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The Journal of Neuroscience, November 1, 1998, 18(21):8936-8946
The Major Cell Populations of the Mouse Retina
Chang-Jin
Jeon1, 4,
Enrica
Strettoi2, and
Richard
H.
Masland3, 4
1 Department of Biology, Kyungpook National University,
Taegu, Korea, 2 Istituto di Neurofisiologia del Consiglio
Nazionale delle Ricerche, Pisa, Italy, 3 Howard Hughes
Medical Institute, Massachusetts General Hospital, Boston,
Massachusetts 02114, and 4 Program in Neuroscience,
Harvard Medical School, Boston, Massachusetts 02115
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ABSTRACT |
We report a quantitative analysis of the major populations of cells
present in the retina of the C57 mouse. Rod and cone photoreceptors were counted using differential interference contrast microscopy in
retinal whole mounts. Horizontal, bipolar, amacrine, and Müller cells were identified in serial section electron micrographs assembled into serial montages. Ganglion cells and displaced amacrine cells were
counted by subtracting the number of axons in the optic nerve, learned
from electron microscopy, from the total neurons of the ganglion cell
layer. The results provide a base of reference for future work on
genetically altered animals and put into perspective certain recent
studies. Comparable data are now available for the retinas of the
rabbit and the monkey. With the exception of the monkey fovea, the
inner nuclear layers of the three species contain populations of cells
that are, overall, quite similar. This contradicts the previous belief
that the retinas of lower mammals are "amacrine-dominated", and
therefore more complex, than those of higher mammals.
Key words:
mouse; retina; anatomy; photoreceptor; horizontal; bipolar; amacrine; ganglion; population
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INTRODUCTION |
The mouse is the mainstay of
transgenic technology, which offers a new set of tools for the study of
integrated nervous system function. Unfortunately, the CNS of the mouse
has been less studied than that of larger laboratory mammals. As a
result, even basic information is sometimes missing. In the retina, the
subject of these studies, manipulation of developmental events can
change the cellular composition of the adult tissue (Bonfanti et al., 1996 ; Soucy et al., 1996) or alter its physiology (Chen et al., 1995;
Masu et al., 1995; Nirenberg and Meister, 1995; Xu et al., 1997). These
are powerful manipulations for understanding the functions of the cells
and circuits of the retina, but they are hard to evaluate if one
does not know the cellular makeup of the wild type.
One goal of the present study was to begin to remedy that lack. We
provide a quantitative description of the major cell populations of the
mouse retina using a systematic approach: in effect, we treated the
tissue as a three-dimensional solid and sought to classify every cell
within it. The aim was to create, in as definitive a way possible, a
base of reference to which later studies can be compared. The
importance of the resulting information for interpreting genetic
manipulations of the retina will be illustrated.
Our second goal was to clarify an issue about the comparative structure
of mammalian visual systems. There has long been a belief that the
retinas of primates are somehow simpler than those of lower mammals, so
that sophisticated processing performed peripherally in lower mammals
is deferred to the cortex in monkeys (Dubin, 1970; Dowling, 1987). In
terms of retinal structure, this belief translates into the idea that
primate retinas contain a large fraction of bipolar cells, simply
transmitting information from the photoreceptor cells, whereas
subprimate mammals have a large fraction of amacrine cells, which
create subtle encodings of the visual stimulus. However, recent
evidence is that many of the identifiable types of bipolar and amacrine
cells are widely conserved among mammals (for review, see Wässle
and Boycott, 1991; McNeil and Masland, 1998). The present results allow
a direct comparison of the fractions of bipolar and amacrine cells in
mice, rabbits, and monkeys.
