On the chameleon's retina : a further contribution to the minute anatomy of the retina of reptiles / by J. W. Hulke.

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4.

XI. On the Chameleon's Retina ; a further Contrihutimi to the Minute Anatomy of the
Eetina of Reptiles. By J. W. Hulke, F.R.C.S., Assistant Surgeon to the Middlesex
and Royal London Ophthalmic Hospitals. Communicated hy William Bowman,
F.R.S.

Received June 1, — Read June 15, 1865.

The chameleon's retina is remarkable in two respects: 1st, it lias a yellow spot and
fovea centralis*; and 2ndly, the fibres which connect the cones with the inner layers
cross the connective-tissue radial fibres instead of running parallel to themf.

The yellow spot lies in the centre of the retina, at the posterior pole of the globe.
The fovea is a deep circular pit. Its bottom (^. e. centre) appears as a dark-brown dot.
encircled by a lighter brown ring corresponding to the sides of the pit, and this in turn
is surrounded by a colourless zone, the outer edge of which passes gradually into the
colour of the surrounding parts (Plate XIX. fig. 1).

A flat subconical pecten, rising above the inner sm-face of the retina, marks the
entrance of the optic nerve, 1"', at the temporal side of the fovea. The nerve pierces
the sclerotic very obliquely, and its bundles, escaping from the base of the pecten in the
level of the ganglionic layer of the retina, are distributed on the inner retinal surface in
such a manner that those only which belong to the fovea run directly towards this from
the pecten, while all other fibres for parts on the nasal side of the pecten arch above
and below the fovea in increasingly open curves.

Minute Structure.

1. Bacillary Layer. — Cones only occur in this layer (figs. 2 & 3). They consist of an
inner and an outer segment, separated by a bright transverse line. The outer segment
is a very slender, strongly-refracting shaft ; it tapers slightly towards its outer end ; its
length increases from the periphery to the centre of the retina, but is always much less
than that of the inner segment. It is completely buried in the choroid, which also sheaths
the outer part of the inner segment. This latter segment, although much larger than
the outer, is inconspicuous in fresh specimens in consequence of its low refraction. At
the centre of the retina its length is very considerable, while its breadth scarcely exceeds
that of the outer segment ; these proportions give the cones in this i)art the appearance
of tall slender pillars ; but at the periphery the inner segment is stout, and the cones
resemble tall flasks. In chromic acid preparations the outer part of the flask-shaped
cone-body is finely granulated, while the inner is more homogeneous, and often exhibits

* Knox, Mem. "Wcrn. Soc. vol. v. p. 2, and Edinb. Phil. Journal, Oct. 1823, p. 358.
t MiiLLER, H., Wiirzb. :Natunviss. Zeitschr. 18G2, Bd. III. Heft 1. S. 20.

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ME. J. W. HULKE ON THE CHAMELEON'S EETINA.

an oval or stellate vacuole, regarded by MtiLLER as a nucleus, and which is not to be
mistaken for an outer granule.

The difference between these extreme forms of cones in the centre and in the peri-
phery of the retina is so great, that, judging from their shape alone, they might not be
unreasonably regarded as different elements ; but a regularly progressive change from
one to the other shape in passing from the centre of the retina outwards, and the con-
stant presence of a bright pale yellow or colourless bead in the outer end of their inner
segment, establish their identity and conic nature. As their stoutness decreases from
the periphery to the centre of the retina, each successive unit of surface in this direction
contains more cones ; and since each cone has its outer granule associated with it, the
numerical increase of the cones is attended with a corresponding increase in the number
of the outer granules. The inner ends of the cones pass through apertures in the mem-
brana limitans externa, which in its structure and relations resembles that of other
reptiles.

2. The Outer Granule-Layer. — The so-called " granules" are large, round, and roundly-
oval nuclei, about awo" in diameter. In the periphery of the retina, where the cones
are stout, they lie in a single tier, one in the inner end of each cone, in or slightly
inside the plane of the membrana limitans externa ; while towards the fovea, where the
slenderness of the cones does not allow them to enclose their outer granule, the granules
form a separate layer, and each is connected with its cone by an intermediate fibre, con-
tinuous with the inner end of the latter. These fibres, for which I would suggest the
term primitive cone-fibres," are identical with those I have described as coming off
from the inner end of the rods and cones in other reptiles, but their course and arrange-
ment in the chameleon are peculiar.

