. 47, p. 519.

Ranson, 8. W. 1916 New evidence in favor of a chief vaso-constrictor center
in the brain. Amer. Jour. Physiol., 42, p. 1.

Senator, H. 1898 Zwei Falle von Querschnittserkrankung des Halsmarks.
Zeitschrift fiir klinische Medizin, 35, p. 18.

SHERRINGTON, C. 8. 1906 The integrative action of the nervous system New

York, p. 246.
Stewart, G.N. 1900 Manual of physiology, 4th ed. London and Philadelphia,
Toe Clete

Stewart, G.N., etal. 1906 The resuscitation of the central nervous system of
mammals. Jour. Exper. Med., 8, p. 289.

Witson, J. G., anv Pikr, F. H. 1912 The effects of stimulation and extirpa-
tion of the labyrinth of the ear and their relation to the motor system.
Part 1. Experimental. Philosophical Trans. Royal Soc., London,
Series B., Vol. 203, p. 127.

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AUTHOR'S ABSTRACT OF THIS PAPER ISSUED
BY THE BIBLIOGRAPHIC SERVICE, AUGUST 7

WEIGHTS OF VARIOUS PARTS OF THE BRAIN IN
NORMAL AND UNDERFED ALBINO RATS
AT DIFFERENT AGES

C. A. STEWART

Institute of Anatomy, University of Minnesota, Minneapolis

ONE FIGURE AND THREE TABLES

CONTENTS
Meatertalvandrmethodsee cic r mnt tant ns ce? cicctiet Montiel oe eat eet eae 512
JBI eee ROBIE te ROA 1 REAL ARE oh CG AA AE RR PODS uae Gea O BGC Ua een) 2 515
(CHIE oF ADT, SHON es EME oh LPO ein ot Cay he a a | A eet eee RON eRe PPh. RO eT 519
Brain ES GCMs errr ae Rye ee ee eels oth ie ck poe SONG EE Re eT meas 521
(Crests) oy sbi livb cates ot aya lag MOR ls aun Bt Ct Ca Alb dc OER gk Me lta 522
Olfactory bulbs 3h. Ares b erie. ck. Po ee, Fae ee ae 523
DISCUSSIONS. are acy Ee SPN LCR he hE ARES ESO. Se a ee 524
SS URTNTET OTA ot ian Meee ee ee Pe ED OP, a! can Sheep nog RE cae 526
SMUD OETA Vise raters Crores ee A ASN cet tao a cys. 5 ea ocla peat tctoend 6 ots EE ti 527

In connection with an earlier study of the changes in the rela-
tive weights of the various organs in underfed albino rats (Stewart,
’18b), the brain was observed to manifest a remarkable tend-
ency toward continued growth in very young animals, even when
increase in body weight was prevented. The work has been
extended in the present investigation to a more detailed con-
sideration of the growth of separate parts of the brain in severely
stunted rats. In addition, a considerable number of observa-
tions was made on the weights of different parts of the brain in
normal rats at various ages. This phase of the work, however,
was discontinued when I learned that Prof. H. H. Donaldson,
of The Wistar Institute of Anatomy, Philadelphia, had under-
taken the latter problem upon an extensive scale. Fortunately,
we had each selected the same brain subdivisions for considera-
tion, so that direct comparison of our results is possible. Dr.
Donaldson has kindly furnished me with a record of his data for

511

512 Cc. A. STEWART

stock albino rats (presented in part in a Harvey Lecture, Decem-
ber, 1916) which in general are in agreement with my own observa-
tions upon normal animals. Only my own data are presented
in this paper, however. This opportunity is taken to acknowl
edge my indebtedness to Prof. C. M. Jackson for valuable
advice given during the course of the present experiments.

MATERIAL AND METHODS

In the present investigation the brains of 64 normal (31 males,
33 females, table 1), and of 29 test rats (19 males, 10 females,
table 2) were used. Among the 64 normal rats are included 22
individuals which also served as the direct controls for the test
rats. The rats used were all Albinos (Mus norvegicus albinus)
from the colony in the Institute of Anatomy here.

The number and sex of the normal animals killed at the selected
periods between birth and adult age are shown in table 1. Of the
direct controls (table 2), 12 rats (8 &, 4 @) were killed at birth
(average weight 4.7 to 5 grams), 9 rats (5 &, 4 2) at approxi-
mately 10 grams, and one male at 12 grams body weight.

The test rats were repeatedly starved by isolation from the
mother for various periods as described elsewhere (Stewart,
18b). In this manner 15 individuals (9 #, 6 2) were held
approximately at birth weight for periods ranging from 5 to 18
days; and 13 rats (9, 4 9) were permitted to increase slightly
in weight reaching approximately 10 grams at 3 weeks of age.
In addition one male was weaned when 21 days old, body weight
10.5 grams, and was placed upon a limited diet of whole wheat
(Graham) bread and whole milk. At 56 days of age this indi-
vidual weighed only 12 grams.

It will be noted that the average final body weight is prac-
tically the same for the control and the test rats of each group
(table 2). In comparing the data for the normal and the starved
individuals, the slight differences existing in body weight have
been disregarded. This seems justified since the error involved
is small and cannot obscure the changes produced by the experi-
mental conditions. Strictly speaking, however, a slight correc-
tion should be made as previously noted (Stewart, ’18 b).

PARTS OF BRAIN

IN NORMAL AND

TABLE 1

UNDERFED RATS

513

Number and sex of rats, body weight and length, and weight of the brain with the
percentage weights of its various subdivisions in normal rats at various ages

Oe CC eC a a a a

nse
Qy

diately measured in the usual manner.

NUMBER, SEX, AND AGE
OF RATS

o', 4 9, Newborn

OPN GAN Siscesereray cera:
OE RANOAVISR cme e ts ccc
OROAdaVS: «crac ees
GiORG ay, San sere eer
ils I Cie ts) CSE oe oe
Hp Oe) Clini panleok
Cee Or 10 davseek ss: «
Oreliliday sry. ere ts
Cpl? CaS nae
OFA aay Si peee co cee
Sil pO 5 PALS. CONT on ae
GS) OAS OU NIETS m Glee nicola
OGIO Wichac ae eo bear
iy) 22), 42:6) daiys. o...
oO, 2) 9), 49:6 days... .
Gil, OBC o o.b:6.0 ota piers
Ct 0) Gays.2.5:
cle Ora ays ac
Cle Ore 2 adaysn..:
Ceecmern4ordaysenns:

>

’

GROSS
BODY
WEIGHT

164.

{ & 357 days..|c7257.
| 9 454 days..| 9213.

BODY
LENGTH

mS & ot or
ee Shee
Nears) KS)

=>

for)
wo orm Ww wy

o>
oon

86.08
97.0
105.0
126.3
115.6
141.0
149.04
176.0
169.5
182.5
0212.0
O19 G0

PER CENT PER CENT|? 2% CENT
BRAIN. ae fee Hs ars
WEIGHT | cERE- eae CEREBEL- gee?
BRUM LUM heh
grams
0.2086} 64.4] 29.3 3.65 Deol
0.2640! 62.4|] 30.38] 4.28 3n12
0.3545} 67.6 PATO) | Wee! iL .aitl
0.4400} 68.6 22.5 0.43 | 3.47
OP5135), 694) 92224286 Pe (6
0.6259} 71.7 18.8 (0},:1395) 2.93
0.6969} 71.4 19.1 Orde |an Ls
0.6699} 71.2 IRS3FS)! ||| 8 saR 2.65
0.7451} 70.1 18.7 8.06 | 3.14
0.6838] 70.9 19.3 7.01 2.79
0.9994) 69.2 6 Ose 3.04
1.2800) 67.1 1622) 258 3.69
1.2087} 65.1 LGRGM S25 4.47
1.3500} 65.0 HGeg 1133. 7 4.33
1.4889} 64.3 ff} || 1133. 4.83
12 2026/2 63a 1883 | 1433 4.15
1.5856} 63.7 Wes a 14a 4.62
1.5962} 63.6 18.0 | 13.9 4.58
1.6084, 64.4 18.8 | 13.9 2.90
1.6839) 61.4 19.4 | 14.1 5.01
Pa ZOLS)> "6201 203) P38 3.81
1.8100) 60.8 21.8 | 14.6 2.92

1 Average of 10 individuals.
2 Average of 2 individuals.
3 Average of 5 individuals.
4 Average of 6 individuals.

5 Not recorded.

The rats were killed either by chloroform or (in a few cases)
by bleeding. The body (nose-anus) and tail lengths were imme-

The head was subse-

quently severed at a point immediately behind the foramen
magnum. The brain was then carefully removed (care being
exercised to preserve the cerebellar paraflocculi) and weighed
in a closed container on balances accurate to 0.1 mgm.

514 Cc. A. STEWART

The brain was next placed upon a moist plate of glass and its
various parts dissected as follows. The olfactory bulbs were
removed by a vertical incision at the point where they pass
beneath the frontal lobes of the cerebrum. The cerebellum was
then removed by severing its various crura or peduncles. Finally
the cerebrum was separated from the brain stem by an incision
immediately anterior to the superior colliculi passing through
the anterior part of the crura cerebri. The cerebrum thus
included the telencephalon (except olfactory lobes) and dien-
cephalon, and the brain stem included the midbrain, pons, and
medulla oblongata. The four brain subdivisions thus obtained
were placed in a moist chamber and later carefully weighed in a
closed container.

In all cases there is some difference between the total weight
of the separate parts and the initial brain weight, due no doubt,
either to evaporation from, or to fluid adhering to, the subdivi-
sions weighed. Fortunately, however, the error is generally
small and insignificant, especially as compared with the changes
in weight that have occurred in the test rats. Based on the
assumption that the error is probably distributed more or less
proportionately among the various portions of the brain weighed,
an attempt was made to correct the existing error n computing
the percentage for each subdivision, by using the total weight of
the separate parts rather than the original brain weight.

The observations in table 1 upon normal rats less than three
weeks of age are grouped only in instances where there were two
or more individuals of the same age. Later, when the brain
growth is less rapid, the data have been averaged, grouping indi-
viduals differing a few (usually three or four) days in age. In
the case of the eight adult rats only is there any considerable
range in ages. Since the sexual difference in brain weight in
animals of corresponding weight is comparatively small (Don-
aldson, ’08, ’09), the observations for males and females of each
group have been combined. This is also justified by the rela-
tively small number of observations, since the individual varia-
tions would obscure any existing difference according to sex.

PARTS OF BRAIN IN NORMAL AND UNDERFED RATS’ 515

In table 2 the data for the control groups and for the test rats
are likewise grouped, only the averages being given. The
original individual observations will be filed at The Wistar
Institute of Anatomy and Biology (Philadelphia), where they
may be consulted by those interested.

A preliminary report of the present investigation appeared in
the Proceedings of the American Association of Anatomists,
Minneapolis Meeting, December, 1917 (Stewart, ’18a).

BRAIN

The weight of the entire brain (table 2) is considerably higher
in the various groups of test rats than in the corresponding
younger controls of the same body weight. In the fifteen
individuals (9 o&, 6 @) held at birth weight for various periods
there is an increase from an average (sexes combined) of 0.2086
gram in the newborn controls to 0.4468 gram in the test rats,
an increase of about 114 per cent. An inspection of the indi-
vidual data in table 2 shows that the increase is greater in those
rats held at maintenance for longer periods.

As may be observed in table 2, the body length also increases,
although the body weight is held constant. The brain weight ~
is also much greater in the stunted animals than in normal
rats of the same body length, although the difference is not so
great as when those of the same body weight are compared.

In the test rats weighing about 10 grams at 3 weeks the rela-
tive increase is less, amounting to approximately 33 per cent;
while at 56 days with body weight at 12 grams the excess of brain
weight in the test rats is about 30 per cent. In an earlier report
(Stewart, 718 b) the brain in rats underfed from birth and weigh-
ing 10 grams at 3 weeks of age was found to exceed that in normal
rats of corresponding body weight by about 60 per cent, which is
considerably more than the excess obtained for a comparable
group in the present series. In general, however, the results
agree in showing a stronger growth tendency of the brain in the
younger and smaller rats.

The increase in brain weight in spite of underfeeding with
nearly stationary body weight is probably best shown in figure 1

ALS

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4

fff és
//

yf

AC

MY

Fig. 1 A and A’, dorsal and ventral view, respectively, of brain of normal
newbornrat. Body weight, 5.4 grams. Brain weight, 0.238 gram. X 3.

B and B’, dorsal and ventral view, respectively, of brain of rat kept at birth
weight by underfeeding for 20 days. Body weight, 5 grams. Brain weight,
0.506 gram. X 3.