Rods and cones are easily counted by using established methodologies
(Carter-Dawson and LaVail, 1979; Curcio et al., 1987; Wikler et al.,
1996). To identify the cells of the inner nuclear and ganglion cell
layers, however, is not a trivial problem. Gross cytological features
are unreliable, and there are few molecular probes that reliably label
single classes of cells. For that reason, we distinguished the cells
from their fundamental definitions by visualizing their axons or
dendrites. For the closely packed cells of the mouse inner nuclear
layer, this could only be done by using electron microscopy. A second
difficulty occurs because the ganglion cell layer contains both
ganglion cells and displaced amacrine cells. Although large ganglion
cells can be distinguished by cytology, displaced amacrine cells and
small ganglion cells overlap in size, and this prevents reliable
counting. We therefore counted ganglion cells by identifying their
axons in the optic nerve.
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MATERIALS AND METHODS |
Adult mice (C57/BL6) were used for these experiments. Mice for
counting of photoreceptors, choline acetyltransferase (ChAT) cells, and
cells of the inner nuclear layer by confocal microscopy were from an
American colony (Charles River Laboratories, Boston, MA). Mice used for
electron microscopy of inner nuclear layer and optic nerve, as well as
mice for total ganglion cell layer counting were from an Italian colony
(Harlan Nossan, Milan, Italy). Animals were anesthetized with a mixture
of ketamine hydrochloride (30-40 mg/kg) and xylazine (3-6 mg/kg).
Proparacaine HCl (100-200 µl) was applied to the cornea to suppress
blink reflexes. Eyes were quickly enucleated after a reference point
was taken to label the superior pole and immersed in fixative; the
animals were euthanized by an overdose of the same anesthetics in
accordance with institutional guidelines.
Photoreceptor staining. Cone photoreceptors were
labeled in retinal whole mounts. Immediately after enucleation, the
eyes were immersed in 4% paraformaldehyde in 0.1 M
phosphate buffer, pH 7.4. The retinas were isolated from the eyecup and
post-fixed for 1-2 hr in 2.5% glutaraldehyde in 0.1 M
phosphate buffer. After being rinsed in buffer, the retinas were
incubated in 50 µg/ml peroxidase-labeled peanut lectin (Sigma, St.
Louis, MO) in 0.25 M Tris buffer, for 16-18 hr (Blanks and
Johnson, 1984). Labeled cells were visualized using a diaminobenzidine
reagent kit in 0.25 M Tris buffer (Kirkegaard & Perry,
Gaithersburg, MD). Retinas were then rinsed, mounted flat on glass
slides, and coverslipped with DMSO. After 12 hr, DMSO was replaced with
100% glycerol. Labeled cones as well as unlabeled rods could be
examined and photographed on a Zeiss Axioplan microscope using high
power differential interference contrast (DIC) optics (Curcio et al.,
1987). Photographs were taken at 300 µm intervals along the central
vertical meridian and printed at a final magnification of 1400×. Cones
were counted in 70 × 70 µm fields (30-80 cells per field).
Rods were counted in 40 × 40 µm fields (470-800 cells per
field). This allowed an estimate of the total number of cells of each
class counted in each retina. Counting along the vertical meridian
samples both the blue cone rich (ventral) and blue cone poor (dorsal)
regions of the retina (Szel et al., 1992), and this might be expected to have consequences for the inner retina (i.e., the blue cone bipolar
might be missing where there are no blue cones). However, blue cones
are rare, and no large difference was detected in the other populations
of retinal cells.
Confocal microscopy. For nuclear staining of the total
population of cells, retinas were immersed for 2-4 hr in 4 µM ethidium homodimer (Molecular Probes, Eugene, OR) and
0.1 M phosphate buffer, pH 7.4. Confocal microscopy was
used to count the total number of cells in the inner nuclear and
ganglion cell layers. The analysis of these cells was performed for the
same retinas used to count photoreceptors (n = 3),
again along the vertical meridian, at 300 µm intervals for ganglion
cell layer cells and 600 µm for inner nuclear layer cells. Serial
optical sections were taken every 1 µm along the z-axis
with a Bio-Rad (Hercules, CA) MRC 500 confocal microscope, using the
TRITC combination of filters. Every ethidium homodimer-stained
nucleus in the inner nuclear and ganglion cell layer was identified in
through-focus prints. Nuclei of endothelial cells of blood vessels in
the ganglion cell layer were not counted, nor were the small, dense,
nuclei of glial cells. Counts were done in 70 × 70 µm fields
that contained 360-580 inner nuclear layer cells and 27-50 ganglion
cell layer cells, respectively.
