Comparative study of the fine structure
of retinal Miiller cells in various
vertebrates
Shigekazu Uga and George K. Smelser
A comparative study was made of the fine structure of Midler's cells in various vertebrates.
In those species with vasctdar retinas (cat, rat, and opossum), the organelles in the cytoplasm of
the Miillerian cells were extremely scanty in the outer layer, but more numerous vitread to the
inner nuclear layer of the retina. The microvilli were relatively few. When there was a supraretinal vascular membrane in the vitreous (frog, carp, Fundulus, and bowfin), distribution of
organelles in the Miillerian cell cytoplasm was similar to that in the vascular type of mammalian retina. The cytoplasm of the Miillerian cells in avascular retinas (rabbit, pigeon, lizard,
turtle, Necturus, and dogfish) had many mitochondria, occasional Golgi apparatus, and microvilli were numerous around the base of the inner segments of the photoreceptor cells. Many
glycogen particles were scattered throughout the cytoplasm of Miillerian cells in the avascular
retina, expecting in bird and lizard, but were somewhat less in the Miillerian cells in vascular
retinae. Arrangement of nuclei of Miillerian cells varied depending on the location of the
amacrine cells. The external limiting membrane was composed of zonulae adhaerentes in many
species, but in a few (frog, carp, and Fundulus), there were extensive gap functions between
Miillerian cells in addition. In the carp retina, desmosomal connections (macula adhaerens)
were also found forming part of the external limiting membrane. In reptiles, a peculiar apparatus, consisting of a network of dense filamentous material occurred in the cytoplasm of the
Miillerian cells at the level of the external limiting membrane.
Key words: Mullerian cells, retina, fine structure, comparative anatomy,
retinal glia, Mullerian mitochondria.
R
From the Department of Ophthalmology, College
of Physicians and Surgeons, Columbia University, New York.
This investigation was supported by National
Institutes of Health Research Grants Nos. EY
00184 and EY 00190 and Public Health Service
Research Career Program Award No. EY 19609,
all from the National Eye Institute and by a
Fight for Sight Postdoctoral Research Fellowship from Fight for Sight, Inc., New York City.
Manuscript submitted for publication July 26,
1972; manuscript accepted for publication March
27, 1973.
'etinal Mullerian cells have several
functions. They allegedly support the neurons mechanically, and may mediate their
metabolic requirements. The metabolic
function of the Mullerian cell in the retina
has been demonstrated by recent histochemical investigations1"7 and it has been
suggested that they "buffer" the potassium
liberated by neuronal activity.s However,
since retinal vascularization in vertebrates
differs from species to species, it may be
434
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Study of retinal Milller cells in vertebrates 435
expected that Miillerian cell structure also
varies, depending, on the blood supply. To
date, the fine morphologic features of Miiller cells have been separately reported in
some species,9"12 but a comparative analysis
has not been made in relation to retinal
vascularization.
The purpose of this paper is to describe
and compare the fine structure of Miillerian
cells in retinae of various vertebrates, including those with vascular and avascular
retinae.
Methods and materials
The following species, which may be roughly
divided into three groups on the basis of retinal
vascularization, were used in this study: (1)
intraretinally vascularized; cat, albino rat, American opossum (marsupial), and eel (AnguiUa
rostrata); (2) supraretinally vascularized; dutch
(pigmented) rabbit (myelinated portion), grass
frog ( Rana pipiens), carp (Cyprinus carpio),
killifish (Fundulus heteroclitus), and bowfin (Amia
calva, a primitive teleost); and ( 3 ) avascular;
rabbit (nonmyelinated portion), pigeon, painted
turtle (Chrysemys picta), lizard (Anolis caroliniensis), mud puppy (Necturus maculosus), and
smooth dogfish (Mustelus canis). All were
adults.
