Maximilian Salzmann.

The anatomy and histology of the human eyeball in the normal state, its development and senescence ; online

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seems to lie in the inner member of the cone) and the affected cone shows an abnormal
structure. The significance of this appearance is not yet clear.

4. THE OUTER PLEXIFORM LAYER (1 ' nternuclear layer)
(PL IV, 3, ap)

This layer shows a thickness of some 20 mu in the extrafoveal por-
tions of the retina, contains no cell-nuclei, and, therefore, takes only tissue
stains, such as eosin. It consists of a densely interwoven reticulum of
fibrous elements arranged principally in two directions perpendicular to
the surface of the retina and parallel to it (at least these directions pre-
dominate over the oblique ones). This structure is difficult to analyze
and by low power and defective staining gives the impression of granu-
lation; therefore, this layer was called the outer granular layer by the
older authors; by higher magnification and better staining of thin
sections it has a fine reticular appearance.

Two well-separated portions can be made out, an outer and an inner.
The outer portion (/) is the thicker; it includes some two- thirds of the
entire layer; it is, however, very subject to swelling and often appears still
thicker. The meshes are loose and a direction parallel to the surface rules.
It is the proximal portions of the rod-cone fibers (see above) which call
forth this picture, and the border between the two portions is formed
by the proximal ends of the cone-fibers (the previously reported cone
swellings), which all lie at the same level.

The inner portion (r) is much thinner and shows the fine reticular
(plexiform) structure in a typical way; it is, therefore, more closely
meshed and stains more densely than the outer portion. It is made up
mainly of the fine extensions of the horizontal cells of the inner nuclear
layer (see the same). In addition, Mueller's supporting fibers have a
part in the formation of the entire layer ; their fine extensions run parallel
to the surface.

In the neighborhood of the fovea the appearance of the outer plexi-
form layer changes in a remarkable way. The rod-and-cone-fibers take
on a more and more oblique direction and finally, in the immediate
vicinity of the foveal center, are arranged almost parallel to the surface.
Thereby, as well as through the marked condensation of the cone-fibers,
which are exclusively present in the center of the fovea, the outer portion
loses every trace of a reticular meshwork and takes on a fibrous appear-
ance. This modification of the outer plexiform layer bears the names of
Henle's outer fiber layer (PI. V, 3, 4, Hf).

This layer can be made out even at the temporal border of the papilla;


the more one approaches the center of the fovea, the longer the cone-
fibers become, the more they are superimposed in layers, and the thicker
the whole fiber layer is. It attains a maximum thickness of 40 to 50 mu
at about the border of the rod-free field, then thins rapidly, and is reduced
to a minimum in the very center of the fovea.

Since the outer fiber layer is equally well developed on all sides of
the fovea, a nearly circular area of almost 8 mm diameter concentric
with the fovea is formed in which the fibrillation has a component
directed radial to the foveal center.

The inner portion of the outer plexiform layer maintains the same
appearance and the same thickness in the region of the fovea as in extra-
foveal parts of the retina.

It is very difficult to obtain good preparations of the outer fiber layer, for this
layer is to a particular degree subject to swelling. This is also the reason why the
region of the fovea is so easily detached post-mortem.


(PL IV, 3,^)

This layer has a thickness of about 30 mu in the extrafoveal portions
of the retina; it is, therefore, appreciably thinner than the outer nuclear
layer, to which it is very similar in appearance in ordinary sections. The
inner nuclei, which make up this layer, are closely placed together; indeed,
the layer consists almost wholly of cell-nuclei with thin mantles of proto-
plasm from which processes of varying number and direction go off.
Here and there one finds larger cells with a rich protoplasm, wholly of the
appearance of ganglion cells, and provided as well with Nissl's granules;
part of the nuclei also show a more elongated form; these are the nuclei
of Mueller's fibers and lie about the middle of the inner nuclear layer.

This is nearly all one can see by the usual staining of cut sections.
The extremely complicated structure of this layer is only revealed by
the methods of Golgi and Ramon y Cajal.