3. Cone-fihre Plexus. — In the periphery of the retina, where the cones enclose their
outer granule, the primitive fibres, on leaving the inner end of the cones, curve verti-
cally inwards and combine in bundles, which run for a considerable distance hori-
zontally towards the periphery, and then again bend vertically inwards among the
inner granules. In the central region, where the cones are slender and numerous and
the outer granules lie in several tiers, the primitive cone-fibres first bend inwards from
the cones, next take up their outer granule, and then, at the inner surface of the outer
granule-layer, combine in bundles which unite in a plexiform manner to form a layer
that attains a remarkable thickness at the border of the fovea centralis. The inclina-
tion of the bundles, and their combination in the plexus, is such that the outer bundles
are gradually brought to the inner surface of the plexus. Here they are again resolved
into primitive fibres that curve inwards through the intergranule-layer to the inner
granules (fig. Ah). li. MUller relates that in his hardened preparations he could not
determine wliether the finer fibres were merely stuck together in the bundles of the
plexus, or whether divisions took place ; my belief is that they cohere very closely
in the bundles of the plexus, but that they never fuse or split. Ikying between the
outer and the inner granules, this plexus was called by Mcller the intergranule-layer,

MR. J. W. HULKE ON THE CHAMELEON'S RETINA.

225

a name which I give to a thin band of connective tissue that bounds the outer surface
of the inner granule-layer, and which corresponds to the intergranule-layer of other
reptiles (fig. 5 i).

A second set of fibres, corresponding to those which in the Turtle's retina I named
the outer radial fibres, crosses the cone-fibre plexus nearly perpendicularly. These
vertical radial fibres are most developed where the plexus is thickest (fig. 5j. Near
the fovea they are very conspicuous, particularly in carmine preparations, in which
they are almost colourless, while the bundles of cone-fibres have a deep red tint. In
sections parallel to the cone-fibre bundles we see the vertical radial fibres traversing the
meshes of the plexus ; while in sections across the bundles, the cut ends of these are
packed in long vertical spaces between the radial fibres, which last appear as stout ver-
tical pillars that divide at acute angles, and becoming fine and numerous, end at the
inner surface of the membrana limitans externa. Near the inner surface of the plexus,
the stout pillar-like fibres also repeatedly divide, the resulting fibrillae spread in a fan-
like manner, and interweaving with others from neighbouring trunks, form the thin
band which I call the intergranule-layer. Through this layer the primitive cone-fibres
pass to the inner granules.

The above description of the outer vertical radial fibres and intergranule-layer applies
particularly to the central region of the retina ; in the periphery, where the retina is
thin, a distinct intergranule-layer is not present, and the outer vertical radial fibres are
replaced by vertical radial fibres which pass from the inner to the outer limiting
membrane.

4. The Layer of Inner Granules. — This layer throughout the retina is thicker than
that of the outer granules. It reaches its greatest development around the fovea cen-
tralis, and diminishes towards the periphery in a more gradual manner than the outer
granule-layer. Several distinct forms of cells and nuclei., and two sets of fibres, a vertical
and an oblique., are distinguishable in it. Near the outer surface of the layer, in the
central region in close relation to the vertical set of fibres just mentioned, we find small
oat-shaped nuclei which carmine scarcely stains. Besides these, other minute nuclei,
bright, angular, and also scarcely tinted by carmine, are scattered throughout the layer,
apparently in relation with the vertical fibres and interstitial connective tissue.

Of the cells, some are of a round and roundly oval form, from g^u" to 45V0" ^i^"
meter. Carmine stains them deeply, and many contain a minute nucleus (figs. 6 & 7).
In rather thick sections, in which the relations of the elementary parts are less dis-
turbed, these cells are often seen disposed in linear series parallel to the oblique fibril-
lation to be presently described. AVhere the layer is broad, they are most numerous
in its middle third. There are other cells which are much larger and of an irregular
figure (figs. 8, 9, & 10). These have a faint single outline, a pale, finely granulated
texture, and contain a large, round, sharply-defined nucleus which nearly fills them,
averaging 30^00". They occur principally near the inner surface of the layer, and
are less numerous than the smaller cells. I have frequently seen a broad, flat, pale

MDCCCLXVI. 2 I

226

m J. W. HULKE ON THE CHAMELEON'S EETINA.

process pass inwards from these large multiangular cells into the granular layer, and
here break up into very fine parallel fibres, which I have traced nearly to the ganglionic
layer, and believe to be continuous with processes from the cells of this layer. On the
outer side the cells are connected with the oblique fibres.

These fibres (figs. 7, 8, 9, 10, & 11) are directed obliquely from the outer to the inner
surface of the layer, and from the centre towards the periphery of the retina. Their
obliquity diminishes towards the inner surface of the layer, where many of them are
nearly horizontal. In the outer part of the layer they are very fine and numerous,
in the middle they are thicker and fewer, while in the inner third their numbers still
further decrease, and they become stouter and flatter. This results from the union of
the primitive fibres in bundles, which have an open plexiform arrangement. In the thin
periphery of the retina the whole course of the fibres is more horizontal.