(Continuation of explanation of figures on page opposite.)
516

PARTS OF BRAIN IN NORMAL AND UNDERFED RATS 5G

TABLE 2

Number, sex, weight, and length, with weights of the brain and its various parts in
normal and underfed rats at different ages

GROSS OLFAC-
NUMBER, SEX, AND AGE OF RATS izopr. Leto | BRAIN | SESe’ | srem Baie pony,
grams mm. grams

8 o&', Control,-newborn.... 4.97} 49.1! | 0.2106) 0.1375} 0.0622} 0.0079) 0.0055
1 Nestitchyoidays tis: 4.7 | 56.0 | 0.3653} 0.2481) 0.1085) 0.0213) 0.0151
i Mest. co) (Otdaye onc: 5.5 | 56.0 | 0.3872} 0.2724) 0.0940) 0.0232) 0.0118
Tl GREK Ke GROCERIES age ao os 4.6 | 55.0 | 0.38743} 0.2563) 0.1027) 0.0213) 0.0150
iL Westin tala ated ope 4.8 | 53.0 | 0.4711] 0.3368) 0.1014) 0.0307) 0.0154
IeMesti ct wl2daysasese ss. 5.8 | 57.0 | 0.5348] 0.3742] 0.1143] 0.0356) 0.0246
ipMestacH poor asta cie as 5.0 | 57.0 | 0.4790) 0.3413) 0.1134) 0.0335) 0.0192
tt Nest. ct elaidayes ese ac. 5.5 | 59.0 | 0.5404) 0.3845] 0.13834) 0.0346) 0.0242
le Mestrod mad avisuccsae 5.5 | 57.0 | 0.4920) 0.3464) 0.1062) 0.0334) 0.0220
iiMest: ot; 14; dayse cs 4: 5.8 | 60.0 0.4571) 0.3247) 0.1053) 0.0291) 0.0180

Average, 10.6 days...... 5.24] 56.7 | 0.4557| 0.3205} 0.1088) 0.0292) 0.0184
An OP ANG wDOLmM use a oe 4.65| 47.5? | 0.2046) 0.1323) 0.0611! 0.0074] 0.0048
eesti eno wd aSeney ee 4.9 | 54.0 | 0.3603) 0.2549) 0.0999) 0.0205) 0.0149
ieReSta Ori lladayse.. oa. 4.0 | 52.0 | 0.3728} 0.2564) 0.1033) 0.0212) 0.0154
I PMEStAC LoL ase mae 4.8] 55.0 | 0.4434) 0.3139) 0.1018) 0.0262) 0.0180
MNES ts Om 2icdayisere., ve 5.0 | 54.0 | 0.5079] 0.3444| 0.1068} 0.0328) 0.0204
iGdest, Op lavdayse, esse. 5.0 | 56.0 | 0.4019} 0.2892) 0.0872) 0.0256) 0.0142
femest; C218 dayash.. . 5... 5.1 | 54.0 | 0.5212) 0.3732) 0.1180) 0.0415) 0.0216

Average, 12 days....... 4.8 | 54.1 | 0.4346} 0.3053) 0.1028) 0.0280] 0.0174
5 Control o&, 9 days...... 10.2 | 63.0 | 0.6309] 0.4589} 0.1280) 0.0396) 0.0181
OrVest tot 22\dayese. 1... 10.4 | 67.8 | 0.8837| 0.6169) 0.1578) 0.0956) 0.0265
4 Control 9, 9.5 days..... 9.6 | 63.3 | 0.6845} 0.4830) 0.1282} 0.0497| 0.0212
4 Test. 9 ,) 22) days. .../... 9.6 | 65.9 | 0.8444] 0.5894) 0.1477) 0.0896) 0.0229
1 Control 6, 9 days...... 12.0 | 69.0 | 0.7324) 0.5304} 0.1340) 0.0556} 0.0240
Ii West ct, oodaysr....... 12.0 | 77.0 | 0.9544} 0.6312) 0.1856} 0.1210) 0.0410

1 Average of 7 individuals.
2 Average of 3 individuals.

On comparison with the brain of the newborn rat (A and A’), it is evident that
during underfeeding (maintenance) not only the brain as a whole, but also the
olfactory bulbs and tracts, cerebral hemispheres, colliculi, cerebellum and floc-
culi, tuber cinereum, pons, and medulla continue to grow in young rats in spite of
practically no change in body weight for 20 days. Comparison with the normal
brain at 20 days (C and C’), however, shows that the growth of the various parts
of the brain mentioned above, while considerable, nevertheless has been greatly
retarded.

C and C’, dorsal and ventral view, respectively, of brain of normal rat at 20
days of age. Body weight, 17.5 grams. Brain weight, 1.047 grams. X 3.

518 Cc. A. STEWART

(a, a’, newborn control; b, b’, test rat). As compared with the
control of the same body weight, not only the various subdivi-
sions weighed, but also the olfactory tracts, tuber cinereum,
corpora quadrigemina, and especially the para flocculi are evi-
dently much larger in the starved rat.

Although considerable brain growth thus occurs during mainte-
nance of constant body weight in young rats, nevertheless it
occurs at a greatly retarded rate in comparison with the normal
growth during the corresponding period of time. This is so
well shown in figure 1 (6, b’ and c, c’) that a lengthy discussion
is unnecessary.

TABLE 3

Comparison of relative intensity of growth of various parts of the brain in normal
and test rats

PERCENTAGE BY WHICH THE WEIGHT OF THE
VARIOUS PARTS OF THE BRAIN

At 11 days es that |At 3 weeks exceeds that

at birth in normal 10-gram rats
Normal Test Normal Test
@erehellluinmve... eee ss Gece cee 696 272 274 113
ACCOR, WS. | Ge. Gk olen seis eee eam 351 240 144 30
Gere rue oe a eee eae mne 293 131 85 29
STAT SETI Ge pee ae ears 130 (2 63 20

In older rats held at maintenance for various periods, investi-
gators in general have noted practically no change in the brain
weight. Thus Hatai (’08) found the brain weight in stunted
rats to be practically identical with that for normal younger
rats of the same body weight. In a large series of rats studied
by Donaldson (’11), after maintenance from 30 to 51 days of
age, the brain exceeded the calculated initial weight by only 3.6
per cent. Jackson (’15 a) and Stewart (’16) conclude that
there is practically no change in the weight of the brain in rats
held at maintenance for various periods starting at 3 weeks of
age. Holt (’17) noted a slight increase in brain weight in under-
sized rats fed upon an unsuitable diet of whole corn after the
period of weaning. |

PARTS OF BRAIN IN NORMAL AND UNDERFED RATS 519

Aron (’11) publishes data showing in a few instances the brain
weight in greatly stunted dogs practically equal to that in normal
heavier dogs of the same age. However, no observations were
made concerning the initial brain weight at the beginning of the
experiment and the extent of the brain growth which apparently
occurred during the underfeeding is therefore uncertain.

It is interesting to note that Variot and Lassabliere (’09)
found the growth of the brain in underfed infants to be retarded
less than the growth in body weight, the brain thus increasing
at the expense of other tissues of the body. This observation
agrees with my own results for young albino rats.

During severe starvation a slight decrease in the weight of the
brain was noted by Bechterew (’95) in puppies and kittens, and
by Hatai (’04) in young rats. Acute and chronic inanition in
adult rats causes but little if any loss in absolute brain weight
(Jackson, ’15b). A very complete summary of the literature
bearing upon the effect of inanition upon the brain is given by
Jackson (’15b).

CEREBRUM

If the percentages are calculated from the combined weight
of the separate brain parts, it appears that the cerebrum (table 1)
(telencephalon and diencephalon, excluding olfactory bulbs)
during normal growth increases from an average of slightly more
than 64 per cent of the entire brain at birth (sexes combined)
to a relative maximum of approximately 71 per cent during the
early part of the second week. Thereafter, although increasing
in absolute weight, the cerebrum forms a progressively smaller
proportion of the brain, decreasing to an average of approximately
67 per cent (sexes combined) at three weeks, and to about 61 per
cent at one year and later. My results agree fairly well with
those of Hatai (15) for adult individuals of approximately
similar body length, with those of Sugita (’17) for the rat during
the first 150 days, and also with the unpublished data of Donald-
son (personal communication). Slight differences appear which
are presumably due partly to experimental error and partly to
normal variability in the size of the brain segments.

520 Cc. A. STEWART

In the stunted rats kept at birth weight for various periods,
and also in those weighing approximately 10 and 12 grams at
three and eight weeks, respectively, the weight of the cerebrum
(table 2) considerably exceeds that of the normal younger con-
trols of corresponding body weight. For the first group (sexes
combined) there is an increase from an average of 0.1358 gram
in the controls to 0.3144 gram in the test rats, an increase of more
than 131 per cent. In the test rats at three weeks (22 days)
the increase in the cerebrum is relatively less, amounting to
approximately 29 per cent, and at eight weeks it has decreased
to about 19 per cent.

As to relative proportions, the percentage weight of the cere-
brum is slightly higher in the test rats kept at birth weight var-
ious periods than in the controls, the apparent increase being
from an average of approximately 64 per cent of the combined
weight of the separate parts in the latter to 67 per cent in the
stunted individuals. The range in the test rats is from about
63 per cent to 69 per cent, increasing in general with the length
of the experiment. If we now compare the corresponding change
in relative proportion of the cerebrum during normal growth, it
is evident that with the increase in brain weight from birth
there is normally an increase in the percentage that the cerebrum
forms of the entire brain, similar and practically equal to that
noted in the brain of equal size in the stunted rats.

In the test rats weighing about 10 grams at three weeks, how-
ever, there is apparently a slight decrease (71 to 69 per cent) in
the relative size of the cerebrum as compared with the controls
of the same body. weight. Likewise during normal growth there
is a similar decrease in the percentage weight of the cerebrum
while the brain weight is increasing from about 0.6500 gram to
0.8700 gram. At eight weeks of age the cerebrum in the test
rats, though absolutely larger, is relatively smaller than in the
control. This change likewise is probably associated with the
usual tendency toward declining relative size of the cerebrum in
normal brains of corresponding weight, although the difference
in this case is greater than would be expected from the apparent
change during normal growth.

t

PARTS OF BRAIN IN NORMAL AND UNDERFED RATS 521

In general, therefore, the data indicate that during the per-
sistent growth of the brain, in very young rats stunted by
underfeeding, the cerebrum (telencephalon and diencephalon)
maintains the same relative size as in the normal brain of
corresponding weight.

BRAIN STEM

The percentage weights (calculated from the combined weights
of separate brain subdivisions) for the brain stem (including.
midbrain, pons, and medulla oblongata) show a relative decrease
from an average of about 29 per cent of the normal brain at
birth to about 16 per cent at three weeks. Subsequently the
growth of the brain stem is more rapid than that of the brain
as a whole, resulting in a gradual increase in relative weight to
an average of about 22 per cent in the adult rats. The normal
initial decrease and subsequent increase in the relative size of
the brain stem is in agreement with the observations by Sugita
(17) and Donaldson (unpublished data). As compared with
adult animals of corresponding body length, my results corre-
spond fairly well with those obtained by Hatai (’15).

In the stunted rats held at birth weight for various periods,
and also in the other groups of test animals, the weight of the
brain stem (table 2) in all cases considerably exceeds that in the
younger controls of the same body weight. In the first group
there is an increase from an average of 0.0618 gram (sexes com-
bined) for the controls to 0.1064 gram in the test rats, an increase
of approximately 72 per cent. In the test rats at three and eight
weeks of age, the increase in brain stem weight amounts to about
20 and 39 per cent, respectively. :

As to relative proportions, the brain stem in the rats held at
birth weight apparently decreases from about 29 per cent (in the
controls) to about 22 per cent of the brain weight. In the test
rats at 22 days the brain stem weight has further decreased to
about 18 per cent, as compared with 19 per cent in the controls
of similar body weight. In the test rat at 56 days, however,
the brain stem has slightly increased to 19 per cent (18 per cent
in the control).

THE JOURNAL OF COMPARATIVE NEUROLOGY, VOL. 29, NO. 5

Hee C..A. STEWART

In these cases, however, the relative size of the brain stem
in the brain of the stunted rats corresponds approximately to
that in normal brains of the same weight. The only exception
is that of the single test rat in which the brain stem should be
relatively slightly smaller than in the control, according to the
change found in the normal brains of corresponding weights.
The difference is slight, however, and may be obscured in this
case by individual variation or experimental error.

-On the whole, therefore, it appears that during the persistent
growth of the brain, in very young rats stunted by underfeeding,
the brain stem (midbrain, pons, and medulla) maintains approxi-
mately the same relative size as in the normal brain of corre-

sponding weight.

CEREBELLUM

Calculations from the data obtained show that during post-
natal growth the cerebellum (table 1) apparently increases
rapidly from an average of about 3.7 per cent of the total weight
of the separate parts of the brain at birth (sexes combined) to
about 14 per cent at seven weeks of age, and maintains approxi-
mately this relative weight in the adult albino rat. In general
these results agree fairly well with those obtained by Hatai
(15) (for adult rats of body length similar to that of my adult
controls), by Sugita (’17) (from birth to 150 days of age), and by
Donaldson (unpublished data).

In the rats underfed for various periods the cerebellum (table
2) shows a remarkable growth. In the individuals held at birth
weight the cerebellum has increased from an average of 0.0077
‘gram in the controls (sexes combined), to 0.0287 gram, an
increase of over 272 per cent. At three and eight weeks of age
the increase in the test rats is approximately 113 and 118 per
cent, respectively, as compared with the younger controls of the
same body weight.

As to relative proportions, the cerebellum is in all cases found
relatively much larger in the brain of the test rats, in comparison
with that in control rats of the same body weight. If the per-
centage of the brain weight formed by the cerebellum in the test

PARTS OF BRAIN IN NORMAL AND UNDERFED RATS 523

-rats (table 2) is compared with that in normal brains (table 1)
of the same weight, however, the agreement is surprisingly
close. It is therefore apparent that during the persistent growth
of the brain in underfed young rats the cerebellum, like the seg-
ments previously considered, maintains approximately the same
relative size as in the normal brain of corresponding weight.

OLFACTORY BULBS

Calculations from my data (table 1) indicate that the olfactory
bulbs, although rather variable, in general increase from an
approximate average (sexes combined) of 2.5 per cent of the
total weight of the separate parts of the brain at birth, to about
3.7 per cent at three weeks, and probably reach a relative max-
imum of about 4.8 per cent at six or seven weeks of age. Sub-
sequently their relative weight decreases in the majority of
cases, reaching about 2.9 per cent in the adult. Attention should
be called to the fact that the data indicate not only a relative
decrease, but even an absolute loss in the weight of the olfactory
bulbs in the older rats. In general my results agree with those
obtained by Hatai (15), Sugita (17), Holt (17), and Donaldson
(unpublished data) for normal albino rats, the existing differ-
ences probably being due partly to normal variability and partly
to experimental error.

In the stunted rats the olfactory bulbs greatly exceed those
in the younger controls of the same weight (table 2). For the
group held at birth weight there is an increase of nearly 240 per
cent. For the other test animals at three and eight weeks of
age the increase is less marked, amounting to 30 and 71 per cent,
respectively.

The percentage that the olfactory bulbs form of the entire
brain weight, especially in the case of the individuals kept at
birth weight for various periods, averages higher than that for
the newborn controls. According to my data, accompanying an
increase in brain weight from approximately 0.2100 gram to
0.4500 gram there is normally a considerable increase in the
relative weight of the olfactory bulbs, although apparently not
so great as in the stunted rats with brains of corresponding weight.

524 Cc. A. STEWART

Thus the olfactory bulbs appear relatively larger in the stunted
rats than in normal rats of the same brain weight.

For the group fasting three weeks the relative increase is slight
and inconstant. In the normal rats with corresponding brain
weight (0.6309 to 0.8837 gram) the relative weight of the olfac-
tory bulbs is likewise nearly stationary, though somewhat var-
iable. This is in agreement with Holt (’17), who found the rela-
tive proportions of the olfactory bulbs to remain practically
unchanged in rats undersized after four and eight weeks of feed-
ing upon an unsuitable diet of whole corn.