According to Greeff (75), one can distinguish the following elements in the inner
nuclear layer:

(i) The horizontal cells, and, indeed,

a) the outer horizontal cells: these are small flat cells whose processes broaden
out in a direction parallel to the surface and end in the outer plexiform layer. They lie
in the outer portion of the inner nuclear layer.

b) The inner horizontal cells: these are larger than the former and likewise broaden
out in a direction parallel to the surface; their end branches mount up toward the
outer plexiform layer. Some of these have a descending (proximal or inward directed)
process as well, ending in the inner plexiform layer. They lie at a plane farther inward
than do the outer horizontal cells.

2. The bipolar cells. According to their union, these are divided into:


a) The rod bipolars: each of these has a basket of ascending (distal or outward)
processes and by means of these is in contact with the ends of the rod-fibers. The
descending (proximal) process is a single fiber coursing through the inner plexiform
layer, and invests a cell of the ganglion-cell layer by means of its less thick branches.

b) The cone bipolars: these lie very close to the outer plexiform layer, their ascend-
ing (distal) processes broaden out parallel to the surface of the retina and come in con-
tact with the proximal ends of the cone-fibers. The descending (proximal) process ends
in the inner plexiform layer with branches parallel to the surface. Some of these cells
are characterized by especially numerous ascending processes (giant bipolars, Greeff).

3. The amacrin cells: these form a continuous layer in the innermost portion of the
inner nuclear layer. Their pear-shaped body measures 10 to 13.7 mu and gives off
a single process inward. One finds:

a) Stratified amacrin cells: these have only one process ending in the inner plexi-
form layer with a superficially parallel branching.

b) Disseminated amacrin cells: the process branches many times and ends in all
parts of the inner plexiform layer.

c) Association amacrin cells: their protoplasmic processes (dendrites) end in the
first sublayer of the inner plexiform layer, the axis cylinder process courses parallel
to the surface for a long stretch on the border between the inner nuclear layer and the
inner plexiform layer and breaks up into numerous branches. These cells also come in
contact with the centrifugal fibers.

4. The already reported nuclei of Mueller's supporting fibers.

Toward the fovea the thickness of the inner nuclear layer very gradu-
ally increases and attains a maximum of 57 to 66 mu between the wall
about the fovea and its center; from there on it thins out very rapidly
and practically disappears in the center of the fovea. Widely isolated
cells are often seen along the inner surface of Henle's fiber layer (PI. V, 3).

Although the layers of the retina are entirely without vessels as far
as the outer plexiform layer, capillary vessels belonging to the system of
the arteria centralis retinae are found even in the inner nuclear layer (PL
IV, 3, c}.

(PL IV, 3, ip)

This layer shows individual variations in thickness from 1 8 to 36 mu;
in some instances, however, it maintains the same thickness in all parts
of the retina, even in the neighborhood of the fovea. It is wanting only
in the middle of the fovea and, indeed, in a somewhat greater expanse
than the inner nuclear layer.

It possesses a finely reticular appearance, like the inner portion of
the outer plexiform layer, to which in this respect it is, in general, similar,
and permits several secondary or sublayers (usually five) to be recog-
nized; these are darker stripes coursing absolutely parallel to the sur-
face of the retina and apparently caused by a thicker interweaving of
the fiber mesh. These sublayers arise because the end branches of the


nerve-cells, coursing parallel to the surface, only lie at certain levels of
the inner plexiform layer. The nerve-cells specially concerned in the
formation of the sublayers are the cone bipolars and the stratified amacrin
cells of the inner nuclear layer (along with their proximal processes),
and the stratified ganglion cells with their distal processes. In general,
the sublayers are not very clearly marked in the human retina; in the
retina of the birds they come out much more plainly.

Although the structural elements of the inner plexiform layer, includ-
ing the corresponding parts of the supporting fibers, are without nuclei,
yet this layer is not wholly devoid of nuclei. It is crossed by retinal
vessels and, moreover, other isolated displaced cells are present (ganglion
or amacrin cells?).


(PL IV, 3) G)

This layer has a thickness of 10 to 20 mu in the nasal part of the
retina and consists of a single row of ganglion cells separated from one
another by Mueller's fibers. Besides these, neuroglia cells are present.
In the neighborhood of the optic nerve the ganglion cells form a closed
row; farther toward the periphery they are more and more separated
from one another, and the spaces are filled out by the nerve-fiber layer.