Eyes from cat, rat, rabbit, opossum, and pigeon
were removed under anesthesia, those of reptiles,
amphibians, and fish were enucleated after decapitation. All eyeballs were rapidly opened by an
incision just anterior to the equatorial plane and
the lens and vitreous body were carefully removed
with forceps. The cup-shaped retinas were immediately immersed in either 3.5 or 4.0 per cent
glutaraldehyde (buffered with 0.1M phosphate
solution at pH 7.4) for two hours, and thereafter
placed in 1 per cent osmium tetroxide with the
same buffering system for two hours. Dehydration
was started in 25 per cent alcohol and, when in
70 per cent alcohol, the specimens were cut into
small pieces. In the cat, rabbit, opossum, pigeon,
and dogfish, the retina and choroid were separated
from the sclera at this time. After further dehydration in alcohol and propylene oxide, the specimens
were embedded in Epon 812 and cut on a PorterBlum MT-2 microtome. Thick sections (about 1 A)
were stained with 0.5 per cent toluidine blue with
borax, and examined by light microscopy to determine orientation and content of each specimen.
For electron microscopy, thin sections (gray-silver
interference color) were stained with uranyl acetate and lead citrate, and examined with a Siemens
Elmiscope 1 or 1A.
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Results
Distribution of mitochondria in the cytoplasm of the Miiller's cell varied. In the
vascularized retina (cat, rat, and opossum),
mitochondria were seldom observed in the
outer (sclerad) portion of the retina, but,
near the vitreous, where the cytoplasm of
the Miillerian cells form footplates, they
were abundant (Fig. 3). In the eel, however, the mitochondria were almost exclusively localized in the apical (sclerad)
and middle portions of the Miiller's cell
cytoplasm (Fig. 1).
The superficially vascularized retinas
(frog, carp, Fundulus, and bowfin) contained many mitochondria in the inner cytoplasm of the Miillerian cell, vitread to the
inner plexiform layer (Fig. 6), and a few
in the outer cytoplasm sclerad to the nucleus. On the other hand, in the myelinated
portion of the rabbit retina, an aggregation
of mitochondria was found in the apical
region near the external limiting membrane, but they were entirely absent in the
cytoplasm vitread to the outer plexiform
layer.
In avascular retinas, (pigeon, turtle, lizard, and Necturus), a dense aggregation of
mitochondria was constantly seen in the
apical region of the Miillerian cells (Figs.
7 and 16), while the inner cytoplasm between the vitreous and the outer plexiform
layer lacked them entirely (Figs. 4 and 8).
Distribution of mitochondria in the nonmyelinated portion of the rabbit retina was
quite similar to that of the myelinated portion of the same eye (Figs. 2 and 5).
The position of a Golgi apparatus in Miillerian cells also varied with the species; in
the cat and opossum it was on the level of
the outer part of the inner nuclear layer,
sclerad to the cell body. The Golgi apparatus
was nearer the nucleus in the rat retina. In
the pigeon, frog, Necturus, and the rabbit
(both the myelinated and nonmyelinated
portions) it was at the level of the sclerad
part of the outer plexiform layer (Fig. 7).
In the turtle and the lizard, it was found in
the outer part of the outer plexiform layer.
436
Investigative Ophthalmology
June 1973
Uga and Smelser
»7
m
N.C
N.C
*
N.C
N.C
Fig. 1. Apical region of the eel retina which has a deep vascular system. Many mitochondria
(m) are seen in the cytoplasm of the Miiller cells just vitiead to the external limiting membrane (ELM). Elongated processes of pigment epithelium (pi) reach near the base of the
inner segments of the photoreceptors. A wall of tangentially cut blood vessels (bv) is shown.
In this species, the cone nuclei (NC) lie external to the external limiting membrane. Rod
nuclei: (NR) (x3,500 original magnification.)
Fig. 2. Apical region of the nonmyelinated portion of the rabbit retina which lacks a- vascular
system. Mitochondria (m) are abundant in the apical cytoplasm of the Miiller cells near the
external limiting membrane (ELM). Microvillous processes (vi) extend outward into the
ventricle lumen among rod inner segments. NR = rod nuclei. (x7,000.)
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Study of retinal Miiller cells in vertebrates 437
-fi
\
sER
sER
Fig. 3. Inner plexiform layer of a vascular retina (opossum). A process of a Miiller cell is
seen containing characteristically few mitochondria (m). together with smooth-surfaced endoplasmic reticulum (sER), glycogen particles (gl), fine filaments (fi)? and neural processes
(np). Microtubules can be identified in cross-sections (xl.2,000.)