The data for my rat underfed from birth to eight weeks indi-
cate an apparent increase in the relative weight of the olfactory
bulbs, which is in accordance with the general tendency toward
an increase in the relative size of olfactory bulbs in normal rats
with brains of corresponding weight. Miss Holt noted a tend-
ency for the bulbs to increase in relative weight during pro-
longed defective feeding in rats weighing about 50 grams.

On the whole it therefore appears that during the persistent
growth of the brain in underfed young rats the olfactory bulbs
tend to maintain a relative size similar to that in the normal
brain of corresponding weight. In the youngest and smallest
group, however, they apparently become relatively hypertro-
phied and appear relatively larger than in normal animals with
the same brain weight.

DISCUSSION

Quite uniformly the results of experiments have shown that
the brain demonstrates a marked ability to grow when increase
in body weight is prevented by underfeeding only in very young
animals and at a time when the normal growth of the brain is very
pronounced. There is, therefore, apparently a definite relation
between the increase in size accomplished during starvation and
the normal growth power possessed by the organ at the time
when underfeeding is commenced That this dependency upon
the intensity of the growth impulse applies also to the various
parts of the brain is evident upon comparison of the relative
rapidity of growth of the various parts of the brain in young rats.

PARTS OF BRAIN IN NORMAL AND UNDERFED RATS 525

As is shown in table 3, in both the normal and test rats, the
cerebellum manifests the strongest growth power, the olfactory
bulbs, cerebrum, and brain stem following in the order mentioned.
The perfect agreement in this respect between the control and
test individuals can hardly be considered a mere coincidence, but
more probably is the expression of inherent normal tendencies.

Furthermore, it has been pointed out that with the growth of
the brain in the stunted rats, the various portions of the brain
undergo practically the same changes in relative size as found in
normal animals of the same brain weight. The olfactory bulbs
which show an overgrowth (in the younger group) apparently
form the only notable exception to this rule. In general, there-
fore, it appears that no:mal growth tendencies foreshadow the
character and the amount of the changes that accompany
growth of the brain during underfeeding. In other words, the
growth of the brain in the stunted rats appears normal, so far as
the changes in the size of the constituent parts is concerned.

The tendency for the different brain subdivisions to maintain
largely the normal proportions during starvation is in marked
contrast to the change in the relative weights produced among
various organs of the body as to result of underfeeding. Jack-
son (715, p. 152) also noted that in some cases (e.g., liver, alimen-
tary canal) there is a certain degree of parallelism between the
normal growth tendency and the behavior of organ weight in
young rats when the body weight is held constant. Further-
more, the greatest number of organs showing growth during
maintenance (constant body weight) occurs in very young rats
during the normal period of most rapid growth (Stewart, ’18).
The above-mentioned principle therefore applies not only to the
brain and its various subdivisions, but also to many other organs.
However, there are certain exceptions to this rule, as pointed out
by Jackson.

It is interesting to note that the marked growth of the brain
in rats stunted by underfeeding occurs only at a period when the
normal increase in size is still due partly to cell multiplication,
especially in the cerebellum (Allen, 712). This is a phase of the
inanition problem worthy of further investigation.

526 Cc. A. STEWART

SUMMARY

1. The weights of various parts of the brain were studied in 64
normal rats at various ages, and also in 29 test animals, of which
15 individuals were held at birth weight by underfeeding for
periods ranging from 5 to 18 days of age, 13 rats were permitted
to increase slightly in weight reaching approximately 10 grams at
3 weeks, and one male weighed 12 grams at 56 days of age.

2. According to the data available, the cerebrum (excluding
olfactory bulbs) increases from a normal average of slightly
more than 64 per cent of the entire brain at birth, to a maximum
of about 71 per cent during the early part of the second week,
but subsequently forms a progressively smaller proportion of the
brain, decreasing to an average of about 61 per cent in the adult.

The brain stem (including midbrain, pons, and medulla
oblongata) decreases from a normal average slightly exceeding
29 per cent of the brain at birth to about 16 per cent at 3 weeks,
but later increases reaching a relative weight of about 22 per
cent in adult animals.

The cerebellum increases rapidly from an apparent average
of 3.7 per cent of the entire brain at birth to about 14 per cent
at 7 weeks of age, and thereafter.

The olfactory bulbs, while variable, in general increase from
an average of about 2.5 per cent at birth to 3.7 per cent at 3
weeks, and probably reach a relative maximum of slightly more
than 4.5 per cent at 6 or 7 weeks of age. Subsequently there is
a gradual decrease in relative weight to about 2.9 per cent in the
adult rat. The data indicate not only a relative decrease, but
even an absolute loss in the weight of the olfactory bulbs in the
older rats.

3. For the stunted rats the weight of the brain as a whole in
the individuals held at birth weight for various periods averaged
114 per cent higher than that in the controls, whereas the excess
in test rats weighing 10 grams at 3 weeks and 12 grams at 8 weeks
of age was 33 and 30 per cent, respectively.

As shown in figure 1, the increase is shared not only by the
various brain parts dissected and weighed, but also by the ol-
factory tracts, tuber cinereum, colliculi, and the paraflocculi.

PARTS OF BRAIN IN NORMAL AND UNDERFED RATS 527

Of the various parts of the brain, the weights of the cerebellum,
olfactory bulbs, cerebrum, and brain stem exceed those for the
control rats of corresponding weight in the order mentioned,
the greatest change occurring in the individuals kept at birth
weight for various periods. In this group of individuals the
different parts of the brain in the order above listed show an
increase of 272, 240, 131, and 72 per cent, respectively.

In the persistent growth of the brain in the young rats stunted
by underfeeding, the various parts of the brain in general preserve
approximately the same relative weight as in normal individuals
of the same brain weight. The olfactory bulbs apparently
form an exception to this rule, as they become abnormally large
in the younger group of stunted rats. This apparent hypertrophy
may be due, however, to experimental error.

BIBLIOGRAPHY

ALLEN, E. 1912 The cessation of mitosis in the central nervous system of the
albino rat. Jour. Comp. Neur., vol. 22, no. 6, pp. 547-568.

Aron, Hans 1911 Nutrition and growth. Philippine Jour. Science, vol. 6,
no. Uy pps L-5i

Donaupson, H. H. 1908 A comparison of the albino rat with man in respect to
the growth of the brain and of the spinal cord. Jour. Comp. Neur.,
vol. 18, no. 4, pp. 345-392.
1909 On the relation of the body length to the body weight and to the
weight of the brain and of the spinal cord in the albino rat (Mus nor-
vegicus var. albus). Jour. Comp. Neur., vol. 19, no. 2, pp. 155-167.

Hara, 8. 1908 Preliminary note on the size and condition of the central nerv-
ous system in albino rats experimentally stunted. Jour. Comp.
Neur., vol. 18, no. 2, pp. 151-155.
1915 The growth of the body and organs in albino rats fed with a
lipoid-free ration. Anat. Rec., vol. 9, no. 1, pp. 1-20.

Hott, C. M. 1917 Studies on the olfactory bulbs of the albino rat. In two
parts: I. Effect of a defective diet and of exercise. II. Number of
cells in bulb. Jour. Comp. Neur., vol. 27, no. 2, pp. 201-259.

Jackson, C.M. 1915 Changes in the relative weights of various parts, systems,
and organs of young albino rats held at constant body weight by under-
feeding for various periods. Jour. Exp. Zool., vol. 19, No. 2, pp. 99-156.
1915e Effect of acute and chronic inanition upon the relative weights
of the various organs and systems of adult albino rats. Am. Jour.
Anat., vol. 18,no.1. Also abstracted in Proc. Amer. Assn. Anatomists.
Anat. Rec., vol. 9, no. 1, p. 90.

528 Cc. A. STEWART

Stewart, C. A. 1916 Growth of the body and of the various organs of young
albino rats after inanition for various periods. Biol. Bull., vol. 31,
no. 1, pp. 16-51.

1918 a Weights of the various parts of the brain in normal and under-
fed albino rats at different ages. (Abstract.) Proc. Amer. Assn.
Anatomists. Anat. Rec., vol. 14, no. 1, p. 51.

1918 b Changes in the relative weights of the various parts, systems,
and organs of young albino rats underfed for various periods. Jour.
Exp. Zool., vol. 25, no. 2, pp. 301-353.

Suerra, N. 1917 Comparative studies on the growth of the cerebral cortex.
I. On the changes in the size and shape of the cerebrum during post-
natal growth of the brain. Albino rat. Jour. Comp. Neur., vol.
28, no. 3, pp. 495-510.

VARIOT ET LASSABLIERE, P. 1909 Autonomie du developpement de l’encéphale,
dans les retards de la croissance chex les jeunes enfants. C. R. Soe.
Biol., Paris, T. 66, pp. 106-108.

AUTHORS’ ABSTRACT OF THIS PAPER
ISSUED BY THE BIBLIOGRAPHIC SERVICE

ON THE INCREASE IN THE DIAMETERS OF NERVE-
CELL BODIES AND OF THE FIBERS ARISING
FROM. THEM--DURING THE *LATER
PHASES OF GROWTH (ALBINO RAT)

HENRY H. DONALDSON AND G. NAGASAKA
The Wistar Institute of Anatomy and Biology

THREE CHARTS AND ONE FIGURE

In the later phases of growth some neurons increase not only
in the diameter of the cell body, but also in the diameter of the
fiber or fibers growing from the cell body. Moreover, in the
case of the fiber, the increase occurs not only in the diameter of
the axis cylinder, but, when myelinated, in the myelin sheath
also.

In order to determine more precisely how this increase in
diameter is distributed between the cell body and the fiber
coming from it, we have undertaken to observe during the later
phases of growth what takes place in two classes of neurons at the
level of the seventh cervical segment of the spinal cord of the
albino rat.

The neurons chosen for study were a) those with the largest
cell bodies in the ventro-lateral group of the ventral horn and the
ventral root fibers which were assumed to come from them, and,
b) those with the largest cell bodies in the corresponding spinal
ganglion together with the largest fibers in both the dorsal root
and in the nerve just distal to the ganglion. This seventh seg-
ment of the spinal cord with ganglia and roots was removed from
a series of twenty-four male albino rats which are listed in table 1.

As table 1 shows, these rats range from 17 to 360 days in age
and from 18.7 to 316.3 grams in body weight.

As one object of the study was to determine whether the nerve
fibers continued to increase in diameter after the cell bodies had

529

530 HENRY H. DONALDSON AND G. NAGASAKA

TABLE 1

Data on the twenty-four normal male albino rats used for this study

NUMBER AGE BODY WEIGHT BODY LENGTH TAIL LENGTH
days grams mm. mm.
I 17 18.7 86 61
II 17 18.7 88 61
Til - 26 25.2 97 74
IV 26 25.2 96 72
Vv 29 43.3 122 94
VI 29 42.8 120 88
VII 39 59.2 130 110
VIII 39 58.9 130 108
IX 49 81.0 148 132
x 49 82.0 147 126
XI 81 115.1 168 141
XII 81 114.5 163 140
XIII 85 120.3 185 150
XIV 85 117.0 185 155
XV 104 149.3 190 158
XVI 104 153.5 187 160
XVII 125 178.0 194 155
XVIII 25a 180.8 195 159
XIX 130 233.1 212 185
xX * ~130 228.8 217 173
xXXI 312 243.1 219 176
XXII 312 236.5 213 172
XXIII 360 316.3 234 178
XXIV 360 314.1 235 180

attained their full size, the examination was begun with rats 17
days of age, since at this time some of the cell bodies at least had
reached nearly their full size.

TECHNIQUE

Each rat was tested while alive to make sure that it was quite
normal in its reactions. Rats thus selected were killed with
chloroform, and the body weight, body length, and tail length
recorded, asin table 1. The rat was then completely eviscerated,
as this makes the subsequent dissection easier. The spinal canal
was next opened so as to expose the seventh cervical segment
with its nerves, and both segment and nerves were removed.

DIAMETERS OF NERVE CELLS AND FIBERS 531

To obtain all the data desired, two rats of like age and size
were required. From the left side of one, the two spinal roots,
the ganglion, and a short part of the nerve were removed together.
These were extended to the normal length on a bit of cardboard
and fixed for twenty-four hours in 1 per cent osmic acid. From
the same rat the seventh cervical segment, with the right roots,
ganglion, and nerve attached, was removed and fixed in Bouin’s
fluid for twenty-four hours, according to the procedure de-
seribed by Sugita (17).

Fig. 1 A scheme of the seventh cervical segment of the spinal cord. Levels
of the nerve-fiber sections: At A, section of seventh nerve; at B, section of ven-
tral root; at C, section of dorsal root. 1. The spinal ganglion, cut in longitudinal
section. 2. Transverse section of segment. 3. Plane of longitudinal section of
the segment.

From the second rat of the pair the seventh cervical segment
of the cord, without the nerve roots, was removed and fixed also
in Bouin’s fluid. The nerve roots and nerve fixed in osmic acid
were washed for twelve hours, run through the alcohols, cleared
in xylol, rapidly imbedded in paraffin and cut in sections 8u
thick. The piece of the spinal cord with the ganglion from
the first rat and the piece of cord from the second rat, both
of which had been fixed in Bouin’s solution, were washed for five
minutes in running water, then treated as above, cut in sections
12u thick and stained with thionin.

Figure 1 shows the localities at which the six series of sections
were made. .

532 HENRY H. DONALDSON AND G. NAGASAKA

From the material as represented in figure 1, the following
series of cross-sections of myelinated fibers fixed in osmic acid
were obtained:

At A, in the seventh cervical nerve close to the ganglion.

At B, in the ventral root. ,

At C, in the dorsal root.

Also, the following sections of nerve-cell bodies from material
fixed in Bouin’s fluid:

At 1, a longitudinal section of the spinal ganglion.

At 2, a transverse section of the spinal cord.

At 3, a longitudinal frontal section of the spinal cord (in the
plane of the rectangle—fig. 1).

In the sections from A, B and C, the fibers were cut as nearly
as possible at right angles to their long axes, which made the
cross-section of a myelinated fiber nearly circular in outline.
In this ease but a single measurement of the diameter of the entire
fiber and of the axis, respectively, was made. For measurement
a Zeiss ocular no. 6 and oil-immersion ob]. 2 mm. were used with
the micrometer eyepiece having each division equal to 2u.
Ten of the largest fibers in a single section were thus measured
for each locality.