Temporal to the nerve the ganglion-cell layer is somewhat thicker
and the cells superimposed in two layers. This superimposition increases
constantly in the direction of the fovea until, finally, at the wall of the
fovea 5 to 7 layers of ganglion cells are present. The thickness of the
whole layer is thereby increased to 57-85 mu on the nasal side, and 45-75
mu on the temporal side (Dimmer, 40).

From these relations in thickness it follows that the wall of the fovea
is mainly formed by the ganglion-cell layer. From here on, the thickness
of the layer decreases rapidly toward the center of the fovea, and it is
lost or fused with the rudiment of the nuclear layer while still in the
region of the clivus (PL V, 4).

Since the same relations are repeated on all sides of the fovea, there
arises a fairly extensive district in the retina in which the ganglion cells
are superimposed.

This area (area centralis, Chievitz, 32) has about the same extent
as the other fiber layer of Henle, i.e., a circular surface area of about 4 mm
radius; from the fact that the stratification of the ganglion cells in layers
can be made out under all circumstances, even in advanced cadaverous
changes, we have here a sure means of differentiating the temporal from
the nasal side of the retina and the section need not necessarily go
through the fovea.


The individual ganglion cells show a most varied appearance. In the
extrafoveal portions of the retina very large ganglion cells with a diameter
of up to 30 mu occur; their nuclei are almost exactly round, clear, and
10 to ii mu in diameter. The nuclei contain large shining nucleoli.
More numerous than these are the smaller ganglion cells with a more
oval nucleus of 8 to 9 mu in diameter and a 11 to 12 mu protoplasmic
body. Only the smaller forms are found in the neighborhood of the
fovea, and, corresponding to the general arrangement, the cell-body
is obliquely elongated.

The ganglion cells are multipolar and have numerous protoplasmic
processes (dendrites), which broaden out in the inner plexiform layer
and are for the most part provided with axis cylinders going over into
nerve-fibers of the adjoining layer. The protoplasm contains the so-
called Nissl granules; these are granules and shoals of varying size, of
rounded or polyhedral form, giving an elective stain especially with blue
dyes, ordinary and polychrome methyl blue, thionin, etc., and at times
also with hematoxylin. The granula extend into the protoplasmic
processes as well, but not into the cylinders.

The peculiarities of the Nissl granula in man are little known; on
technical grounds they have been best studied in lower animals (Bach,
13; Birch-Hirshfeld, 25; Abelsdorff, 2; only the latter writer depicts
a cell in man). In the normal retina of an eye enucleated for orbital
carcinoma which I was able to .study, the large cells contained granula
varying much in size, quite uniformly distributed through the protoplasm,
usually with a granula-free zone immediately about the nucleus; the
smaller cells contained correspondingly small granula. In general, it is
very surprising how well these structures, which otherwise are very
easily disintegrated, are retained in detachment of the retina following
traumatic inflammation.

Other fixative and staining methods bring out a fibrillar structure
in the cell-body and its processes. Dogiel (44) discovered these struc-
tures with his methyl-blue method; then Embden (57) demonstrated
them by the method of Bethe, and finally Bartels (16) in the human
with the method of Bielschofsky. According to Bartels, the fibrillae
course from one process to another, and in this way pass by the cell-body;
in part, too, they radiate from the processes toward the nucleus and possi-
bly form there a network. The fibrillae are extremely fine and smooth
(without nodosities) ; they lie more loosely in the protoplasmic processes ;
in the axis cylinder processes they are closely pressed together.

According to Dogiel, the protoplasmic processes of cells of the same type are united
into nets. According to the authors named, it follows from the fibrillar structure


that no fundamental difference exists between the protoplasmic processes and the axis
cylinder process; both are of a nervous nature and the fibrillae are genuine conduct-
ing organs.

The controversy as to whether the ganglion cells have a granular or a fibrillar struc-
ture appears to me to be quite useless; both structures may very well be present at the
same time and only one or the other come out after a certain fixation. A view which in
a certain sense lies between these two extremes is that of Held concerning the net-like
structure of the body and the processes of the nerve-cells (Archiv. fur Anatomie und
Physiologic, anatomische Abteilung, 1897, p. 204), yet the observations of this investi-
gator were not made on the retina.