ChAT immunocytochemistry. Freshly dissected retinas
(n = 3) were fixed in 4% paraformaldehyde in 0.1 M phosphate buffer, pH 7.4, and processed for whole-mount
immunocytochemistry against ChAT, using polyclonal antibody
Ab143 from Chemicon (Temecula, CA) diluted 1:200, followed by 1:200
biotinylated horse anti-goat IgG and 1:50 FITC-conjugated avidin
DCS (Vector Laboratories, Burlingame, CA). Retinas were mounted
flat on glass slides and coverslipped with Vectashield (Vector
Laboratories), a glycerol-based antifading medium. Retinas were
examined on a Zeiss Axioplan fluorescence microscope; cholinergic cells
in the inner nuclear and ganglion cell layer were photographed at 300 µm intervals along the central vertical meridian. Counts were done on
micrographs in 200 × 200 µm fields (25-40 cells per
field).
Electron microscopy. Mice (n = 2) were
perfused transcardially with 2% paraformaldehyde and 2.5%
glutaraldehyde in 0.1 M phosphate buffer. The eyes were
enucleated and the eyecups post-fixed overnight in the same fixative.
Six or seven 1 × 2 mm retinal strips were dissected from the
central vertical meridian with a sharp blade and processed separately.
They were osmicated, stained en bloc with 1% uranyl acetate,
dehydrated in ethanol, and embedded flat in Epon Araldite. Series of
124 and 115 vertical sections, 90-nm-thick, were obtained from one
central (close to the optic nerve head) and one peripheral block,
respectively, using a Leica (Nussloch, Germany) Reichert Ultracut
ultramicrotome equipped with a diamond knife. Consecutive ribbons of
15-20 serial sections were cut, and four or five sections were
collected together on single-hole, Formvar-coated grids. Sections were
stained with uranyl acetate and lead citrate, and examined with a Jeol
JEM-100 CX II electron microscope. Every fourth or fifth section was
photographed at a magnification of 2800×. Five or six adjacent
pictures were taken across the inner nuclear layer. Pictures were
printed at a final magnification of 7300×, assembled in montages, and
pasted on cardboard. The inner nuclear layer areas in each montage were
2025 and 1830 µm2 for central and peripheral
retinas, respectively.
Details of identifying cell types in the serial photomicrographs have
been described elsewhere (Strettoi and Masland, 1995, 1996). Every cell
present in the serial photomicrographs was identified as bipolar,
amacrine, horizontal, or Müller cell from processes emerging from
the cell bodies. Partially sectioned cells were included only if they
had a clear nucleolus. We counted a total of 258 cells from the central
and 330 cells from the peripheral retina. As a cross-check of the
serial section analysis, estimates of the ratios of the various cell
types in the inner nuclear layer were obtained for both central and
peripheral retina applying the dissector method (Sterio, 1984;
Gundersen, 1986) in two groups of sections located 4 µm apart.
The two methods gave very close estimates.
Electron microscopy of the optic nerve and total ganglion cell
layer counts. Because a large variation in the number of axons in
the optic nerve has been reported for different strains of mice
(Williams et al., 1996), we estimated such number for optic nerves of
C57BL/6J, adult mice of one of our colonies (the Italian colony
originating from Nossan), according to the methods described in Cenni
et al. (1996). Briefly, mice (n = 4) were anesthetized and perfused transcardially with a mixture of 2% paraformaldheyde and
2.5% gluteraldehyde in cacodylate buffer. Optic nerves were carefully
dissected and fixed in 4% gluteraldehyde, post-fixed in 2% osmium
tetroxide, stained en bloc with 1% uranyl acetate, dehydrated in
ethanol, and embedded in Epon Araldite. Ultrathin sections,
~90-nm-thick, were cut perpendicularly to the long axis of the nerves
on a Leica Ultratome V ultramicrotome, and collected on 200 mesh copper
grids. Nerve sections were obtained at a distance (~300 µm) from
the posterior pole of the eye, where most of the fibers are myelinated.