In the case of the nerve cells, more measurements were neces-
sary because, in the first place, the outline of the cell bodies is not
circular, and, in the second place, it was necessary to measure the
nuclei also.

In the case of the spinal ganglion cells the two maximum diam-
eters at right angles to each other were determined, while one
diameter alone was taken for the nucleus.

In the case of the spinal cord cells the longitudinal diameter
was the longer one, passing through the long axis of the cell and
at right angles to the transverse or short diameter which was
measured through the middle of the nucleus. This is similar to
the method described by Hardesty (’02). Here again, but one
diameter of the nucleus was measured. In each instance the
largest cells in a given section were those measured. These
series of measurements taken on the fibers at A, B, and C, and
on the cells at 1, 2, and 3, furnish the data that are to be consid-

DIAMETERS OF NERVE CELLS AND FIBERS 533

ered. In each instance, both for cells and for fibers, the values
given in tables 2 to 6 are averages based on ten measurements.

In table 2 are given the values for the diameters of the largest
nerve fibers found in the seventh spinal nerve and in the dorsal
and ventral spinal roots, respectively, in twelve albino rats rang-
ing from 18.7 to 316.3 grams in body weight. The measurements
are not only for the entire fiber, but for the axis also. At the
bottom of each column is given the ratio of the diameter at 18.7

TABLE 2

Giving in micra the mean diameters of the largest entire fibers in the seventh cervical
nerve and in the ventral and dorsal roots, together with the diameters of their respec-
tive axes. The ratio between the first and the last measurement stands at the bottom
of each column

SEVENTH NERVE JUST
VENTRAL ROOT DIAMETER] DORSAL ROOT DIAMETER | DISTAL TO THE GANGLION
BODY WBIGET DIAMETER

Entire fiber Axis Entire fiber Axis Entire fiber Axis

grams
18.7 8.8 5.5 8.6 5.4 8.9 5.6
25.0 11.5 Wise 11.8 7.5 11.4 7.2
43.3 11.9 We, 12.0 7.8 11.9 7.5
59.2 12.1 (foe 12.3 7.9 12.2 Wot!
81.0 12.8 7.6 13.2 7.8 13.0 8.0
115.1 13.2 9.0 13.6 9.8 13.6 9.8
120.3 14.3 9.8 14.5 10.0 14.3 9.6
149.3 14.6 9.8 14.8 9.6 15.0 9.8
178.0 17.6 12.7 17.8 12.2 18.1 12.6
233.1 16.7 12.4 Weil 12.4 16.9 12.0
243.1 17.6 11.6 17.6 13.4 WG 13.2
316.3 20.2 14.0 20.3 14.3 19.8 14.2
Ratios....... 12s W255 13253 1:2.6 1: 2.2 1:2.5

grams to that at 316.3 grams of body weight. For the entire
fiber this ranges between 2.2 for the fibers from the nerve and 2.3
for both the ventral root and dorsal root fibers. The difference
is so slight that we conclude that all three sets of fibers increase in
diameter by the same amount. When the ratios for the axes
are considered, it is seen that they also are nearly alike (i.e., from
2.5 to 2.6), but higher than those for the entire fiber, showing
that the axis is growing in diameter somewhat more rapidly than

534 HENRY H. DONALDSON AND G. NAGASAKA

the myelin sheath which encloses it. To this point we shall
return later. .

Passing to the ganglion cells, the measurements obtained for
groups of the ten largest cells in a single longitudinal section
in each of twelve albino rats (the same rats that furnished the
nerve fibers for table 2) are given in table 3.

The first column gives the long diameter, the second the short
diameter, and the third column the ‘computed diameter,’ i.e.,
TABLE 3
Mean diameters in micra of the ten largest spinal ganglion cells in the seventh cervical
ganglion. Long diameter, short diameter, and the ‘computed diameter’—which

is the square root of the product of the long and short diameters. Also the mean

diameters of the respective nuclei. The ratio of the last to the first entry is given
at the foot of each column

_CELL BODY

BODY WEIGHT SERIA

Long diameter Short diameter neue’ Mer
grams '
18.7 26.4 17.6 21.6 10.6
25.0 29.2 18.4 232 10.8
43.3 Sane 19.8 25.6 14.4
59.2 35.2 19.8 29.1 14.8
81.0 36.0 24.0 29.4 15.2
ayer 36.8 25.6 30.8 14.4
120.3 36.6 28 .4 S2E2 1592
149.3 38.4 30.0 33.9 16.0
178.0 39.2 29.8 34.2 16.4
233.1 40.4 34.4 Bf 2 18.2
243.1 41.6 ae 39.4 18.0
316.3 41.8 34.0 BY 17.8
Ratios.cn 4-88 iB ES 11.9 1 28 UE EZ

the square root of their products. These last values approximate
the mean diameters of the cells. . Finally, the last column in the
table gives the diameters of the nuclei.

Determining the ratios for the last two columns, it appears
that the spinal ganglion cells have increased 1.8 times in diam-
eter and the nuclei 1.7 times. This increase is considerable, but
somewhat less than that of the dorsal root fibers or of the fibers
just distal to the ganglion.

DIAMETERS OF NERVE CELLS AND FIBERS San

In table 4 are a series of measurements for the large cell bodies
in the ventrolateral part of the ventral horn of the seventh
cervical segment of the spinal cord as they appear in transverse
section (at 2, fig. 1). The arrangement of the data is as given
in table 3. The increase for the computed diameters is 1.3 for the
cell bodies and 1.2 for the nuclei.

When the corresponding data for the longitudinal section of the
spinal cord (at 3, in fig. 1) are tabulated, they appear as in table 5

TABLE 4

Mean diameters in micra of the ten largest spinal cord cells—from the ventrolateral
area of the ventral horn as they appear in a transverse section. Long diameter,
short diameter, and ‘computed diameter,’ which is the square root of the product
of the long and short diameters. Also the mean diameters of the respective nuclet.
The ratio of the last to the first entry is given at the foot of each column

CELLS
NUCLEI

BODY WEIGHT a PMSA. LL? . oe ba Er) co kee See TD
Long diameter Short diameter Sa v heteyt
grams
18.7 29.4 18.0 2800). 12.8
25.0 30.8 18.0 23.5 13.0
43.3 34.6 18.4 25.2 13.4
59.2 30.4 18.8 25.8 14.4
81.0 34.0 22.0 27.4 14.8
115.0 37.6 21.6 28.6 14.8
120.3 36.0 22.0 28.2 16.0
149.3 38.4 22.4 29.4 15.2
178.0 37.0 22.6 28.9 Toye
Doon 36.6 22.0 28 .4 15.2
243.1 36.4 22.4 28.6 15.2
316.3 36.8 24.4 29.9 15.4
IRATIOBSSsok seo 1:1.3- 1:1.3+ 13148 ele

and show an increase of 1.2 in the diameter cell body and 1.2 in
the nuclei.

The relations represented by the numbers in tables 2 to 5 are.
shown graphically in charts 1, 2, and 3.

In this connection it may be well to repeat the statement that
necessarily two different specimens were used for the cells in the
spinal cord so that the data in tables 4 and 5 are not only from
sections made in different planes, but also from a different series

536 HENRY H. DONALDSON AND G. NAGASAKA

of rats. The object of making the sections and measurements in

different planes was to determine whether the long axes of the

cells were in a fixed relation to the long axis of the cord. There

is a slight difference between the long axes in these two cases in

favor of the longitudinal section, but the difference is too small

to warrant placing any emphasis on it at present. This problem .
of orientation must be taken up later.

TABLE 5

Mean diameters in micra of the ten largest spinal cord cells, from the ventrolateral
area of the ventral horn as they appear in a longitudinal section. Long diameter,
short diameter, and ‘computed diameter,’ which is the square root of the product of
the long and short diameters. Also the mean diameters of the respective nuclet.
The ratio of the last to the first entry ts given at the foot of each column

CELLS

BODY WEIGHT SRE
Long diameter Short diameter Computed RLS.
grams
18.7 B2ne 19.0 24.8 13.0
25.2 33.6 18.2 24.8 1S2
42.8 34.8 18.4 Aa) 3} 13.4
58.9 35.8 18.8 25.9 14.2
82.0 37.6 22.4 29.0 15.6
114.5 40.0 Done 30.5 16.8
117.0 36.0 22.4 28.4 14.8
153.5 39.0 25.2 31.4 16.4
180.8 37.4 22.8 29.2 15.0
228 .8 36.6 23.6 29.4 ivan
236.5 38.8 22.8 29.8 16.8
314.1 37.0 22.8 29.2 15s 2
Rahlosiece-cece 1:1.2— ihe2 Weber 1:1.2-—

In the meantime we shall treat the data as though the position
of the long axis of the cells in relation to that of the cord was
indeterminate, and, for discussion, the two series of data may be
combined. Table 6 contains the combined values for the two
series, taken from tables 4 and 5.

In order to determine the relations of the values given in tables
2 to 5 it has seemed best to condense these tables by taking
the means of the entries, in successive groups of three, as thus
several relations among the data can be brought out more clearly.

micra DIAMETERS OF FIBERS AND AXES IN VENTRAL ROOT AT B.
Seen ot al

200 F
175

150
Bah |
40.0 + + Siar: Ae
15 ee ea | ae

50 | | : to

25/- + | + i I. .
ASSET NC ae Ney TL || | aopy|weranr

0 20 40 60 80 100 120 140 160 180 200 220 240 260 280 300 320 gms.
micra DIAMETERS OF FIBERS AND AXES /N DORSAL ROOT AT C. .
|

200
{T5
15.0;

0 4H BODY |\WEIG UTS al
0 2 40 60 80 400 120 140 {60 180 200 220 AO 260 280 300 320 gms.
micra. D/AME TERS OF FIBERS AND AXES. SLIGHTLY Dis TAL TO SPINAL Es
= ane Tiled The ee aalls T
=F 1 + 3 + D =
eas
] | ae +|A
sel ies maces
ie Oe
25 <I Sia = are ;
|
0 he | |__| BoDy| WEIGHT

0 20 40 60 80 100 {20 140 {60 180 200 220 240 260 280 300 320 pms.

Chart 1 shows on body weight the graphs in micra for the
diameters of the fibers and their axes in the ventral root attB,
in the dorsal root at C, and in the nerve just distal to the spinal
ganglion at A. F, entire fiber; A, axis.

537

THE JOURNAL OF COMPARATIVE NEUROLOGY, VOL. 29, No. 5

538 HENRY H. DONALDSON AND G. NAGASAKA

ee ee ee
ed Sg

ie)

Nes | ee BODY |WEIGHT
0 w® © 60 80 100 {20 140 160 180 200 220 240 260 280 300 320 gms.

Chart 2 shows on body weight the graphs, in micra, for the
spinal ganglion cells and their nuclei. C, cell body. JN, nucleus.

———

Wake } |

‘|

=

|

1

|

| | |
ot. =
|

|

—

|

|

|

|

| BODY

| i}
i; 1
|

WEIGHT

ie Es =
0 20 40 60 80 1400 120 140 160 180 200 220 240 260 280 300 320 gms.

micra D/AMETERS OF LARGE VENTRAL HORN CELLS Uh CERVICAL) LONGI TUDINAL.

a Zl NA eal ce ih | i
Can nn RL
22s Leal Hadid
Le a a |

ER ne aa
|
{00 |

‘aoe ey

| |
50 xu alist oa ¥ poe
25 =} =i)
0 . ony weKGHr ne
C) a 40 60 8 86400 «120 «140 «160 «180 «9200 220 240 260 280 300 320 gms.

Chart 3 shows on body weight the graphs, in micra, for the
ventral horn cells, above, as seen in transverse section, below,
as seen in longitudinal section. C, cell body. N, nucleus.

539

540 HENRY H. DONALDSON AND G. NAGASAKA

TABLE 6

Giving in micra the mean values for the computed diameter of the cell body and of the
nucleus of cells from the ventrolateral area of the ventral horn by combining the
data as they appear in tables 4 and 6

CELL BODY MEAN ‘COMPUTED

MEAN BODY WEIGHT NUCLEUS MEAN DIAMETER

DIAMETER’

grams

1S 23.9 12.9
25.1 24.2 113341
42.9 25.3 13.4
59.1 P25) 18) 14.3
81.5 28.2 1522
114.8 29.6 15.8
118.7 28.3 15.4
151.4 30.4 15.8
179.4 29.5 15.1
231.0 28.9 16.2
249.8 29.2 16.0
315.2 29.6 15.3

RUAGLOS Sse se cere im 1:1.2+ 1:1.2-—

Table 7 enables us to compare the average diameters of the
largest nerve cells in the spinal ganglion of the seventh spinal
nerve with the corresponding average diameters of the largest
myelinated fibers at C in the dorsal nerve root, and at A in the
spinal nerve just distal to the ganglion. Looking at the column

TABLE 7

Comparing the diameters of the spinal ganglion cells in albino rats of different sizes
with the diameters of the corresponding dorsal root fibers and of the fibers just distal
to the ganglion. In the last two columns are given the respective ratios. Data
condensed from tables 2 and 3

AVERAGE AVERAGE
eee mae Cee RATIOS

BODY WEIGHT AGE cetits In |_OF DORSAL | pispar To

SPINAL oe Gy THE GAN-
GANGLION at(C) |grion ar (A)| C:Sp. G

grams days BL 7 BL

29.0 24 2aE0 10.8 10.7 L218
85.1 56, 29.8 13.0 12.9 2829
149.2 105 33.4 15 se¢7 15.8 12s
264.2 267 38.1 18.3 18.1 12508

atlogee sees eG Shy isa 7

DIAMETERS OF NERVE CELLS AND FIBERS 541

next to the last it appears that the ratio is a trifle smaller in
the last than in the first group—2.08 compared with 2.18. There-
fore the entire nerve fibers have grown in diameter a little more
rapidly than the ganglion cells from which they arise. In the
last column the fibers from the distal side of the ganglion are
compared with the ganglion cells and these behave in nearly the
same manner. As will be shown later the increase in the diam-
eters of the axes is Somewhat more rapid than that of the entire
fiber and the relation of the axes to the cell bodies is given for the
fibers distal to the ganglion in table 9 (B).