Fig. 4. Inner plexiform layer of an avascular retina (Necturus). The cytoplasm of the Miiller
cell is entirely lacking in mitochondria, in this region, but other organelles, such as smoothsurfaced endoplasmic reticulum (sER), glycogen particles (gl), and filamentous materials (fi)
are present similar to the case of the vascular retina, as shown in Fig. 3, neural processes:
(np). (xl5,000.)
In the teleost retina (carp, Fundulus, eel,
and bowfin) the Golgi apparatus occurred
in the supranuclear region, similar to the
cat retina, but in the elasmobranch (dogfish) it was more external, on the level of
the outer nuclear layer, as in the reptilian
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retina (Fig. 8). In all species, however, it
was apical, i.e., sclerad, to the nucleus.
The distribution of glycogen particles,
250 to 300 A in diameter, varied with different species; in the cat, rat, and opossum
retinas they were moderately abundant,
438 Uga and Smelser
Investigative Ophthalmology
June 1973
sER
Fig. 5. Innermost region of the avascular (nonmyelinated) portion of the rabbit retina. Smoothsurfaced endoplasmic reticulum (sER) and glycogen particles (gl) are abundant in the
Miillerian cell cytoplasm, but mitochondria are not seen in this region. Ganglion cell: (GC).
Internal limiting membrane: (ILM). Nerve axons: (na). (x8,500.)
Fig. 6. Innermost region of the superficially vascular retina (carp). Several mitochondria (m)
and abudant glycogen particles (gl) are seen in the cytoplasm of the Muller cell in the vicinity
of a blood vessel which contains an erthrocyte. Nerve axons (na) are mostly myelinated in this
retina. Endothelial cell: (En). Internal limiting membrane: (ILM). (#7,500.)
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Study of retinal Muller cells in vertebrates 439
whereas in the pigeon and lizard there were
only a few. Abundant glycogen particles
were found in rabbit (both the medulated
and nonmedulated portions), turtle, amphibian, and fish retinas.
Smooth-surfaced endoplasmic reticulum,
in the vitread cytoplasm of the Miillerian
cells, showed a somewhat different distribution among species. In many it was abundant, but in the pigeon and lizard it consisted of relatively small numbers of cisternae. However, in the latter species, fine
filaments, about 50 A in diameter, were
abundant.
In the rabbit retina, which has blood
vessels supplying only a limited portion of
the retina, the distribution of organellas
was very similar in the Miillerian cells of
the vascular as well as the avascular portion. In the myelinated portion, there were
two glial elements, oligodendrolglia and astrocytes. The astrocytes were located close
to the vessels, and were always enveloped
by basement membrane material. Occasionally, processes of the astrocytes grew out
into the vitreous through the internal limiting membrane and tended to wrap around,
or enclose, the vessels. Consequently, the
internal limiting membrane was interrupted
by astrocyte processes protruding into the
vitreous.
A pair of centrioles was always recognizable in the apical cytoplasm of Miillerian
cells near the external limiting membrane
(Fig. 18). Often a ciliary process, about 1.2
/x in length, with a short striated bundle at
its base, arose from one centriole. In the
turtle retina, this cilium was atypical in that
it consisted of a 9 + 0 triplet of tubules in
its base (Fig. 19) and a 7 + 1 doublet of
filaments in its distal portion (Fig. 20). In
the pigeon and lizard, ciliary processes projected either from the side of the cells into
the space between them, or into the ventricle lumen. A cilium was not encountered
in the opossum, bowfin, and dogfish Miillerian cells.
In addition to the organelles mentioned
above, Miillerian cells contained numerous
fine filaments in their inner cytoplasm vit-
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read to the inner plexiform layer. Sometimes, the fine filaments formed a bundle
in the carp and eel retina. Rough-surfaced
endoplasmic reticulum was often observed
in the perinuclear region. Microtubules,
oriented parallel to the long axis of the cell,
were dispersed throughout the elongated cytoplasm of the Miillerian cells in all species.
The location of Miillerian cell nuclei differed among species. Figs. 12 and 13 show
vertical sections of the retina through the
inner nuclear layer. The Miillerian cells are
darkly stained. In mammalian retinae (cat,
rat, rabbit, and opossum), and in fish (teleosts and elasmobranchs), the nulcei of Miillerian cells were located in the first and
second innermost zones of the inner nuclear
layer (Fig. 12), whereas in the urodelian
retina (Necturus) they were invariably seen
in the second innermost layer of this zone.