The Nissl granules cover the diplosome of the ganglion cell; this structure is, there-
fore, only visible in the embryonal eye, before the development of the granula (cf. chap,

According to the manner in which the dendrites end in the inner plexiform layer
(wholly analogous to the amacrin cells), one distinguishes stratified and disseminated
ganglion cells. The former spread their end brushes out in one or more planes of the
inner plexiform layer and in this way produce their sublayers. The diffuse ones
branch like a tree and end everywhere throughout the inner plexiform layer. A part
of the cells send no axis cylinders into the nerve-fiber layer; they are looked upon as
displaced amacrin cells.

The neuroglia cells, which we meet here for the first time in the retina,
have smaller and more densely-stained nuclei than the ganglion cells,
and a flat body. Golgi preparations make them look like spider cells
here, as in the nerve-fiber layer, i.e., cells provided with numerous fine


(PL IV, 3, AO

This layer is thickest (20 to 30 mu) about the circumference of the
optic-nerve entrance, and, indeed, about the upper, nasal and lower

Toward the periphery its thickness decreases, rapidly at first, then
more slowly. In the extreme periphery the nerve-fibers and the ganglion-
cell layer flow together, so to say, i.e., the few ganglion cells still present
in this zone lie between the nerve-fibers and reach to the basal cones
of the supporting fibers.

At the temporal border of the optic nerve the nerve-fiber layer is very
much thinner (some n mu); its thickness decreases still farther toward
the fovea; it goes a little way beyond the wall of the fovea, then dis-
appears entirely (PL V, 4).

Unlike the rest of the layers of the retina, in which a direction parallel
to the surface or a plexus formation predominates, the nerve-fiber layer
shows an exquisite fibrous structure, in which the elements are in general
arranged radial to the optic-nerve entrance. In the entire nasal half of the


retina this convergence toward the optic nerve is not disturbed; in the
temporal half, however, the arrangement of the fibers varies in that those
fibers which pass the area of the fovea on their way to the optic nerve
bow away from it and go around it in circles above and below the fovea.
In this way a sort of raphe arises in the meridian of the fovea on the
temporal side in the periphery; from this the fibers go off like feathers,
above and below, and finally at the temporal border of the fovea itself
they form an actual ring (Greeff, 65). Only the few fibers of the fovea
itself and those which course from the portions lying between it and the
optic nerve run fairly straight. Since, furthermore, these fibers remain
close to one another and frequently show isolated disease, one calls this
the papillomacular bundle; the loss of its function calls forth the
appearance of typical central scotoma.

The fibrous structure of the nerve-fiber layer is responsible for the fact that extra-
vasation into this layer appears to be made up of fine striae or short streaks arranged
radial to the optic nerve. Extravasates in the other layers of the retina appear as
rounded flecks, on the other hand.

The nerve-fibers in the retina are everywhere grouped in small
bundles; these unite into a sort of net, with narrow elongated meshes.
Rows of Mueller's fibers lie in these meshes and the rows have the same
direction as the nerve-fibers. The nerve bundles are spread out in one
plane, as a general thing; the nearer one approaches the optic nerve,
however, the more slender and the higher the bundles become, until when
very close to the optic nerve, they become superimposed and in this way
go over into the grouping characteristic of the optic nerve itself.

The nerve-fiber layer, therefore, presents a varying picture dependent
upon whether the section runs parallel or at right angles to the fibers;
on longitudinal section the nerve-fiber layer shows a fibrillation parallel
to the surface and only shows the Mueller's fibers indistinctly; the cross-
section, on the other hand, shows the Mueller's fibers very plainly, and
the cross-sections of the individual small nerve-fiber bundles lying in the
arcades formed by Mueller's fibers have a reticular appearance. One
sees the picture of the longitudinal section in meridional sections and the
cross-section picture in equatorial sections. As a result of the unusual
course of its fibers, the region of the fovea makes an exception: one sees
the cross-section picture on the temporal side in a horizontal section
through the fovea; on the nasal side of the fovea, i.e., between it and the
papilla, one sees the longitudinal section picture. A vertical section of
the fovea shows the cross-section picture on each side of the depression.