While there is a slight tendency for the ratios in table 7 to
decrease as we pass from the first to the last groups, by far the

TABLE 8

Comparing the computed diameters of the spinal cord cells in albino rats of different
sizes with the diameters of the corresponding ventral root fibers. In the last column
are given the ratios. Data condensed from tables 2 and 6

AVERAGE
DIAMETERS OF

SPINAL CORD CELLS. VE NS RATIOS
Da eae Eaves Nee) Mere an PaaS SHiTHAL. ‘oor
LONGITUDINAL FIBERS AT (B) /_________—
SECTIONS B: Sp. G. C.
grams days
29.0 24 24.5 10.7 he 2229
85.1 56 27.9 DING 12220
149.5 105 29.4 . 1: 1.90
264.8 267 29.2 18.2 1: 1.60
IRENMO Se alee one feel? plea

most striking point is their similarity at allages (=body weights),
the increase in the diameters of the cells and fibers running nearly
parallel.

Table 8 is based on tables 2 and 6, and gives the mean values
for the diameters of the spinal cord cells (data from the longitud-
inal and transverse sections combined) and the diameters of the
largest myelinated fibers in the ventral root. In the last column
it is seen that the relative value for the nerve cells diminishes very
rapidly because the growth of the cell bodies in diameter early
(56 days, chart 3) becomes very slow, while the nerve fibers con-

542 HENRY H. DONALDSON AND G. NAGASAKA

tinue to increase rather rapidly in diameter with the increase in
body size.

There appear therefore to be the following relations between
the cells and fibers which have been chosen for study. All of
the (largest) fibers, dorsal root fibers, the fibers just distal to the
ganglion, and ventral root fibers increase at about the same rate
and to about the same diameter (table 2, chart 1). The spinal
ganglion cells increase in diameter at nearly the same rate (not
quite so rapidly) as the fibers which come from them (table 7,
chart 2). On the other hand, the spinal cord cells early reach
nearly full size (tables 4, 5, and 6, chart 3), after which they grow
very slowly. Therefore the ventral root fibers increase in diam-
eter much more than do the cells from which they come. The
difference in growth appears therefore to be between the two
classes of cell bodies.

DISCUSSION

In the first place we note that the spinal ganglion cells are affer-
ent neurons of the first order—and the spinal cord cells (here
studied) are efferent neurons of the first order. In loaking for
other differences which might explain this lack of agreement, we
recall that the distal process (nerve fiber) from the ganglion cell
is physiologically a dendrite—that is, it carries impulses into the
cell body—whereas the dorsal root fibers and the ventral root
fibers both convey impulses from the cell body.

Growth of the axon process in diameter is not necessarily
accompanied by a corresponding growth of the cell body, as is
shown by the spinal cord cells. We should not, therefore, look
for an explanation of the growth of the cell body of the spinal
ganglion neuron as due to the enlargement of its central or axon
process which forms a fiber in the dorsal root. If this argument is
sound, then it is to the distal process which forms a fiber in the
nerve trunk, but which has the function of a dendrite, that we
must turn for an explanation. As the body surface (and the
surface of other organs innervated by afferent fibers) increases,
not only is the area innervated by the fiber increased, but sensory
discrimination (the ‘local sign’) is in a measure maintained.

DIAMETERS OF NERVE CELLS AND FIBERS 543

It is fair to assume that this maintenance of the sensory dis-
crimination calls for an increase of histological complexity in the
cell body, and with this we might associate the increase of size.

In this connection it is worth noting first that if we take
the data from table 7 and assume, as is usually done, that the
squares of the cube roots of the body weights stand in the same
relation as the respective surfaces of the animals compared, then

TABLE 9

Giving (A) the ratios of the relative body areas (squares of the cube roots of the body
weights) of the four groups of rats and the ratios of the corresponding relative vol-
umes (cubes of the diameters) of the spinal ganglion cells; and (B), the ratios of
the relative body areas compared with the relative areas of the axis cylinders in the
corresponding dorsal root fibers—as given in table 10

(A)
RELATIVE AREAS OF BODY RELATIVE VOLUME OF GANGLION CELLS
Body weights, grams Ratios Can diam- Ratios
VY 29.0? : 7/264.2? 1 Aah | 23a8) 3 Bete 1 4.26
V 85.1? : 7/ 264.22 1 Doig |. 2O.83 = Sar 18 1 2.09
V 149.22: 7/264.22 1 1.46 | 33.43 : 38.13 1 1.48
V 264.22 : 7/264.22 1 1.00 | 38.13 ; 38.18 1 1.00

RELATIVE AREAS OF AXIS CYLINDERS IN

RELATIVE AREA F BODY
x et 3 SQUARE MICRA

In root fibers distal to
ganglion at (A)

Aer || aiden, Be. weer ie yes

PREY | eee SET oS Be | ey:
1.46 | 89.9 :. 134.7 1

TROOM PUSAN (ar es 13467, 1

oe oe os

the first column in table 9, giving the squares of the cube roots of
the body weights can be used to obtain a series of ratios. The
relative area for the heaviest group is used as the standard, and
the ratios between it and the values for the preceding groups.
determined.

If the first three areas are compared successively with the final
or fourth area, there appear the ratios given in the last column

544 HENRY H. DONALDSON AND G. NAGASAKA

under ‘relative areas of body’ in table 9 (A). If, for comparison,
we take the cubes of the mean diameters of the ganglion cells,
which correspond to the relative volumes of these cells, and com-
pare these in a similar manner, we obtain the series of ratios in
the last column under the ‘relative volumes of ganglion cells.’
The volume ratios there given correspond very closely with the
ratios for the increasing areas. From these relations it is fair to
conclude that within the limits of this series the volume of the
spinal ganglion cells increases at the same rate as the area of the
body surface.- This result accords with the conclusion reached
by Levi (08) and with the general results of the later work by
Busacea (716), although the explanation of the relation here
presented is an extension of that given by those authors.

It is hardly necessary to repeat that the cell bodies in the
ventral horn of the spinal cord do not enlarge in a like way, as
can be seen by comparing the data for cell diameters in table 3
with the corresponding data in table 6.

In this connection another important relation appears, although
for the discussion of it data which are not given until table 10
must be used.

Linking the ganglion cell body with the surface of the body,
and other points of termination, is the peripheral fiber in which
the axis represents the conducting tissue. It might be assumed
that this axis would increase in its cross-section in a definite rela-
tion to the increase in the surface to which it is distributed.

The relations of the increasing area of the axis cylinder to the
increasing surface of the body are shown in table 9 (B) where the
values for the areas of the axis cylinder in the fibers just distal
to the ganglion (at A, fig. 1) are treated in the same manner as are
the computed areas of the body in the several groups. The
table shows that the areas of the axis cylinder increase at about
the same rate as the areas of the entire body. However, in the
first instance, when the area of the axis in the smallest group is
compared with that in the largest, the ratio, 3.71, is found to be
less than that for the body surface, which is 4.37. It is just
possible that the smaller increase in the areas of the axes is due
to the splitting of the fibers in their course to the periphery, but

{

DIAMETERS OF NERVE CELLS AND FIBERS 545

a discussion of this point must be reserved until the relation has
been more carefully examined. The relations between the volume
of the ganglion cell and the area of the axis cylinder of the fibers
passing to the periphery were briefly noted by Donaldson (’00),
and the results of the present study are in good agreement with
the earlier observations.

Bringing these observations together, it may be said that in the
afferent fibers just distal to the ganglion the increase in the area
of the axis, as the rat increases in size, during the later phases of
growth tends to be at the same rate as the increase in the surface
of the body and as the volume of the ganglion cells from which
the fibers arise.

CONSIDERATION OF INCIDENTAL RESULTS HERE OBTAINED

In order to bring the incidental observations made in the course
of this study into relation with other observations previously
recorded for the albino rat, it has seemed worth while to compare
our data with those already published.

The relations between the diameters of ganglion cell bodies
and the diameters of the entire fibers cannot be directly compared
with the results obtained by Hatai (’02, ’07) after osmic acid, on
account of differences in the fixation methods and in the pro-
cedure of measurement.' The records most suitable for com-
parison are those by Dunn (12) on the diameters of the ventral
root fibers of the econd cervical nerve of the albino rat of differ-
ent sizes. For 1 ke body weights the ventral root fibers in the
second cervical nerve run about 2y less in diameter than the
fibers in the seventh cervical, but the increase in diameter within

1 A special set of preparations of spinal ganglion cells shows that the mean

diameter of the nucleus is much less after osmic acid than after fixation in Bouin’s
fluid.

DIAMETERS IN yu

Cells Nuclei

Fixation ing bouts 15 oasecte ts ease sas be By 14.4
Hixa tlonpisvosMCeaClGen sect -h ciate chk enc 34.0 10.8

546 HENRY H. DONALDSON AND G. NAGASAKA

the range of body weight which we have used is similar in both
nerves. In the second and seventh cervical nerves, therefore,
the ventral root fibers grow in diameter at the same rate.

It will be noted that in table 2 the diameters of the ax’s cyl-
inders are given for each group of nerve fibers. In 1905 Donald-
son and Hoke published a series of observations on the areas of
the axis cylinder and of the myelin sheath as seen in cross-sections
of the spinal nerves of vertebrates. Since that time several sim-
ilar determinations have been made, and it was thought impor-
tant to have a determination made in this study also, since it
permitted the comparison of the fibers in the ventral and dorsal

TABLE 10

Giving the areas of nerve fibers and their axes in square micra—also the percentage
of the total area occupied by the axis, based on groups of three, from table 2

IN THE SEVENTH CER-

VENTRAL ROOT FIBERS | DORSAL ROOT FIBERS VICAL DISTAL TO THE
SPINAL GANGLION
AVERAGE a
ari cob ates Areas g S Areas 8 6 Areas 3 a)
Ent.F.| Axis | 584 /Ent.F| Axis | $94 |Ent.F| Axis | § ae
grams days
29.0 24 89.9) 36.3 40 91.6) 37.4 41 89.9} 36.3 40
85.1 56 12686|ole5 41 13250) 5One 43 130.6} 56.7 43
149.2 105 188.6} 91.6 48 193.5) 88.3 46 196.0) 89.9 46
264.2 267 260 .0/126.6 49 262 .9}141.0 53 257 .2)134.7 52

roots and in the nerve trunk near the ganglion, in respect of this
character. In table 2 are given the diameters of the axes of the
three classes of nerve fibers, and it has already been pointed out
that the axes increase in diameter slightly more rapidly than do
the entire fibers.

Using the diameters just mentioned the areas of the entire
fiber and of the axis (considered as circles) have been computed
and entered in the condensed table 10.

The columns which show the percentage of the entire area of
the fiber represented by the axis reveal several interesting rela-
tions. In the first place, the order of percentages is the same in
the three classes of fibers and their absolute values at the same

DIAMETERS OF NERVE CELLS AND FIBERS 547

body weight are also very close in all three classes. Between
105 days and 267 days the area of the axis approximates 50 per
cent of the entire area; i.e., the area of the axis is equal to the
area of the ring of myelin surrounding it. This ‘one to one’ rela-
tion was that found by Donaldson and Hoke in 1905 (table VI,
p. 9). That paper shows that in general the small fibers from
young albino rats had an axis somewhat less than half the area
of the fiber, while in the fibers from older rats this area was a
trifle more than half that of the entire fiber, but in the study of
1905 no attention was paid to age or to the abso'ute size of the
fibers. In 1912 Dunn examined these relations in the second
cervical nerve of albino rats from the standpoint of age, sex,
TABLE 11

Showing the percentage of the area of the entire fiber represented by the area of the

axis in the ten largest fibers found in the ventral root of the second cervical nerve

of the albino rat—Dunn (’12)—and in the ten largest fibers in the ventral root of
the seventh cervical nerve of the albino rat, as shown in table 10

DATA FROM TABLE 10 DATA FROM DUNN (’12)
Age Area of axis Area of axis Age
days per cent per cent days

24 40 40 36
56 41 44 75
105 48 44 sy
267 49 50 270

and body weight. The relations are expressed by her (loc. cit.,
table 2, p. 135) as ratios of the area of the axis taken as one, to
the area of the entire fiber. When, however, her data are recast
in the form which we have chosen, and age is made the basis of
comparison, there appear the relations shown in table 11.

When the comparison is made, as in table 11, it appears that
the axis-sheath relation is similar n the fibers forming the
ventral roots of the second and the seventh cervical nerves,
respectively, and that in both cases the ‘one to one’ relationship
is attained in the oldest group. These nerves were all measured
with the eyepiece micrometer.

There are still other observations on this point. Greenman
(13, table 9) reported at the proximal end of a bit of normal

548 HENRY H. DONALDSON AND G. NAGASAKA

peroneal nerve from the albino rat the value of the area of the
axis as 53.7 per cent and at the distal end of the same nerve the
value of 49.9 per cent. The mean body weight of the rats was
135 gms. In another series of studies, Greenman (’17) has
found the area of the axis about 40 per cent in a series of thirty
peroneal nerves from fifteen animals, all about 151 days of age.
In both these series the fibers were projected, outlined, and then
measured with a planimeter. In the cases where the sheath was
wavy this method would give a somewhat greater area for the
sheath than would be determined by direct micrometric measure-
TABLE 12

Giving the relations of the spinal ganglion cells and their nuclei. In the last

column appears the ratio of the volume of the cytoplasm (the volume of the entire

cell less the volume of the nucleus) to the volume of the nucleus. Data condensed
from table 3

NERVE CELLS NUCLEI 2
pei AVERAGE i fen 6 Se eee Cane curondinae
WEIGHT Mere Mean Ratio of Mean Ratio of LORVOLU MEO:
diameter jenlargement| diameter {enlargement RE
grams days BK mn
29.0 24 M3) 3) 1.00 11.9 1.00 ILE 70,
85.1 56 29.8 1.29 14.8 1.24 7-216
149.2 105 33.4 1.42 15.9 1.34 Sane
264.2 267 38.1 1.62 18.0 | 151) 1: 8.48

ment, and thus. contribute to giving a low percentage for the
area of the axis, as it appears in the last 1917 series.

We may conclude from Dunn’s record and our own that there
is a growth in the relative area of the axis up to about 250 to 300
days and that the axes in the fibers of the ventral nerve roots of
the spinal nerves have 50 per cent of the area of the fiber at
this age, when the measurements are made with the eyepiece
micrometer.