The following are the relations of the oblique fibres and the other tissues. The finest
fibres in the outer part of the layer are continuous through the intergranule-layer with
the primitive fibres of the cone-fibre plexus, as I have already mentioned in describing
this ; they also take up the smaller round and roundly oval inner granules. Combining
as they pass through the layer, becoming stouter and more horizontal, they join the large
ganglion-cell-like cells which lie near the inner surface of the layer, and the pale band-
like fibres which these cells send into the granular layer may be regarded as their further
continuations.

5. The Granular Layer. — Around the fovea the thickness of this layer nearly equals
that of the inner granules ; from this point it very gradually decreases towards the peri-
phery of the retina. Its minute structure is a close and intricate web of exceedingly
fine soft filaments. It is marked by horizontal parallel bands, which appear to result
from a longitudinal disposition of the filaments.

Two sets of vertical fibres are distinguishable in it. The first are connective fibres
passing outwards from the membrana limitans interna ; they are finer near the centre
than at the periphery of the retina. They divide at acute angles, and give off fine lateral
branches which are lost in the proper tissue of the layer.

The second set consists of the fibres which pass inwards from the large multipolar inner
granules (which I look upon as ganglion-cells), and of those passing outwards from the
cells of the ganglionic layer. I have already said that I believe these fibres are con-
tinuous. I have occasionally seen large ganglionic cells in vacuoles in the middle of
this layer, at a distance from the inner granules and ganglionic layer.

G. Tlie GaiKjUonic Layer. — The cells of this layer are distinctly multipolar (fig. 12).
They have a faint single outline, a soft, finely granulated texture, and a very conspicuous
hirge circular nucleus. On the one side they send ofi" the fibres mentioned in the
account of the granular layer, while on the other they send fibres, which cannot be
distinguished from nerve-fibres, to the plexiform expansion of the optic nerve. Around
the fovea tliey lie four or five deep; their numbers increase for about from this in a
peripheral direction, and then decrease.

ME. J. W. HULKE ON THE CHAMELEON'S EETINA.

227

7. Optic Nerve-layer. — The general appearances of the optic nerve have been ah-eady
described ; its finer distribution does not exhibit any special characters. The bundles
are disposed in a plexus, the meshes of which transmit the connective radial fibres.

The plexus is separated from the membrana limitans interna by a narrow band, which
has a finely granular and striated texture. Its minute structure agrees with that of the
granular layer. This band is bounded by the membrana limitans interna, from the
inner surface of which the connective radial fibres arise by fine converging roots ; their
course has been given in the descriptions of the difierent layers.

Fovea Centralis.

Owing to the great thickness of the retina immediately around it (fig. 13), the fovea is
encircled by a raised margin, from which the surface rapidly declines centrally to the
bottom of the fovea, while it slopes gently towards the periphery of the retina. Oppo-
site its margin the optic nerve, granular, inner granule, layers, cone-fibre plexus, and
the inner limit of the outer granule-layer, begin to bend outwards, and becoming gradu-
ally thinner, they converge to the bottom of the fovea, where they cease, the cones
(with their fibres diverging on all sides towards the outer granule-layer) alone, covered
by a thin fibro-granular band, existing at this spot.

Reviewing the layers at the fovea in order, from the inner surface of retina outwards,
we find the optic nerve-fibres in decreasing number from the margin to the bottom of the
fovea.

The ganglion-cells around the bottom lie in a single and interrupted series, which,
midway towards the margin, becomes continuous, and double or treble, while at the
margin the cells lie four or five deep. The greatest development of the ganglionic
layer is not, however, here, but about from the centre of the fovea.

The granular layer blends in the bottom of the fovea with the granular band, which
in other parts lies between the optic nerve-layer and the membrana limitans intenia.
This band in the fovea exhibits a very distinct vertical striation.

The inner granule-layer., in sloping towards the bottom of the fovea, closely approaches
the outer granule-layer, as the cone-fibre plexus which lies between them becomes
thinner. It attains its maximum development slightly nearer the fovea than that of the
ganglionic layer.

The cone-fibre plexus commences near the bottom of the fovea, in the angle between
the inner and outer granules, and steadily increases in breadth till it reaches its maxi-
mum development, slightly nearer the fovea than that of the inner granules.