Sections were counterstained with uranyl acetate and lead citrate and
viewed with a Jeol 1200 EXII electron microscope.
Micrographs of the optic nerve were taken at a nominal magnification of
6000×, using the supporting grid as a sampling matrix. A total of
30-40 pictures were taken for each nerve, covering the entire surface
of the nerve. A carbon replica grating was photographed at the same
magnification and used to print the images at a total magnification of
12,000×. Axons, identified by the presence of a myelin sheath in 95%
of the cases, were counted in fields 14 × 20 µm; a total number
of 5500-6000 fibers were counted for each nerve; this included
both myelinated and unmyelinated fibers. The total number of fibers in
the optic nerve was obtained by multiplying the ratio of counted fibers
to sampled area by the total area of the nerve. The latter was measured
from low power EM negatives of ultrathin sections collected on single
hole grids and digitized in an image analysis system together with the
image of a calibrating grid photographed at the same nominal magnification.
To learn the fraction of ganglion cells in the ganglion cell layer, we
counted the total number of cells of this layer in the retinas of four
additional mice, matched in age and weight to the ones used for optic
nerve counting. These mice were perfused with 4% paraformaldehyde, and
the retinas were carefully dissected, rinsed, and stained with ethidium
homodimer as above. Retinas were coverslipped with Vectashield and
viewed with a Leica TCS NT confocal microscope. Serial optical
sections of the ganglion cell layer were taken at 300-400 µm
intervals along both the nasotemporal and dorsoventral meridians and
counted in fields 250 × 250 µm (120-300 cells per field).
For each retina, the total number of cells was obtained by multiplying
the sampled density by the total retinal area measured in camera lucida
drawings of the retinal profiles. Perfusion, as compared with immersion
fixation, allowed RNA retention and caused cytoplasmic as well as
nuclear staining of retinal cells with ethidium. This helped in
discriminating between neuronal and glial or endothelial elements in
the ganglion cell layer. For one retina, both the total number of cells
in the ganglion cell layer and the total number of axons in the optic
nerve could be determined. The relative fractions of ganglion cells and
displaced amacrine cells were determined by subtracting the number of
optic nerve axons from the total neurons of the ganglion cell layer. The statistical errors of the fractions shown are the propagated errors, including the SEs of each measurement (Altman, 1991; Bevington and Robinson, 1992).
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RESULTS |
We began with three retinas prepared as whole mounts after
aldehyde fixation and mounted in aqueous media. We first mapped the
distribution of rods and cones, using DIC optics. The retinas were then
optically sectioned horizontally for counting the total nuclei of the
inner nuclear and ganglion cell layers. In additional series of
retinas, the fractions of cells of specific types within the inner
nuclear and ganglion cell layers were learned by electron microscopy.
Rods and cones
The mosaic of rods and cones in the mouse retina is shown in
Figure 1. The distribution of cones, at
300 µm intervals dorsal and ventral to the optic nerve, is shown for
three retinas in Table 1 and Figure 7:
the average cone density is 12,400 cells/mm2, with a
gradient of <2 from the point of highest density, located 600 µm
from the optic nerve head, to the far periphery. The curve in the
dorsal retina is approximately symmetric to that of the ventral retina.
Values for the ventral half of the retina are in close agreement with
those reported recently by Wikler et al. (1996) for short-wavelength
cones. The total number of cones estimated from our samples is
~180,000. The density of rod photoreceptors has a slightly flatter
distribution than that of cones (density gradient, ~1.4). Their
average density is about 437,000 cells/mm2, giving a
total number of rods of ~6.4 million per retina. Thus, on average,
rods are 97.2%, and cones are 2.8% of all the photoreceptors. This is
in accord with the estimate of Carter-Dawson and LaVail (1979).