Aside from the nerve-fibers and Mueller's supporting fibers, the layer
in question also contains neuroglia. As in the optic nerve this consists
of cells and fibers. The cells have a longish, quite densely-staining


nucleus, whose axis is directed parallel to the course of the nerve-fibers
(PI. IV, 3, g/), and a small amount of protoplasm of varying form. The
fibers are very fine and form a meshwork between the nerve-fibers. (For
more details concerning the neuroglia, see chap, viii.)

Finally, the nerve-fiber layer also contains the larger retinal vessels,
branches of the arteria and vena centralis retinae. They are imbedded in
the nerve-fiber layer and also in part in the ganglion-cell layer, and do not
bulge the inner surface of the retina inward at all or not appreciably so.
The vessel wall is relatively little developed, especially the muscularis of
the arteries ; the adventitia'l connective tissue is sharply set off against the
surrounding nerve tissue. According to Kreuckmann (123), the glial
reticulum ends at the vessel wall in a sort of border membrane, which he
calls the limitans perivascularis.

These tissues (glia and vessel wall) , which have originated from different embryonal
layers, are not infrequently separated under pathologic conditions, and, for instance,
in atrophic conditions of the retina resulting from obliteration of the vessels, an
interspace is formed into which the pigment epithelium frequently grows; the well-
known picture of pigmentary degeneration of the retina arises in this way.

The modern methods of study (Dogiel's methyl-blue staining, Golgi's and Ramon y
Cajal's methods) bring to light still other details not to be recognized in ordinary sec-
tions (Greeff, 65). The nerve-fibers are clear, non-medullated fibers, varying from an
immeasurable fineness up to a thickness of 3-5 mu. Divisions of the fibers occur and
among the typically coursing fibers one finds individuals which cross the others.

The majority of the fibers come from the ganglion cells of the retina, and are,
therefore, centripetal and serve for the conduction of visual sensations. Aside from
these, fibers are, however, found of which the nerve-cells do not lie in the retina and
which, therefore, are centrifugal conductors. According to Ramon y Cajal, these
are larger than the centripetal, yet they course in the nerve-fiber layer with them. If
one follows such a fiber in a centrifugal direction, one sees it course through the ganglion-
cell layer and the inner plexiform layer and end in an amacrin cell, by means of a
perivascular nest, and at other amacrin cells by processes. These fibers do not press
deeper into the retina than the layer of the amacrin cells.

Moreover, the region of the fovea is not entirely devoid of nerve-fibers. A deli-
cate ring is found at the place where the nerve-fiber layer seems to cease in ordinary
preparations, according to Dogiel, and from this a wide-meshed plexus of fibers extends
over the floor of the fovea.

The Radial or Mueller's Fibers

(PL IV, 3, M)

All of the layers of the retina heretofore discussed contain a frame-
work which is not of a nervous nature, i.e., it does not serve either for the
perception or conduction of light (in a centripetal or centrifugal direction).
This framework consists of elongated cells, the radial or Mueller's sup-


porting fibers already repeatedly mentioned. They course through the
extrafoveal portions of the retina parallel to the surface; starting along
the inner surface of the retina in conical expansions (closely placed bases),
they form quite closely placed rows of small nerve-fiber bundles in the
nerve-fiber layer, diverge and break up beyond the ganglion-cell layer.
From the inner nuclear layer on, the fibers lie isolated and are uniformly

They participate especially in the formation of the plexiform layers
in that they give off numerous fine extensions parallel to the surface in
the level of these layers. Furthermore, they form the reticulum of the
nuclear layers by means of wing-like processes, go over into the membrana
limitans externa, and finally end between the inner members of the rods
and cones in the above-reported fiber-baskets by means of fine fibrillae.
Their cell nature is shown by a longish nucleus lying in a mid-level of the
inner nuclear layer.

Since the Mueller's fibers possess no processes or branchings (or only a
few) in the territory of the nerve-fiber and ganglion-cell layers, they are
much more plainly set off from the surrounding tissues in these layers
and are to be seen without special aid in ordinary preparations, especially
when the section falls at right angles to the course of the nerve-fibers,
because one then has the rows of fibers before him in profile view. In
the rest of the layers they are not to be made out so off-hand; they and
their relations to these layers come out plainly by the method of Ramon

Online LibraryMaximilian SalzmannThe anatomy and histology of the human eyeball in the normal state, its development and senescence ; → online text (page 9 of 27)