In the bird (pigeon), reptiles (lizard and
turtle), and anura (frog), they always occurred more externally, in the middle of this
layer (Fig. 13).
Delicate microvilli of the Muller cells, the
fiber baskets of Schultze,13 invariably projected from the apex of the cells into the
ventricle lumen, but differed in form
among various species. Figs. 14 and 15
show cross-sectioned profiles at the base of
the inner segments. In the intraretinally
vascularized retina (cat, rat, opossum, and
eel), Miillerian cells possessed only a small
number of microvilli (Fig. 14). In the supraretinally vascularized type (frog, carp,
Fundulus, bowfin, and rabbit, in both the
myelinated and nonmyelinated portions)
they were moderately abundant and sometimes were grouped, owing to lateral cytoplasmic expansions of the photoreceptor
cells (frog and bowfin). In the avascular
retina (pigeon, lizard, turtle, and dogfish)
they were very numerous (Fig. 15). In addition, in reptiles and the bowfin, broad processes often occuned among the ordinaiy
microvilli (Fig. 17). These varied in size and
shape, and contained abundant glycogen
particles. The Miillerian processes were exceptionally short and irregular in Necturus.
The amphibian (Necturus and frog) Miil-
440 Uga and Smelser
Investigative Ophthalmology
June 1973
M
M
M
11
Figs. 7 through 11. For legend see opposite page.
lerian cells have deep infoldings in the most
apical and most basal portions. These are
not invariably found in all sections, perhaps
due to the orientation of the block of tissue.
Such infoldings have been described by
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Lasanskys in the toad and by Miller and
Dowling," in Necturus. This arrangement
effectively increases the surface of the cell
exposed to the space surrounding the photoreceptors.
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Study of retinal Miiller cells in vertebrates 441
Comparison of the structure of the external limiting membrane was also made
among species. Junctions were characterized by slightly increased electron density
of the membranes and neighboring cytoplasm (Fig. 9). The intercellular space was
about 200 A, though frequently narrowing
to about 100 A over a short distance. The
former was undoubtedly of the zonula adhaerens type (intermediate junction), as
demonstrated by many workers. It could
not be determined, in our material, whether
the latter type was a fusion, or simply a
narrowing of the space between the apposed membranes. The narrowed intercellular space between junctions was visible,
however, even when the retina was cut
tangentially. These junctional complexes
were the same between photoreceptors
and Miiller cells as between adjacent
Miiller cells in all species, except frog, carp,
and Fundulus. In these species, the cell
junctions between adjacent Miillerian cells
consisted of extensive "tight" junctions and
intermediate (zonula adhaerens) junctions
(Fig. 10). At high magnifications of the
"tight" junction, the two apposed membranes were found to be separated by a
narrow space which forms a gap junction
(Fig. 11). In the carp retina, desmosomal
connections (Macula adhaerens), were observed, in addition to the two types mentioned above. These cell junctions occurred
only between adjacent Miiller cells, never
between the photoreceptor and Miiller cells,
where only intermediate junctions were
present.
A most interesting arrangement of the
cone nuclei was noted in the eel retina.
Here, most of the cone nuclei lay external
(i.e., sclerad) to the external limiting membrane. This condition was general, observable near the ora serrata, as well as in the
fundus of the retina. In some instances a
cone nucleus was at the level of the external
limiting membrane as if it were about to
squeeze outward from the mass of rod
nuclei. The pigment cell processes reached
far inward in the eel, clasping the perikaryon of the cone cells as well as the inner
and outer segments (Fig. 1).
In reptiles, a lattice network of dense
filamentous material was found in the Miillerian cell cytoplasm at the level of the external limiting membrane (Fig. 21). This
network had a flattened dense body where
the filaments intersected, and structurally
were continuous with the dense material in
the terminal bar. Several microtubules interposed between masses of the filamentous
material.
The results described are summarized in
Figure 22.