The outer granule-layer., also commencing near the bottom, swells very rapidly, and
opposite the margin of the fovea acquires a remarkable thickness. From tliis point it
slowly declines for about f " from the fovea, and then becomes abruptly thin. Its extra-
ordinary enlargement immediately around the fovea is due to the presence here, not only
of the outer granules which belong to the cones lying immediately at its outer surface,
but also of those outer granules that belong to the cones which lie at the centre of the

22S

MR. J. W. HIJLKE ON THE CHAMELEON'S EETINA.

fovea. Besides which the great proportional number of cones in the fovea is attended
with a corresponding increase in the number of the outer granules.

Conal Layer. — The cones become thinner, longer, and more numerous from the peri-
phery to the centre of the retina, i. e. of the fovea. At the centre of the fovea they
reach the extraordinary length of In fresh specimens the characteristic bead in

the outer end of the inner segment of the cones here was conspicuous, though very
minute.

A careful study of many sections has convinced me that the cones stand vertically on
the choroid ; the primitive fibres proceeding from them to the outer granules do, how-
ever, incline on all sides from the centre of the fovea ; and the bundles of the cone-fibre
plexus, as also the oblique fibres in the inner granule-layer, are similarly deflected.

Enumerated briefly, the peculiarities of the fovea consist in the attenuation of the optic
nerve, ganglionic, granular layers, and cone-fibre plexus, from its margin towards its
centre ; in the absence of these layers at the centre ; in the great slenderness and length
of the cones ; in the deflection of the primitive cone-fibres and of their continuations
in the outer and inner granule-layers from the centre towards the periphery ; and in the
maximum development of all the layers, excepting the bacillary, at successively
increasing distances from the centre of the fovea in their order of superposition from
the outer to the inner surface of the retina.

Explanation of Plate.
PLATE XIX.

Fig. 1. An enlarged view of the Fovea centralis in the fresh retina.

Fig. 2. Cones from the Fovea : a, the outer ; the inner segment.

Fig. 3. Cones from the periphery of the retina: a, the outer segment; h, the inner
segment containing, an outer granule, and produced inwards as a primitive
fibre through the membrana limitans externa ; c*, intended to mark this latter
(the horizontal line), has been placed too high by the artist.

Fig. 4. A vertical section near the Fovea parallel to a, the bundles of the cone-fibre
plexus ; b, primitive fibres passing from these bundles through d, a granular
stratum, into the inner granule-layer ; c, the outer vertically-radial connective-
tissue fibres.

Fig. 5. A vertical section through the outer layers near the Fovea. Only the connective-
tissue frame is represented: I, the bacillary layer; 2, the outer granule-
layer ; 2', the cone-fibre plexus ; 3, a granular stratum representing the inter-
granule-layer ; c, the membrana limitans externa ; f, the trunks of the outer
vertically-radial connective-tissue fibres; ^, their outer ends, branching and
terminating in the membrana limitans externa (the arti;?t has drawn these too
thick) ; /t, the branching inner ends of the fibres forming the intergranule-

ME. J. W. HULKE ON THE CHAMELEON'S EETINA.

229

layer and terminating in a thin band bounding the outer surface of the
inner granule-layer ; the vertically-radial connective-tissue fibres in the
inner granule-layer.

Figs. 6 & 7. Oblique fibres in the inner granule-layer arranged in a plexiform manner.

with smaller inner granules.
Fig. 8. A vertical section through the inner granule -layer, near its inner surface :

«, larger inner granules (= ganglion-cells 1); 5, fibres passing from them into

the granular layer.

Fig. 9. Two larger inner granules, from the same situation: a, b indicate the same parts
as in the preceding figure ; c, a vertically-radial connective-tissue fibre.

Fig. 10. A vertical section near the inner surface of the inner granule-layer: a, smaller ;

b, larger inner granules ; c, a vertically-radial connective-tissue fibre ;
d, stout band-like (nervous) fibres resulting from the union of the finer oblique
fibres, and directed radially from the centre towards the periphery of the
retina and from the outer towards the inner surface.

Fig. 11. Two larger (ganglion-cell like) inner granules.

Fig. 12. Ganglion-cells and optic nerve-fibres.

Fig. 13. A vertical section through the Fovea, x20: 1, bacillary layer (at its outer
surface the choroid) ; owing to a slight artificial folding of this layer the cones
are represented as decreasing slightly in length from the edge to the centre
of the fovea instead of increasing as they actually do ; 2, the outer granule-
layer followed by the cone-fibre plexus ; 3, the intergranule-layer ; 4, tlie
inner granule-layer ; 5, the granular layer ; 6, the ganglionic and optic-nerve
layers.

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PkLL Trouus. MDOCCDCVI Plale XIX