ON THE NUCLEUS-PLASMA RELATIONS

In the spinal ganglion cells here measured the mean diameters
of the cell bodies and of their nuclei are given in the condensed
table 12, and the ratios of the volume of the nucleus to that of
the cytoplasm (= cell volume less nucleus volume) have been

DIAMETERS OF NERVE CELLS AND FIBERS d49

entered in the last column. This ratio rises with the increasing
weight (age) of the rat, being as table 12 shows 6.70 for the
smallest group and 8.48 for the largest, an increase which is
definite and also regular. This shows that these cells are not
only growing in volume, but maturing, as indicated by the in-
crease in the ratio.

Contrasted with these results are the relations which appear in
the case of the ventral horn cells, as shown in table 13. Here,
as the last column shows, the nucleus-plasma relation is not
progressive and is only slightly higher in the largest rats as com-
pared with the smallest—5.68 for the largest as compared with
5.54 for the smallest.

TABLE 13

Giving the relations of the spinal cord cells and their nuclei. In the last column
appears the ratio of the volume of the cytoplasm (volume of entire cell less the
volume of the nuleus) to the volume of the nucleus. Data condensed from table 6

YERVE CELLS NUCLEI
Sone Hae a a a lll a ge ae
WEIGHT Sere Mean Ratio of Mean Ratio of ee ta oat oe
diameter |jenlargement| diameter jenlargement vee DE
grams days KL Be
28.9 24 24.5 1.00 13.1 1.00 1: 5.54
85.1 56 27.9 1.14 15a 1.15 1: 5.31
149.8 105 29.4 120 15.4 1.18 T5095
265.3 267 29.2 1.19 ayes) 1.18 1: 5.68

We infer from this that at twenty-four days the nucleus-
plasma relation in the ventral horn cells has nearly reached
equilibrium, although there is some slight increase in volume of
the entire cell body, as shown in the previous tables 4, 5, and 6.

The two types of cells here examined have a different nucleus-
plasma relation, therefore, and the plasma in the case of the
ganglion cells is not only absolutely more abundant, but increases
with the size (age) of the rat.

This seems to be an important difference. As the spinal cord
cells do not show a change in the nucleus-plasma relation, despite
the continued growth of the axon in diameter, we should not
consider the change in the spinal ganglion cell as due to the growth

550 HENRY H. DONALDSON AND G. NAGASAKA

of its axon process, the process which runs in the dorsal spinal
root. The change must therefore be associated with the distal
process of the ganglion cell, which is to be considered physio-
logically as a dendrite, bringing impulses into the cell body and
in some way stimulating not only its growth as a whole, but the
progressive change in the nucleus-plasma relation, which appears
to be an adaptation to maintain the discriminative sensibility
despite the increase in the skin area over which a given fiber is
necessarily distributed.

CONCLUSIONS

This study was made to determine whether in the albino rat
the increase in the diameter of the cell body of a neuron and in the
diameter of the fiber, or fibers, coming from it ceased at the
same time. It was therefore a study of the later phases of the
growth of the neuron.

The material was taken from the seventh cervical segment of
the spinal cord with the accompanying nerves, and measurements
were made on the largest fibers in the dorsal and ventral roots and
in the nerve just distal to the ganglion cells (all fixed in osmic
acid) and also on the spinal ganglion cells and on the ventro-
lateral group of large efferent cells in the ventral horn of the
spinal cord (both fixed in Bouin’s fluid).

Under these conditions of preparation, and as shown in tables
7 to 18—

1. All of the nerve fibers enlarge to the same extent, showing
(tables 7 and 8) in the heaviest group, diameters 1.7 greater
than in the lightest group of rats which weighed 29 grams and
were twenty-four days old.

2. The axis-sheath relation in these fibers was such that the
area of the axis in the youngest groups was about 40 per cent of the
area of the entire fiber, but this area increases with the increasing
age (and size) of the rat until it becomes about 50 per cent in the
largest animals (Table 10). This is in agreement with the results
of previous studies in which the same methods of measurement
were used, and shows that the axis has grown in diameter a
trifle more rapidly than the entire fiber.

DIAMETERS OF NERVE CELLS AND FIBERS Sow

3. The ganglion cells continue to increase in diameter with the
growth of the rat, and in the largest group (as indicated in the
condensed table 7) have a diameter about 1.6 times that found in
the smallest group. The ratio between the diameters of the
ganglion cells and those of the fibers arising from them decreases
somewhat with increasing body size, showing that the fibers are
increasing in diameter slightly more rapidly than is the cell body
(table 7); but in general the. cell is enlarging nearly in proportion
to its entire fibers, but less rapidly than the corresponding axes.
This enlargement of the ganglion cells is accompanied by a rela-
tive overgrowth of the cytoplasm as shown by the nucleus-plasma
relation, and further a study of the volumes of the ganglion cells
shows them to increase in volume in direct proportion to the
enlargement of the area or skin surface of the rat (table 9).
This enlargement of the cell is considered as an adaptation for
maintaining the sensory discrimination despite the extension of
the area supplied by a single neuron.

4. The areas of the axes of the afferent fibers also increase in
proportion to the increase of the body surface. (Table 9,B.)

5. The growth of the large spinal cord cell bodies is compara-
tively slight. The diameter of the fibers increases much more
rapidly than that of the cell body, as shown by the ratios in table
8, and in the cell body the nucleus-plasma relation is nearly
constant within the limits of these observations (table 13).
The enlargement of the axon to meet the requirements of the
increased muscle mass to be innervated is therefore not accom-
panied by any notable increase in the size or internal arrange-
ments of the cell.

These results reveal a marked difference, then, between the
growth changes which take place in the afferent as contrasted
with the efferent neurons of the first order, but it remains for
future investigation to determine the corresponding growth
changes in the case of the central neurons (i.e., neurons which
lie entirely within the central system) as well as in those which
constitute the peripheral ganglia.

552 HENRY H. DONALDSON AND G. NAGASAKA

LITERATURE CITED

Busacca, ARCHIMEDE 1916 Studi sulla curva di accrescimento delle cellule
nervose dei gangli spinali nel mammiferi. Arch. Ital. di Anat. e di
Embriologia, vol. 15, pp. 265-281.

Donaupson, H. H. 1900 The functional significance of the size and shape of
the neurone. J. of Nervous and Mental Disease, October.
Donaupson, H. H., anp Hoxr, G.W. 1905 On the areas of the axis cylinder and
medullary sheath as seen in cross-sections of the spinal nerves of

vertebrates. Jour. Comp. Neur. and Psychol., vol. 15, pp. 1-16.

Dunn, Evizapetu, H. 1912 The influence of age, sex, weight and relationship
upon the number of medullated nerve fibers and on the size of the
largest fibers in the ventral root of the second cervical nerve of the
albino rat. Jour. Comp. Neur., vol. 22, pp. 131-157.

GREENMAN, M. J. 1913 Studies on the regeneration of the peroneal nerve of

the albino rat: number and sectional areas of fibers: area relation of
axis to sheath. Jour. Comp. Neur., vol. 23, pp. 479-518.
1917 The number, size and axis-sheath relation of the large myelinated
fibers in the peroneal nerve of the inbred albino rat—under normal
conditions, in disease and after stimulation. Jour. Comp. Neur.,
vol. 27, pp. 403-420.

Harpesty, I. 1902 Observations on the medulla spinalis of the elephant with
some comparative studies of the intumescentia cervicalis and the
neurones of the columna anterior. Jour. Comp. Neur., vol. 12, pp.
125-182.

Harar, S. 1902 Number and size of the spinal ganglion cells and dorsal root
fibers in the white rat at different ages. Jour. Comp. Neur., vol. 12,
pp. 107-124.

1907 A study of the diameters of the cells and nuclei in the second
cervical spinal ganglion of the adult albino rat. Jour. Comp. Neur.,
vol. 17, pp. 469-491.

Levi, G. 1908 I gangli cerebrospinali.. Studi di istologia comparata e di isto
genesi. Supp. Arch. Ital. Anat. ed Embr. vol. 7.

1916 I fattori che determinano il volume degli elementi nervosl.
Rivista di Patologia nervosa e mentale, anno XXI, fase. 12.

Suaita, N. 1917 Comparative studies on the growth of the cerebral cortex.
II. On the increase in the thickness of the cerebral cortex during the
postnatal growth of the brain. Albino rat. Jour. Comp. Neur.,
vol. 28, pp. 511-591.

é

AUTHOR’S ABSTRACT OF THIS PAPER ISSUED
BY THE BIBLIOGRAPHIC SERVICE, AUGUST 7

NERVE ENDINGS OF SENSORY TYPE IN THE
MUSCULAR COAT OF THE STOMACH AND
SMALL INTESTINE

PRELIMINARY NOTE

F. W. CARPENTER
Biological Laboratory of Trinity College, Hartford, Connecticut

FOUR FIGURES

A variety of visceral sensations are attributed by physiologists
to impulses originating in the muscular coats of hollow organs.
Such sensations of the alimentary canal as fullness and distension,
emptiness and hunger, and especially pain, are believed to be due
to the stimulation of sensory nerve endings lying, not in the
mucous or submucous tunics, but in the coat of smooth muscle
external to these. Much of the evidence for this view, based on
physiological experimentation and clinical observations, is given
by Hurst (’11) in his Goulstonian Lectures on ‘“The Sensibility
of the Alimentary Canal.’ The cause of visceral pain receives
particular consideration from this author, who regards tension
on the fibers of smooth muscle to be the adequate stimulus for
the sensation. His general conclusion is, indeed, that ‘tension
is the only cause of true visceral pain.”

The recent detailed investigations of Carlson and his co-workers
on the physiology of the stomach tend to confirm the view that
the nerve endings concerned in sensory impulses from this organ
are to be sought in its muscular coats, although the submucosa
is also recognized as a possible site of such endings. Carlson
(13) concludes that the gastric sensory apparatus for hunger
lies in the muscularis or in the adjacent connective tissue of the
submucosa, but not in the mucosa. Carlson and Braafladt
(15) find the normal gastric mucosa devoid of pain and tactile
sensibility, and agree that “‘the literature seems to show that the

553

THE JOURNAL OF COMPARATIVE NEUROLOGY, VOL. 29, NO. 5

554 F. W. CARPENTER

gastric pain accompanying excessive inflation, gastric ulcers,
and chronic obstruction is due to the mechanical stimulation of
hypersensitive nerves or nerve endings in the muscularis or sub-
mucosa by excessive distention or contraction.”
Neurohistologists on the other hand, have been unable to
verify by direct observation the presence, of sensory nerve end-
ings in the smooth muscle of the abdominal viscera. As far as
the writer is aware, no figures or descriptions of such structures
are to be found in the text-books of neurology or general his-
tology. Barker (’01), in his ‘Nervous System’ refers to a variety
of pain characteristic enough to be designated as ‘smooth muscle
pain,’ but leaves it to further investigation to determine the
afferent elements among the numerous fibrils supplying smooth
muscle membranes. Herrick (’15) recognizes the presence of gen-
eral visceral receptors in visceral muscles, but points out that their
endings have not been differentiated histologically from the
simple terminations of the effector fibers. In their recently
published “Text-book of Histology,’ Jordan and Ferguson (’16)
describe only motor nerve endings in smooth muscle, although
they, too, agree that “many of the nerve fibers in smooth muscle
are undoubtedly of sensory function.’”’ In their chapter on the
histology of the digestive system they give a diagram (from
Kuntz, 713) illustrating the probable relationship of sympa-
thetic neurones in the myenteric and submucous plexuses.
This scheme shows sensory fibers distributed, outside the plex-
uses, to the epithelium and tunica propria of the mucosa only;
no afferent fibers are represented as ending in the muscular coat.
In searching the special literature of the subject one meets,
as haS been intimated, with exceedingly few references to nerve
endings in smooth muscle that give evidence of being sensory.
Practically all the endings described, such as the terminations
in involuntary muscle figured by Huber and DeWitt (’98) are,
by general agreement, regarded as motor in function. Schultz,
in 1895, described multipolar nerve cells, which he believed to be ©
sensory elements, in the muscularis of the frog’s stomach. His
observations, however, have not been confirmed, and Huber
and DeWitt were doubtless right in regarding these as specialized

NERVE ENDINGS, STOMACH AND SMALL INTESTINE 590

cells of connective-tissue origin falling in the same category as
the so-called ‘interstitial ganglion cells’ of Ramon y Cajal.
Ploschko (97) found intermuscular ‘Endbiumschen’ in the wall
of the trachea. ‘These arborescent endings appear to be of sen-
sory type. They will be referred to again in connection with the
description of somewhat similar terminations present in the
muscularis of the intestine.

ENDINGS IN THE LONGITUDINAL MUSCLE OF THE CARDIAC
STOMACH OF THE CAT

In a series of sections of the cardiac stomach of the cat stained
intra-vitam with methylene blue there appear in the longitudinal
muscle layer numerous nervous structures, many of them termi-
nal, which seem to be receptive rather than effective in type.
They are wholly different in their structural details from the
simple motor endings which have previously been described as
terminating on the cells of involuntary muscle tissue. They
have so far been found only in the longitudinal layer of the mus-
cularis and in the thin serous coat external to it. In the latter
tunic a few have been seen in the connective tissue subjacent to
the peritoneal epithelium; but the great majority are confined to
the region of the longitudinal muscle. Not one of these struc-
tures has as yet been seen in the circular muscle layer or else-
where in the stomach wall.

The structures in question may be described as, (1) skeins and,
(2) networks of very fine varicose fibrils. The fibrils arise from
the division of nerve fibers of somewhat larger caliber, which also
show varicosities, and which appear to be non-medullated as far
as they have been traced. ‘Their source has not been determined,
but they have been followed in a central direction close to the
region of the myenteric plexus.

The delicate fibrils composing a typical skein (fig. 1) lie for
the most part roughly parallel to one another, and form a rather
wide, loose bundle which is often spirally twisted. The skein
may terminate a fiber, frequently branching to make a T-shaped
ending, or it may occur midway in the course of a fairly compact
strand of fibrils derived from a fiber by the splitting up of the
latter.

556 F. W. CARPENTER

Fig. 1 Terminal skein from the longitudinal muscle coat of the cardiac stom-
ach of the cat.

Fig. 2 Terminal net from the longitudinal muscle coat of the cardiac stomach
of the cat.

Both figures were drawn with the aid of a camera lucida under a no. 4 Leitz
ocular and a 1/12 in. oil-immersion objective.

NERVE ENDINGS, STOMACH AND SMALL INTESTINE 557

In the net-like terminal structures the component fibrils appar-
ently anastomose to form a reticulum (fig. 2). The central re-
gion of this reticulum sometimes takes on a slight stain suggesting
the presence of some homogeneous substance on or in which the
net lies.