Discussion
Much information concerning retinal vascularization, derived from light microscopy,
has been reviewed in a standard textbook.™
Many mammalian retinas have an intraretinal blood supply, but rabbit and hare
retinas are supplied by supraretinal vessels
running along the horizontal medulated
nerve fibers. Bird retinas are avascular, but
a peculiar vascular structure, the pecten,
Fig. 7. Outer portion of the avascular retina (pigeon). Golgi apparatus (G) in the Miiller cell
(M) is located at the outer nuclear layer. Mitochondria (m) are seen in the outer end of the
Miillerian cell cytoplasm. Process of Landolt's club: (LC). Nucleus of photoreceptor: (NP).
(x7,500.)
Fig. 8. Outer region of the dogfish retina (avascular). Elongated sacs of Golgi apparatus (G)
in the Miillerian cell (M) are in the outer portion of the outer plexiform layer. Masses of
glycogen particles (gl) are seen. Nucleus of photoreceptors: (NP). (x9,000.)
Fig. 9. External limiting membrane of the rabbit retina, showing cell junctions between
photoreceptor (P) and Miiller cells (M) and between adjacent Miiller cells. (x47,000.)
Fig. 10. External limiting membrane of the frog retina. Note an extensive gap junction
(between arrows) occurring between neighboring Miiller cells (M). This junction is extensive
but lies only between Miillerian cells. (M) Photoreceptor cell: (P). (x45,000.)
Fig. 11. Higher magnification of the gap junction (frog retina). (xl35,000.)
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Investigative Ophthalmology
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Uga and Smelser
AC
m N.M
N.M
f\[
M
AC
, AC
IPL
Fig. 12. Inner nuclear layer of the cat retina. The nuclei of the Miiller cells (NM) are arranged at the innermost zone of this layer together with amacrine cells (AC). Inner plexiform layer: (IPL), Miiller cell: (M). (x5,000.)
Fig. 13. Inner nuclear layer of the pigeon retina. The nuclei of the amacrine (AC) are often
piled up in the vitread half of this layer, and the Miiller cell nuclei (NM) are in the middle
of the layer. The other cells shown here are bipolar cells. Nucleolus: (nl). Inner plexiform
layer: (IPL). (x2,000.)
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Study of retinal Mutter cells in vertebrates 443
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Vi
rod
rod
VI
VI
VI
cone
VI
vi
Fig. 14. Horizontal section of the rat retina at the level of the base of the rod inner segments.
Relatively few microvilli (vi) of Miillerian cells are seen among them. (xl3,000.)
Fig. 15. Horizontal section of the pigeon retina through the base of the inner segments. In this
species the microvillous processes (vi) of the Miiller cells are numerous between the cone
inner segments. (xl5,500.)
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Uga and Smelser
Figs. 16 through 21. For legend see opposite page.
grows out from the optic disc into the vitreous. In reptiles, the lacertilean (lizard) and
chelonian (turtle) retinas are also avascular, but the lacertilean eye has a vascular
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structure (a conus papillaris) extending
into the vitreous, as the pecten does in
birds. The chelonian eye entirely lacks vessels in both the vitreous and the retina. In
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Study of retinal Muller cells in vertebrates 445
amphibians, the anuran eye (frog) has a
vascular membrane in the vitreous lying on
the surface of the retina, but the urodelian
retina (salamander) is quite avascular. The
elasmobranch retina (fish) is also avascular, whereas most teleost eyes are supplied
by a superficial network on the inner surface of the retina. Of the teleosts, the eel,
Anguilla, is said to be the only known exception, having an intraretinal vascular
system.
The present investigation showed several
variations in the fine structure of the Miillerian cells among various species.
The variation in the distribution of mitochondria and Golgi apparatus may be related to the vascularity of the retina. Except
in the eel, mitochondria were rarely observed in the apical cytoplasm in the vascular retina (both intra- and supraretinally
vascularized). The Golgi apparatus was
generally situated near, and apical to, the
nucleus. On the other hand, in an avascular
retina the mitochondria were always concentrated in the apical (sclerad) region, and
the Golgi apparatus was also found in the
outer portion of the retina. These were
notable features of the Miillerian cells of
avascular retinas, and may indicate that the
outer portion of the cell is metabolically
very active. Similar findings have been reported in the avascular retina, such as
reptiles10'lx and chick embryos.12 Moreover,
a significant heavy staining for succinic de-
hydrogenase, suggesting the presence of aggregated mitochondria, has been obtained
in this region of avascular,7 or less vascularized, retinas.3'5
Evidence also suggesting high metabolic
activity may be the number of Miillerian
cell microvilli. Relatively few Miillerian
microvilli were found in the intraretinally
vascularized retinae, whereas the supraretinally vascularized and avascular retina
possessed numerous microvilli around the
base of the photoreceptor inner segments.