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Figure 1.
The mosaic of rods and cones in the mouse retina.
DIC optics, focal plane through the photoreceptor inner segments. The
lighter, more or less polygonal, structures are rod inner segments. The
inner segments of cones are outlined darkly by the diaminobenzidine
reaction product. Scale bar, 10 µm.
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Total cells of the inner nuclear and ganglion cell layers
In the same three retinas used for photoreceptor counting, the
total number of cells in the inner nuclear and ganglion cell layers was
also estimated at each eccentricity (Fig.
2). Both are shown in Table 1. The cells
of the inner nuclear layer have a distribution slightly more peaked
than that of the photoreceptors; those of the ganglion cell layer are
more peaked still. All three distributions, though, are flatter than
those found in rats, rabbits, cats, or monkeys (Hughes, 1977;
Mitrofanis et al., 1988; Martin and Grunert, 1992; Strettoi and
Masland, 1995).
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Figure 2.
Serial confocal sections at 1 µm
z intervals through the inner nuclear layer. All nuclei
of the layer were labeled with ethidium homodimer. The cells were
counted by following individual cells through the series, as
illustrated for the numbered examples. Scale bar, 10 µm.
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The average density of neurons in the ganglion cell layer was
~8200 cells/mm2. Of these, ~41%, or 3300 cells/mm2, are indeed ganglion cells (see below).
This gives an average ratio of cones to ganglion cells of slightly less
than four.
Horizontal, bipolar, Müller, and amacrine cells
The high density of cells in the inner nuclear layer of the mouse,
combined with their small size, made it necessary to use electron
microscopy of serial sections to distinguish among the various cell
types (Fig. 3). Cells were identified on
the basis of the morphology and distribution of processes leaving from
their somata. Cytological and positional features also helped in the identification. For instance, Müller cells display dark,
elongated nuclei, which form an almost continuous layer separating the
sclerally located bipolar and horizontal cells from amacrine cell
somata, mostly positioned at the vitreal side of the inner nuclear
layer.
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Figure 3.
Low-power electron microscopy of the inner nuclear
layer. Series of montages (part of one is shown) were assembled for
locations in the central and peripheral retinas. Within each series of
montages, every cell of the inner nuclear layer was identified. This
was done by visualizing the axons or dendrites of the cells as they
left the soma; examples are indicated by arrowheads.
Scale bar, 5 µm.
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Table 2 gives the numbers and relative
fractions of various cell types in the inner nuclear layer. Bipolars
make up ~41% of all the cells in the layer, amacrines 39%,
Müller cells 16%, and horizontal cells 3%. The size of the
sample that one can examine with the electron microscope is obviously
limited; this causes a considerable uncertainty in the estimate of
fractions of horizontal cells, which are rarely encountered within the
series of sections. The estimate for bipolars and amacrines is more
accurate.
As a cross-check, selected sections of the series were used to assess
the same numbers and fractions by means of a widely used statistical
sampling strategy, the dissector method (Gundersen, 1986). We found
that a distance of 4 µm between the first and last section was
suitable for applying the dissector method to the mouse inner nuclear
layer. The results were close to those obtained by serial section
analysis (Table 2). Although this was a useful exercise, note that
using the dissector does not eliminate the need for an independent
method of learning the identity of the partially sectioned cells.
Ganglion cells and displaced amacrine cells
We counted cells in the ganglion cell layer by staining another
series of retinal whole mounts with ethidium homodimer and examining
the preparations with a confocal microscope. All cells encountered in
the samples were counted, with the exceptions of endothelial cells,
clearly identified by their elongated shape and close association with
blood vessels, and astrocytes, which have very small cell bodies with
dense nuclei and are slightly displaced toward the optic fiber layer.
Because we needed to determine the absolute number of ganglion cell
layer neurons in the whole retina, we collected data from both the
dorsoventral and the nasotemporal central meridians.