Not infrequently the strand of fibrils into which a main fiber
divides continues for some distance without developing skeins or
nets and interlaces with other fibrils to form a wide-meshed plexus
running through the muscular tissue. From this plexus terminal
skeins, and in some cases terminal networks, may be given off
laterally. Loops from such an interlacement of fibrils have been
traced into the serous coat, where they give rise to terminal
nets.

ENDINGS IN THE LONGITUDINAL MUSCLE OF THE SMALL
INTESTINE OF THE DOG

In the longitudinal muscle of the dog’s small intestine meth-
ylene blue staining has revealed nerve terminals to which the
name of end tufts may appropriately be given. Each occurs
at the extremity of a fine, non-medullated, varicose fiber, which
has been seen, in the limits of a single section, actually to emerge
from the myenteric plexus (fig. 3). Such fibers are noticeably
finer than certain others (such as the one marked ‘mf.’ in fig.
3) which run parallel to the muscle cells, and have been traced
to sumple motor endings on these cells.

The structure of the end tufts themselves is difficult to make
out satisfactorily even with the highest powers of the microscope.
Under oil immersion they appear to consist of exceedingly deli-
cate fibrils liberally besprinkled with minute varicosities (fig. 4).
The exact relation of the ultimate fibrils to one another has not
been positively determined, but the impression gained has been
that they spread out into a brush- or tuft-like structure without
uniting into a network. Except for the extreme delicacy of its
fibrillar constituents the ending under consideration bears a
general resemblance to the intermuscular end arborizations
(‘Endbiiumschen’) described by Ploschko (’97) as terminating a
rather large medullated nerve fiber in the wall of the trachea.

558 F. W. CARPENTER

Fig.3 End tuft from the longitudinal muscle coat of the small intestine of the
dog. The nerve fiber with which the end tuft is connected emerges from the
myenteric plexus. Drawn with the aid of a camera lucida under a no. 2 Leitz
ocular and a 1/12 in. oil-immersion objective. m.f., motor nerve fiber; m.p.,
region of myenteric plexus.

Fig. 4 End tuft from the longitudinal muscle coat of the small intestine of
the dog. Drawn with the aid of a camera lucida under a no. 4 Leitz ocular and a
1/12 in. oil-immersion objective.

NERVE ENDINGS, STOMACH AND SMALL INTESTINE 559

As is also true of the skeins and end nets in the stomach of the
cat, these intestinal endings of the dog are confined in all. the
preparations studied to the outer or longitudinal muscle coat and
to the adjacent connective tissue of the serous coat. All three
types of ending are thus so placed that they would doubtless be
directly affected by the contractions or distentions of the smooth
muscle tunic within which the majority of them lie. As has been
pointed out above, stimuli arising in this manner are, in the opin-
ion of the physiologists quoted, the source of most of the sensa-
tions, including pain, associated with the alimentary canal.

SUMMARY

1. Terminal structures in the form of, 1) skeins and, 2) nets,
both composed of fine fibrils with numerous varicosities, occur in
the longitudinal muscle coat of the cardiac stomach of the cat.
A few are present in the serous coat. These endings are con-
nected with unmyelinated, varicose nerve fibers, the source of
which has not been determined.

2. Terminal structures in the form of tufts of exceedingly deli-
cate fibrils exhibiting more plainly differentiated varicosities in
great abundance occur in the longitudinal muscle coat of the small
intestine of the dog, and also to some extent in the subperitoneal
connective tissue. These end tufts terminate fine non-medul-
lated nerve fibers which appear of smaller caliber than the motor
fibers supplying the smooth muscle cells. They have been traced
centrally into the myenteric plexus.

3. Structurally these endings conform to the sensory rather
than to the motor type of nerve terminations. Their presence
in the muscular coat, but not in the mucosa or submucosa, is
consistent with the results of recent physiological experimenta-
tion on the sensibility of the alimentary canal.

560 F. W. CARPENTER

LITERATURE CITED

Barker, L. F. 1901 The nervous system and its constituent neurones. New
York, xxxli + 1122 pp.

Cartson, A. J. 1913 The relation between the contractions of the empty
stomach and the sensation of hunger. Amer. Jour. Physiol., vol.
31, pp. 175-192.

Cartson, A. J. anp Braaruapt, L. H. 1915 On the sensibility of the gastric
mucosa. Ibid., vol. 36, pp. 153-170.

Herrick, C. J. 1915 An introduction to neurology. Philadelphia, 355 pp.

Huser, G. C., anp DeWitt, Lyp1a M. A. 1898 A contribution on the motor
nerve-endings and on the nerve-endings in muscle-spindles. Jour.
Comp. Neur., vol. 7, pp. 169-230.

Hurst, A. F. 1911 The sensibility of the alimentary canal. London, 838 pp.

Jorpan, H. E., anp Fereuson, J. 8. 1916 A text-book of histology. New
York, xxvuli + 799 pp.

Kuntz, A. 1913 On the innervation of the digestive tube. Jour. Comp.
Neur., vol. 23, pp. 173-192.

Proscuxo, A. 1897 Die Nervenendigungen und Ganglien der Respirations-
organe. Anat. Anz., Bd. 13, pp. 12-22.

Scuuttz, P. 1895 Die glatte Musculatur der Wirbelthiere. I. Ihr Bau. Arch.
f. Anat. und Physiol., physiol. Abth., Jahrg. 1895, pp. 517-550.

SUBJECT AND AUTHOR INDEX

CTIVITY of the nervous system. Il.
The partition of non-protein nitrogen in
the brain of the gray snapper (Neomae-

nis griseus) and also the brain weight in

relation to the body length of this fish.

Metabolic

ILLINGSLEY, P. R., anp Ranson, S.
W. Branches of the ganglion cervicale
superius

On the number of nerve cells in the

ganglion cervicale superius and of nerve

fibers in the cephalic end of the truncus
sympathicus in the cat and on the nu-
merical relations of preganglionic and
postganglionic neurones

An experimental analysis of the

sympathetic trunk and greater splanchnic

nerve in the cat

. The superior cervical ganglion and

the cervical portion of the sympathetic

trunk

The thoracie truncus sympathicus,

rami communicantes and _ splanchnic
MOL VER MMU Me Calter cs sas laa SO eG cite lee
Body length of this fish. Metabolic activity
of the nervous system. II. The parti-
tion of non-protein nitrogen in the brain
of the gray snapper (Neomaenis griseus)
and also the brain weight in relation to

Brain in normal and underfed albino rats at
different ages. Weights of various parts
Brain of the gray snapper (Neomaenis gris-
eus) and also the brain weight in relation

to the body length’of this fish. Metabolic
activity of the nervous system. II. The
partition of non-protein nitrogen in the...
. VI. Part If. On the increase in
size of some nerve cells in the cerebral
cortex of the Norway rat (Mus norvegi-
cus), compared with the corresponding
changes in the albino rat. Comparative
studies on the growth of the cerebral cor-
tex. VI. Part I. On the increase in
size and on the developmental changes of
some nerve cells in the cerebral cortex of
the albino rat during the growth of the...
, together with the changes in these
characters according to the growth of
the brain. V. Part II. On the area of
the cortex and on the number of cells in a
unit volume, measured on the frontal and
sagittal sections of the brain of the Nor-
way rat (Mus norvegicus), compared
with the corresponding data for the
albino rat. Comparative studies on the
growth of the cerebral cortex. V. Part
On the area of the cortex and on the
number of cells in a unit volume, meas-
ured on the frontal and sagittal sections
of the albino rat

ARPENTER, F. W. Nerve endings of
sensory type in the muscular coat of
the stomach and small intestine. Pre-

Lisminsiryano Ges saset geste wekietsatteeiocts nines

367

441

405

41

511

41

119

61

Cat and on the numerical relations of pre-
ganglionic and postganglionic neurones.
On the number of nerve cells in the
ganglion cervicale superius and of nerve
fibers in the cephalic end of the truncus
sympathicus in the

An experimental analysis of the

sympathetic trunk and greater splanch-

Hicmerve in) THe: setae pitautle vabevon eee

The thoracic truncus sympathicus,
rami communicantes and _ splanchnic
nerves in the

Cells in a unit volume, measured on the
frontal and sagittal sections of the albino
rat brain, together with the changes in
these characters according to the growth
of the brain. V. Part IJ. On the area of
the cortex and on the number of cells in a
unit volume, measured on the frontal
and sagittal sections of the brain of the
Norway rat (Mus norvegicus), compared
with the corresponding data for the
albino rat. Comparative studies on the
growth of the cerebral cortex. V. Part I.
On the area of the cortex and on the
number of

in several mammals, together with
some postnatal growth changes in these
structures. Comparative studies on the
growth of the cerebral cortex. VIII.
General review of data for the thickness
of the cerebral cortex and the size of the
COTEICAIAGE Ae i SO RR EE EE

—— in the cerebral cortex of the albino rat
during the growth of the brain. VI.
Part Il. On the increase in size of some
nerve cells in the cerebral cortex of the
Norway rat (Mus norvegicus), com-
pared with the corresponding changes in
the albino rat. Comparative studies
on the growth of the cerebral cortex.
VI. Part I. On the increase in size and
on the developmental changes of some

in the ganglion cervicale superius ord
of nerve fibers in the cephalic end of the
truncus sympathicus in the cat and on
the numerical relations of preganglionic
and postganglionic neurones. On the
numiberofmenve:caniiae ys eet eee
Cerebrum in the Norway rat (Mus norvegi-
cus) and a comparison of these with the
corresponding characters in the albino
rat. Comparative studies on the growth

of the cerebral cortex. III. On the size
andishapelofthe: ae ececasaee: 22a
Cervicale superius and of nerve fibers in the
cephalic end of the truncus sympathicus

in the cat and on the numerical relations

of preganglionic and postganglionic neu-
rones. On the number of nerve cells in
the ganglion
Branches of the ganglion
ganglion and the cervical portion of the
sympathetic trunk. The superior
Commissural neurones in the sympathetic
ganglia. On the question of

359

61

241

562

Cortex. III. On the size and shape of the
cerebrum in the Norway rat (Mus nor-
vegicus) and a comparison of these with
the corresponding characters in the albino
rat. Comparative studies on the growth
OlsthHECereralls eis. cased ee Osea

IV. On the thickness of the cerebral

cortex of the Norway rat (Mus norvegi-

cus) and a comparison of the same with
the cortical thickness in the albino rat.

Comparative studies on the growth of the

ROLCOLAl. secrete eee

V. Part I. On the area of the cor-

tex and on the number of cells in a unit

volume, measured on the frontal and
sagittal sections of the albino rat brain,
together with the changes in these char-
acters according to the growth of the
brain. V. Part II. On the area of the

cortex and on the number of cells in a

unit volume, measured on the frontal

and sagittal sections of the brain of the

Norway rat (Mus norvegicus), com-

pared with the corresponding data for

the albino rat. Comparative studies on
the growth of thecerebral.............

VI. Part I. On the increase in size

and on the developmental changes of

some nerve cells in the cerebral cortex
of the albino rat during the growth of the
brain. VI. Part II. On the increase in
size of some nerve Cells in the cerebral cor-
tex of the Norway rat (Mus norvegicus),
compared with the corresponding changes
in the albino rat. Comparative studies
on the growth of the cerebral............

VII. On the influence of starvation

at an early age upon the development of

the cerebral cortex. Albino rat. Com-
parative studies on the growth of the
cerebral

General review of data for
the thickness of the cerebral cortex and
the size of the cortical cells in several
mammals, together with some postnatal
growth changes in these structures.
Comparative studies on the growth of

IAMETERS of nerve-cell bodies and of
the fibers arising from them—during
the later phases of growth (albino rat).

On the increase in the:............... )

Diptera. The olfactory organs of............
Donaupson, Henry H., AnD NaGasaka, G.

On the increase in the diameters of nerve-

cell bodies and of the fibers arising from

them—during the later phases of growth

(albinomat) 3. ee Vd sane Dae ate

AR of Trigonocephalus japonicus. On
the development of the nerve endorgans
rhe 4 a eh ee Gung iery Ae Sake ors Re tere nae

Endings of sensory type in the muscular coat
of the stomach and small intestine. Pre-
liminary note. Nerve...... hte. eee

Endorgans in the ear of Trigonocephalus
japonicus. On the development of the

Nerve Aire Ooh eee.

(Epinephelus striatus). On tactile responses
of the de-eyed hamlet.....................

BUsees arising from them—during the
later phases of growth (albino rat). On
the increase in the diameters of nerve-
celitbodies'andtotther...u see eae

in the cephalic end of the truncus sym-
pathicus in the cat and on the numerical

INDEX

11

61

HLS

241
163

- 529
. 457

529

291

relations of preganglionic and postgan-
glionic neurones. On the number of
nerve cells in the ganglion cervicale
superius and of nerve................-.---

Paes On the question of commis-
sural neurones in the sympathetic.....

Ganglion and the cervical portion of the sym-
pathetic trunk. The superior cervical... .
——— cervicale superius and of nerve fibers
in the cephalic end of the truncus sym-
pathicus in the cat and on the numerical
relations of preganglionic and postgan-
glionic neurones. On the number of
nerveicellsiinithe ss. £20. eek. ce eee eee
cervicale superius. Branches of the....
Growth (albino rat). On the increase in the
diameters of nerve-cell bodies and of

359

313

359
367

the fibers arising from them—during the .

later phases of en scisssae eee cee
——— of the cerebral cortex. III. On the
size and shape of the cerebrum in the
Norway rat (Mus norvegicus) and a com-
parison of these with the corresponding

characters in the albino rat. Compara-
tive studiesionithe.. 25. Ns see ee
—— of the cerebral cortex. IV. On the

thickness of the cerebral cortex of the
Norway rat (Mus norvegicus) and a
comparison of the same with the cortical
thickness in the albino rat. Compara-
tivelstudiesionithere. seers eee oe eee
of the cerebral cortex. V. Part I.
On the area of the cortex and on the num-
ber of cells in a unit volume, measured
on the frontal and sagittal sections of
the albino rat brain, together with the
changes in these characters according to
the growth of the brain. V. Part Il.
On the area of the cortex and on the num-
ber of cells in a unit volume, measured
on the frontal and sagittal sections of the
brain of the Norway rat (Mus norvegi-
cus), compared with the corresponding

data for the albino rat. Comparative
studies.onsthew en, wae were. cole ee ee
——— of the cerebral cortex. VI. Part I.