Necturus retina may be an exception in
having extremely short microvilli. The presence of great numbers of microvilli represents an enlarged surface area of the cell
and perhaps greater permeability compared
with the same area of the vascular retina. In
addition, the histologic features of the pigment epithelium of an avascular retina, indicating a well-developed basal infolding
and large, oriented mitochondria, also suggest an active exchange of metabolites in
this cell.15 Therefore, these structural differences between the two types of retina appear to reflect a contrast between dependence of retinal nutrition on either the
choroidal or retinal vessels. Since the number of microvilli of the Miillerian cells may
also be related to the degree of development of the processes of the pigment epithelium and/or the neuron-glial (Miillerian
cell) ratio in the retina, it may not be
proper to generalize only from the view-
Fig. 16. Apical region of the Necturus retina. The Muller cells in this species extend extremely
short, irregular microvilli (vi) into the ventricle lumen between photoreceptor inner segments.
Mitochondria: (m). Nucleus of photoreceptor: (NP). (x4,800.)
Fig. 17. Apical region of the bowfin (Amia) retina. Broad processes (bp) of the Muller cells
containing abundant glycogen particles (gl) occur among ordinary microvilli (arrows). External limiting membrane (ELM). (xlO.OOO).
Fig. 18. Apical region of the rat retina showing paired centrioles in the Muller cell. (x28,000.)
Fig. 19. Cross-section of the centriole in the apical cytoplasm of a Muller cell (turtle retina).
(x46,000.)
Fig. 20. Cross-section of a ciliary process of a Muller cell projecting into the ventricle lumen
(turtle retina). The cilium always consists of a 7 + 1 system of paired tubules in this species.
(x66,000.)
Fig. 21. Horizontal section of the lizard retina at the level of the external limiting membrane.
A lattice network of dense filamentous material, which is continuous with dense material of
terminal bars (t), is seen in the Muller cell cytoplasm. Arrows show profile of microtubules.
Photoreceptor cell: (P). (x26,000.)
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Investigative Ophthalmology
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Uga and Smelser
Cat
Rot
Rabbit
Opossum
Pigeon
Turtle
Lizard
ILM
Frog
Neciurus
Carp
Fundulus
Eel
Bowfin
Dogfish
Fig. 22. A highly schematic representation of the Miillerian cells in the species studied. The
actual shape and relative size of the cells is not shown, however, the type, size, and relative
frequency of the Miillerian processes and the type of junctional complexes forming the external
limiting membrane (ELM) are shown. The complicated branches of these cells which penetrate the inner and outer plexiform layers are only indicated. Representation of their actual
diversity is not attempted. The relative concentration of mitochondria (m) is indicated in
different parts of the Miillerian cell. In the same manner, the location of the Golgi apparatus
(G) is shown. Rough-surfaced endoplasmic reticulum (rER) was always found in a perinuclear position. The irregular lateral branches of the Miillerian cells which are found among
the neural processes of the inner and outer plexiform layers are indicated. The basal lamina
invariably covers the Miillerian cell's cytoplasm on the vitreous surface. The vascular supply of
the various retinas studied is shown by drawings of cross-sections of a capillary (cap) located
at the most outward (sclerad) level reached by the vascular system. The absence of vessels
indicates that the retina is avascular. The rabbit retina diagram is the nonmyelinated portion
which is avascular. DF: dense filamentous material; ce: centriole; ILM: internal limiting
membrane; N: nucleus; ZA: zonula adhaerens; ZO: zonula occludens.
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Study of retinal Milller cells in vertebrates 447
point of retina vascularization. However,
Mullerian cells in the avascular retina tend
to possess significantly more numerous microvilli than those of the vascular retina.
The distribution of mitochondria in the
eel with the intraretinal vascular network
was an exception to the generalization mentioned above. Mitochondria were located
not only in the middle, but also at the apex,
of the Mullerian cells. It is noted that the
retinal capillary net in this fish is distributed in the inner and outer nuclear layers11
in relation to the location of mitochondria.