The distributions of total GCL neurons are shown in Figure
4. The dorsoventral curves are not
strictly symmetric to their nasotemporal counterparts. Because cells in
the far periphery of the nasal retina have higher densities than for
other peripheral regions, the center-to-periphery gradient for the
nasal retina is lower than elsewhere. The total number of retinal cells
in the layer was determined by multiplying the average density of cells
in each retina by the total area of the retina. (A similar result was
obtained by multiplying the measured local densities by the total area
of the retina.)
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Figure 4.
Neurons of the ganglion cell layer. The top
panel (A) shows a confocal image of the
ganglion cell layer, as seen after staining with ethidium. Under these
conditions both DNA and RNA are stained, so that extranuclear cytoplasm
is revealed (arrows). The nuclei of glia and endothelial
cells (arrowhead) were not counted. The two graphs
(B, C) show the numbers of cells
encountered along two axes (dorsoventral and nasotemporal) intersecting
the optic nerve head. Counts are from the Italian colony of C57/BL6
mice.
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The total number of ganglion cells was learned by counting their axons
in the optic nerve, at a distance (~300 µm) from the posterior pole
of the eye in which most of them are myelinated and can be
unequivocally identified at the electron microscope level (Fig.
5). On average, 44,860 ± 3125 fibers were estimated (Table 3). Only 5%
of them were clearly unmyelinated. For retinas with 110,242 ± 5826 neurons in the ganglion cell layer, 65,385 ± 6385 displaced
amacrine cells thus exist, 59 ± 4% of the total.
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Figure 5.
Electron micrograph from transverse
ultrathin section of the mouse optic nerve. Both large- and small-size
axons are visible in this field, and all of them are myelinated. This
magnification is approximately the same used for counting fibers.
Nu, Nucleus of a glial cell. Scale bar, 1 µm.
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ChAT (starburst) amacrine cells
As in other mammalian species, antibodies directed against choline
acetyltransferase label two populations of virtually identical amacrine
cells, whose cell bodies are located in the inner nuclear layer and
ganglion cell layer, respectively, and whose dendrites form two narrow
stratified bands within the inner plexiform layer. Confocal microscopy
of the dendritic plexi labeled by anti-ChAT reveals the typical
structure of starburst cell processes, with arbors that overlap to form
a lattice pattern (Fig. 6).
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Figure 6.
The distribution of ChAT-positive (starburst)
cells across three mouse retinas. In the top micrograph
(A) the ChAT-positive neurons are, labeled here
with Cy3, shown in red. They form two populations, one
in the inner nuclear layer and one in the ganglion cell layer. Their
dendrites are stratified narrowly in two bands. The middle
micrograph (B) shows a collapsed
whole-mount view. The ChAT cells of the inner nuclear layer are
red, and those of the ganglion cell layer are
green. The bottom micrograph
(C) shows the mosaic of stained dendrites within
the inner plexiform layer.
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The numerical distribution of the two population of cells is quite
symmetrical, with the cells in the inner nuclear layer reaching
slightly higher densities at all eccentricities (on average, 1100 cells/mm2 for inner nuclear layer cells vs 945 of
the cells in the ganglion cell layer). The center-to-periphery gradient
along the dorsoventral axis is two for the inner nuclear layer cells
and slightly lower for the cells located in the ganglion cell
layer.
The number of ChAT-positive cells can be compared with the total number
of cells in the inner nuclear layer and ganglion cell layer learned by
means of confocal microscopy (Table 1). ChAT cells with the cell bodies
in the inner nuclear layer are ~1% of all the cells in that layer.
Since, in turn, 39% of all the inner nuclear layer cells are
represented by amacrines, ChAT cells with the cell bodies in the inner
nuclear layer are ~3% of all amacrine cells. ChAT cells in the
ganglion cell layer are 11.5% of all the cells in the layer, or 19.5%
of all the displaced amacrines. The total population of ChAT cells
(inner nuclear layer plus ganglion cell layer) represents 5.2% of the
total number of amacrine cells in the mouse retina.