On the increase in size and on the develop-
mental changes of some nerve cells in the
cerebral cortex of the albino rat during
the growth of the brain. VI. Part II.
On the increase in size of some nerve cells
in the cerebral cortex of the Norway rat
(Mus norvegicus), compared with the
corresponding changes in the albino rat.
Comparative studies on the...............

——— of the cerebral cortex. VII. On the
influence of starvation at an early age
upon the development of the cerebral
cortex. Albinorat. Comparative studies
OD THe Best cre rt oe Gere See

——— of the cerebral cortex. VIII. General
review of data for the thickness of the
cerebral cortex and the size of the corti-
cal cells in several mammals, together
with some postnatal growth changes
in these structures. Comparative studies
on thes: 5 La ee eee

AMLET (Epinephelus _ striatus).
tactile responses of the de-eyed.......

Hatat, SHINKIsHI. Metabolic activity of
the nervous system. II. The partition
of non-protein nitrogen in the brain of
the gray snapper (Neomaenis griseus)
and also the brain weight in relation to
the body length of this fish...............

On

529

11

61

119

177

241

. 163

INDEX 563

NTESTINE. Preliminary note. Nerve
I endings of sensory type in the muscular
coat of the stomach and small............ 553

OHNSON, Sypnry E. On the question
of commissural neurones in the sym-

At HELIO PAN alinrya seine. is tiie) ice ceisleietie ese 385
The peripheral terminations of the
nervus lateralis in Squalus sucklii......... 279

UDO, Toxvyasu. On the develop-
ment of the nerve endorgans in the
ear of Trigonocephalus japonicus........ 291

ATERALIS in Squalus sucklii. The
peripheral terminations of the nervus... 279

Lokalisation im Grosshirn.’’ Remarks on
vor Monakow’sis Dies. c. 2224 cece sae ces 485

Moe?: N. E. The olfactory organs
OL Diptera. tie sete ninco lo ec eeime cre 457

Monakow’s ‘Die Lokalisation im Gross-
hind?) Rentarksion VOns ss: caauewsio cs ate. 485
(Mus norvegicus) and a comparison of the
same with the cortical thickness in the
albino rat. Comparative studies on the
growth of the cerebral cortex. IV. On
the thickness of the cerebral cortex of
THOAN GWA Vib at serysctoen, crete oyeechess’s ereptielocs: 11
and a comparison of these with the
corresponding characters in the albino
rat. Comparative studies on the growth
of the cerebral cortex. III. On the size
and shape of the cerebrum in the Norway

compared with the corresponding
changes in the albino rat. Comparative
studies on the growth of the cerebral cor-
tex. VI. Part I. On the increase in size
and on the developmental changes of
some nerve cells in the cerebral cortex
of the albino rat during the growth of
the brain. VI. Part II. On the in-
crease in size of some nerve cells in the
cerebral cortex of the Norway rat......... 119
, compared with the corresponding
data for the albino rat. Comparative
studies on the growth of the cerebral
cortex. V. Part I. On the area of the
cortex and on the number of cells in a
unit volume, measured on the frontal
and sagittal sections of the albino rat
brain, together with the changes in these
characters according to the growth of the
brain. V. Part II. On the area of the
cortex and on the number of cells in a
unit volume, measured on the frontal
and sagittal sections of the brain of the
IWorway mat: saeame warrant este dareiclaaeers co ere 61

AGASAKA, G., Donaupson, Henry H.,
AND. On the increase in the diameters
of nerve-cell bodies and of the fibers
arising from them—during the later
phases of growth (albino rat)............. 529
Neomaenis griseus) and_ also the brain
weight in relation to the body length of
this fish. Metabolic activity of the nerv-
ous system. II. The partition of non-
DEge nitrogen in the brain of the gray
BDS PPeW see asec ese eas ss) sla ran sisetoayse oawiele 41
Warveoclr P hadies and of the fibers arising
from them—during the later phases of
growth (albino rat). On the increase
AINGNO CIAMOELEIS/ OL. s. se see teers 529
endings of sensory type in the mus-
cular coat of the stomach and small
intestine. Preliminary note.............. 553
endorgans in the ear of Trigonoceph-
alus japonicus. On the development of
PNOss ee ee tee eee a roe aera pase 291

Nerve-cell in the cat. An experimental analy-
sis of the sympathetic trunk and greater

Gloire (dares UV aisci6 anno nee deonan deuoerne 441
in the cat. The thoracic truncus sym-
pathicus, rami communicantes and
BplANnehNIC! | pee eee ees ee ee Shs 405
Nervous system. An introduction to a

series of studies on the sympathetic....... 305
. The partition of non-protein
nitrogen in the brain of the gray snapper
(Neomaenis griseus) and also the brain
weight in relation to the body length of

this fish. Metabolic activity of the.. 41
Nervus lateralis in Squalus sucklii. “The

peripheral terminations of the............ 279
Neurones in the sympathetic ganglia. On

the question of commissural.............. 385

On the number of nerve cells in the
ganglion cervicale superius and of nerve
fibers in the cephalic end of the truncus
sympathicus in the cat and on the numer-
ical relations of preganglionic and post-
anelionic wre nee een 359

Nitrogen in the brain of the gray snapper
(Neomaenis griseus) and also the brain
weight in relation to the body length of
this fish. Metabolic activity of the
nervous system. II. The partition of
NGN=provelnw: Sco ase see emo aoe hee 41

Gees sey organs of Diptera. The.... 457

Organs of Diptera. The olfactory............ 457
ERIPHERAL terminations of the nervus
lateralis in Squalus sucklii. The... .... 279

Pixs, F. H. Remarks on von Monakow’s
““Tie Lokalisation im Grosshirn.”’........ 485

AMI communicantes and _ splanchnic
nervesint hecat. The thoracic truncus
SYIMpAthICush. .ceatseros nel enemas 405

Ranson, 8. W. An introduction to a series
of studies on the sympathetic nervous
BYALEM eyes he cae eee ore 305
, AND Bruuinecstey, P. R. An exper-
imental analysis of the sympathetic
trunk and greater splanchnic nerve in
LBC) REP nea EOC AA oth bet Gee OB Gane 441

, AND Briutinestry, P. R. The su-
perior cervical ganglion and the cervical
portion of the sympathetic trunk......... 313

, AND BILLINGsLEy, P. R. The tho-
racic truncus sympathicus, rami com-
municantes and splanchnic nerves in the
(Cr) He edS shige ene Rel tert Se aA C eh een ac” 405

———, Binuinestey, P. R. anv. Branches
of the ganglion cervicale superius......... 367

——, Bruuinestry, P. R. anv. On the
number of nerve cells in the ganglion cer-
vicale superius and of nerve fibers in the
cephalic end of the truncus sympathicus
in the cat and on the numerical relations
of preganglionic and postganglionic neu-

Rat brain, together with the changes in these
characters according to the growth of the
brain. V. Part II. On the area of the
cortex and on the number of cells in a
unit volume, measured on the frontal
and sagittal sections of the brain of the
Norway rat (Mus norvegicus), compared
with the corresponding data for the
albino rat. Comparative studies on the
growth of the cerebral cortex. V. Part

On the area of the cortex and on the
number of cells in a unit volume, meas-
ured on the frontal and sagittal sections
ofthealbinos ene eee eee 61

564

Rat brain, Comparative studies on the
growth of the cerebral cortex. VII. On
the influence of starvation at an early age
upon the development of the cerebral
COLE AMAL DINO eis oe soe oe ee 177

—— during the growth of the brain. VI.
Part II. On the increase in size of some
nerve cells in the cerebral cortex of the
Norway rat (Mus norvegicus), compared
with the corresponding changes in the
albino rat. Comparative studies on the
growth of the cerebral cortex. VI. Part
I. On the increase in size and on the
developmental changes of some nerve
cells in the cerebral cortex of the albino... 119

——— (Mus norvegicus) and a comparison
of the same with the cortical thickness
in the albino rat. Comparative studies
on the growth of the cerebral cortex. IV.

On the thickness of the cerebral cortex
of HheiNorway-ee re ee ee 11

(Mus norvegicus) and a comparison of

these with the corresponding characters

in the albino rat. Comparative studies

on the growth of the cerebral cortex. III.

On the size and shape of the cerebrum in

thie NOE WS aiid sc ere ree cia 1

On the increase in the diameters of
nerve-cell bodies and of the fibers arising
from them—during the later phases of
prow (albino. ee cee dec eee 592

Rats at different ages. Weights of various
parts of the brain in normal and under-
fed albimoy. wae see ieee or er eee 511

Responses of the de-eyed hamlet (Epineph-
elusstriatus): Onitactil.. 2...) 163

ENSORY type in the muscular coat of
the stomach and small intestine. Pre-
liminary note. Nerve endings of... .... 553

Small intestine. Preliminary note. Nerve
endings of sensory type in the muscular
ecoationbhe stomach ands -- 4-4. a eee 553

Snapper (Neomaenis griseus) and also the
brain weight in relation to the body
length of this fish. Metabolic activity of
the nervous system. II. The partition
of non-protein nitrogen in the brain
OMCRCIOTAY Seer erie io Pee eae 41

Splanchnie nerve in the cat. An _ experi-
mental analysis of the sympathetic trunk
ANG greater ceeh Mee been eee 441

Splanchnic nerves in the cat. The thoracic

truncus sympathicus, rami communi-

Garitesiand =; sto ek Ate eee ee 405
Squalus sucklii. The peripheral termina-

tions of the nervus lateralisin............ 279

Starvation at an early age upon the devel-
opment of the cerebral cortex. Albino
rat. Comparative studies on the growth
of the cerebral cortex. III. On the
INHUEHCE. Ole a Cee ee 177

Srewart, C. A. Weights of various parts of
the brain in normal and underfed albino
rats‘at differentages....0).. 29) UYl eee. 511

Stomach and small intestine. Preliminary
note. Nerve endings of sensory type
in the muscular coat of the............... 553

Sueira, Naoxr. Comparative studies on
the growth of the cerebral cortex. III.
On the size and shape of the cerebrum
in the Norway rat (Mus norvegicus) and
a comparison of these with the corre-
sponding characters in the albino rat..... il

, Naoxrt. Comparative studies on the

growth of the cerebral cortex. IV. On

the thickness of the cerebral cortex of
the Norway rat (Mus norvegicus) and

a comparison of the same with the corti-

cal thickness in the albinorat............. il

, Naoxrt. Comparative studies on the

growth of the cerebral cortex. V. Part

INDEX

I. On the area of the cortex and on the
number of cells in a unit volume, meas-
ured on the frontal and sagittal sections
of the albino rat brain, together with
the changes in these characters accord-
ing to the growth of the brain. V. Part
II. On the area of the cortex and on the
number of cells in a unit volume, meas-
ured on the frontal and sagittal sections
of the brain of the Norway rat (Mus
norvegicus), compared with the cor-
responding data for the albino rat......... 61
. Comparative studies on the growth
of the cerebral cortex. VI. Part I. On
the increase in size and on the devel-
opmental changes of some nerve cells in
the cerebral cortex of the albino rat dur-
ing the growth of the brain. VI. Part
II. On the increase in size of some
nerve cells in the cerebral cortex of the
Norway rat (Mus norvegicus), com-
pared with the corresponding changes in
thealbmo rats. sere
. Comparative studies on the growth
of the cerebral cortex. VI]l. On the
influence of starvation at an early age
upon the development of the cerebral
cortex, “Albinoirathc sass cee eee eee 177
. Comparative studies on the growth
of the cerebral cortex. VIII. General
review of data for the thickness of the
cerebral cortex and the size of the cortical
cells in several mammals, together with
some postnatal growth changes in these
BUrUCctIneSs Cuetec ee eee ere 241
Superior cervical ganglion and the cervical
portion of the sympathetic trunk. The.. 313
Superius and of nerve fibers in the cephalic
end of the truncus sympathicus in the
cat and on the numerical relations of
preganglionic and postganglionic neu-
rones. On the number of nerve cells in
the ganglion cervicale..................-.- 359

Branches of the ganglion cervicale... 367
Sympathetic ganglia. On the question of

commissural neurones in the.............. 385
nervous system. An introduction to
a series of studies on the.................. 305

trunk and greater splanchnic nerve in
the cat. An experimental analysis of the. 441

trunk. The superior cervical gan-

glion and the cervical portion of the....... 313
Sympathicus, rami communicantes and
splanchnic nerves in the cat. The tho-
TACICHtRUNCUS) eee eee eee 405
System. An introduction to a series of
studies on the sympathetic nervous....... 305
——. Il. The partition of non-protein

nitrogen in the brain of the gray snapper
(Neomaenis griseus) and also the brain
weight in relation to the body length
of this fish. Metabolic activity of the

NOLVOUB 25 seis forsee oemdiolace saath See 41
fl Pie aeeee responses of the de-eyed hamlet
(Epinephelus striatus). On............. 163
Terminations of the nervus lateralis in Squa-

lus sucklii. The peripheral............... 279
Thoracic truncus sympathicus, rami com-
municantes and splanchnic nerves in
theidst:, Ses Beh ee eee 405
Trigonocephalus japonicus. On the devel-
opment of the nerve endorgans in the
Gar Of sss ese Sh eon a Nee eee 291
Truncus sympathicus in the cat and on the
numerical relations of preganglionic and
postganglionic neurones. On the num-
ber of nerve cells in the ganglion cervi-
cale superius and of nerve fibers in the
cephalic end of the.............00:0ese000. 359

INDEX

Truncus sympathicus, rami communicantes
and splanchnic nerves in the cat. The
EHOLACIG eer ce res

Trunk and greater splanchnic nerve in the
eat. An experimental analysis of the
BYINPIMUDELIC sete ttre in sven Soe we ees 441

. The superior cervical ganglion and

the cervical portion of the sympathetic... 313

NDERFED albino rats at different
ages. Weights of various parts of the
DLamelnenOrois And ep eerie ee 511

565

Was in relation to the body length

of this fish. Metabolic activity of

the nervous system. II. The parti-

tion of non-protein nitrogen in the brain of

the gray snapper (Neomaents griseus) and
also the) Drain eete nee a loc. ee ss wid 41

of various pyrts of the brain in normal

and underfed albino rats at different

MVR ey oe
I eran

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