However, it cannot be ruled out that the
mitochondria in the apical portion may be
there because of an exchange of metabolites
from the choroidal side, for the eel retina
possesses closely packed photoreceptor elements in the outer layer and long, welldeveloped microvilli of the pigment epithelium which reach the level of the inner
segments of the photoreceptors (Fig. 1.)
Contrary to the impression given in
Duke-Elder,11 we found the eel to possess a
choroidal blood supply, although it was
much less well developed than in most vertebrates. The choroid consisted of layers of
melanocytes and some major vessels which
supplied a choriocapillaris. Therefore, the
eel retina does receive a choroidal blood
supply, although we cannot estimate its
relative importance.
Variation in the distribution of glycogen
particles may also be correlated with vascularity of the retina. The avascular retina
contained abundant glycogen particles,
whereas these were less abundant in the
vascular retina. The pigeon and lizard
retinas were exceptions to this generalization, however, in both species there was a
vascular structure (the pecten or the conus
papillaris) which may have provided indirect blood-borne nutrients to the retina.
The present electron microscopic observations were similar to those obtained by histochemical examination of the glycogen
content in various species.0
Recently, the importance of a diffusion
pathway from the vitreous to the retina has
been emphasized by the demonstration10"18
of rapid diffusion of tracer particles from
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the vitreous, suggesting that nutrient materials in the vitreous are conveyed to all
layers of the retina.155 Thus, the retina would
be nourished by retinal vessels, choroid
and supraretinal vessels, or a combination
of these. The present comparative analysis
indicates that the difference in the retinal
vascularity among species appears to have
an effective influence on the distribution of
cell organelles in the Mullerian cell cytoplasm.
The possession of a cilium by Mullerian
cells may be due to the fact that they are
derived from ciliated neuroectoderm, and
the ciliary filament pattern in the distal portion may be vestigial. A ciliary structure in
the retina has also been found in ganglion,
bipolar, and pigment epithelial cells.19
Variation in arrangement of the Miiller
cell nuclei may depend on the distribution
of amacrine cells. In mammalian retinas
the nuclei of the Mullerian cells were generally located sclerad to, or between, amacrine cells. This location corresponds to
Zones 6-c or 6-d in Polyak's classification.20
In birds, reptiles, and anura, they were in
the middle of the inner nuclear layer (Zone
6-c). In these species, amacrine cells were
often piled up in the vitread half of the inner nuclear layer, forming a thick 6-d zone.
In the urodela and the fish, they were arranged in Zone 6-c or 6-d, as in mammalian
retinas. Those species with abundant amacrine cells in the inner nuclear layer may
have the complex type of receptive field organization.21' 22 There was also a variation
in the types of junctions forming the external limiting membrane. In many species
this consisted of a "zonula adhaerens."23' 2I
However, a few lower vertebrate retinas
distinctly possessed two types of junctions,
tight and intermediate, between neighboring Miiller cells. The external limiting
membrane comprising the two types of
junctions has been found in the mudpuppy
retina.22 In addition, Miiller cells of the
carp possessed typical desmosomes in this
region. The meaning of this variation is not
clear, but Dowling22 suggests that the tight
junctions might mediate electrical interactions between Mullerian cells.
448 Uga and Smelser
The network of dense filamentous material which is connected with the junctions
in the external limiting membrane of reptiles is a peculiar apparatus. It may serve
to mechanicallyfix,or support, the base of
the photoreceptor processes.
There were two variations in the villous
processes of the Miillerian cells. Broad
processes occurred together with the ordinary microvilli in the reptilian and bowfin
retina. Large amounts of glycogen particles
in them suggest that it serves as a site for
metabolite storage. Another case of unusual
processes was found in the Necturus retina
in which extremely short microvilli extended into the ventricle lumen. Here, arrangement of photoreceptor cells was
clearly less compact than in the other species so that the surface portion of the Miiller cells facing the ventricle lumen occupied
a large area among the photoreceptor cells.
Thus, the apical portion of the Miillerian
cells in this species may have been as large
as that of the other avascular retinae which
have tightly packed receptors.
Investigative Ophthalmology
June 1973
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