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DISCUSSION |
The distributions of each major cell type in the mouse retina are
summarized in Figure 7. We find the mouse
retina to be strongly rod-dominated: rods outnumber cones by roughly
35:1. Somewhat surprisingly, the average cone density in the mouse
retina is the same found in the primate's retina at 3-4 mm
eccentricity (Packer et al., 1989). However, at the same eccentricity
the density of rod photoreceptors in primates is only 100,000 cells/mm2. Thus, the major difference between the
photoreceptor mosaics of monkeys and mice is the higher density of
(very small) rods in the latter.
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Figure 7.
Comparative distributions of the major cell
classes in the retina of the mouse. All data are from the American
colony of C57/BL6 mice.
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In accord with the small overall size of the mouse eye, the cells of
the inner nuclear layer are also small. Their average total density was
100,541 cells/mm2, more than twice that in the
rabbit (Strettoi and Masland, 1995). We find them distributed at 3.1%
horizontal cells, 41% bipolars, 16% Müller cells, and 39%
amacrine cells (Table 2). These fractions have previously been
estimated from cytological features (Young, 1985). The corresponding
values were 0.1, 48, 12 and 39%. The results are in fairly good
agreement, with the exception that Young identified more bipolar and
fewer Müller cells than we found. In our electron micrographs
there is little ambiguity in distinguishing the two. It is likely that
Young mistook some Müller cells for bipolars. This would be easy
to do when the judgment is made purely from light microscopic cytology,
because both cells can have vertically elongated somata and because the
descending process of a Müller cell, which in the mouse is
unusually thin, can resemble an axon of a bipolar cell.
The number of ganglion cells was very close to a previous computation
done with similar methods in the same colony of animals, but almost
20% lower than that given in a careful study by Williams et al.
(1996). The major difference between our counting strategy and theirs
is that we use a larger field to count fibers: we count a larger number
of fibers in a lower number of nerves. It is not obvious that technical
differences would produce a discrepancy in the results. Two other
factors could contribute to the difference: variation in tissue
processing and individual variability between the American and the
Italian colonies of mice. Tissue shrinkage, however, which is the major
variable affected by processing, would not account for a difference in
the total number of cells per retina. The more likely is that the
Italian colony has a lower number of ganglion cells. There is precedent
for such a difference: Williams et al. (1996) demonstrated a 21%
difference in the numbers of ganglion cells between two Jackson
Laboratory (Bar Harbor, ME) colonies of C57BL/6J mice. Note that the
absolute densities of cells in the ganglion cell layer of retinas used
for optic nerve counting were consistently lower than for the whole
mounts in which we counted photoreceptors and inner nuclear layer
cells; the total number of cells in the ganglion cell layer was lower in Italian than American mice (110,000 vs 124,000).
It is worth noting that the number of retinal ganglion cells is quite
variable in normal cats, monkeys, and humans (Illing and Wässle,
1981; Curcio and Allen, 1990; Spear et al., 1996). Ganglion cell number
appears especially susceptible to small genetic or even environmental
differences.
Fortunately, the difference in mice is only 11% and affects the
absolute density but not the relative fraction of ganglion cells in the
ganglion cell layer. That estimate was 41 ± 4%, obtained from
animals of the same colony. In one case, the total number of cells in
the ganglion cell layer and of fibers in the optic nerve was calculated
for the same retina (this cannot be done routinely, because differing
fixatives need to be used for whole mounts or electron microscopy). For
that retina, the fraction of ganglion cells in the ganglion cell layer
was 43%. If one takes the number of optic nerve fibers from Williams
et al. (1996) (54,600) and the total number of ganglion cells from our
American mice, the value is 44%. This is close to what we find, and
within the limits of the error of any of these measurements.
A base of reference for future work
The absolute densities of the cells were quite reproducible from
animal to animal for our series of identically prepared specimens (Table 1). When tissue preparation differs (in fixative, histochemical protocol, or coverslipping method) the variation will be greater because of variable shrinkage and/or distortion of the tissue. The
absolute density may also vary with the age of the animal, because the
mouse's eye grows throughout early adult life without the addition of
neurons. However, the relative fractions of cells are not subject to
such influences. The retina is built of interlocking microcircuits
whose individual elements must be present in the same ratios in order
for the system to function properly. Previous work and the present
studies agree that the fractions of horizontal, bipolar, Müller,
and amacrine cells are remarkably constant from specimen to specimen
and animal to animal (Strettoi and Masland, 1995).
For that reason, the results of the present studies can be used as a
base of reference for future work. If mouse retinas are prepared as
whole mounts in aqueous medium after light aldehyde fixation, the
numbers of cells can be compared directly without gross error. If not,
new data can be referred back to the present ones by using proportions.
For example, the numerical importance of a newly stained type of
bipolar cell can be learned if one establishes that cell's fraction of
the total cell population of the inner nuclear layer. From those data
and the present ones the fraction of all bipolar cells occupied by the
newly stained one can be directly calculated.
As a practical matter, we have provided the relative density of the
ChAT-containing amacrines, a readily stained population for which good
antibodies are available. These can be used as a reference population.
For example, at location V7 (2.1 mm ventral to the optic nerve), the
ChAT-positive cells had a density of 800 cells/mm2.
Using the information presented in Tables 1 and 2, one may calculate
that this represents 2.4% of all amacrine cells or 2.1% of all
bipolar cells present at that eccentricity. Thus, if a new cell and the
ChAT cells are stained in the same preparation, the fraction of all
inner nuclear layer cells or all bipolar or all amacrine cells occupied
by the new cell can be approximated. This avoids the necessity of
counting the total cells of the inner nuclear layer. Because small
fractions are involved, however, the results are accurate only to a
first approximation; for more precision the density of a new cell
should be referred to counts of the total cells of the inner nuclear
layer.
Perspectives on normal and genetically altered mice
Knowledge of the cell populations of the retina will be important
as genetic techniques are used to alter retinal structures, because
changing one element in the retinal network can have secondary effects
on others. Cone deletion (Soucy et al., 1996) and ganglion cell
overexpression (Bonfanti et al., 1996) are current examples. Even when
no structures have been changed, however, the information is useful.
Several examples, among many possible, follow.
Starburst amacrine cells in our whole mounts had a peak density in the
inner nuclear layer of ~1400 cells/mm2. In the
rabbit, however, their peak density is 800/mm2. Does
this suggest that the starburst cells have different functions in mice
and rabbits? The present results show that starburst cells in mice
represent 3% of all amacrine cells at that eccentricity, exactly the
same fraction (3%) found in the rabbit (Strettoi and Masland, 1996). A
postulated role of the dopaminergic amacrine cells is also
strengthened. The present results allow the calculation that they
represent only 0.08% of all amacrine cells, as would be expected for a
cell widely believed to serve a neuromodulatory function (Masland et
al., 1993; Gustincich et al., 1997).
Quantitative information is also important in interpreting
developmental manipulations. In a now classic study, Turner et al.
(1990) labeled retinal progenitor cells by retroviral injection. At the
animal's maturity, the retroviral marker was found to be present in
all of the classes of retinal neuron. However, the distribution of
labeled cells did not match the normal adult distribution shown here.
For retinas labeled at embryonic day 13 (E13), the proportions of
labeled cells in the inner nuclear layer were: horizontal cells 0.7%,
bipolar cells 70%, Müller cells 6%, and amacrine cells 23%. In
effect, there were far too many labeled bipolar cells and too few
Müller and amacrine cells (Table 2). The sample of cells studied
by Turner et al. was large enough to exclude chance variation as the
cause. The mismatch does not affect their fundamental conclusion: that
all cell classes can derive from E13 progenitors. One possibility would
be that, contrary to the original belief (Turner et al., 1990), some
Müller and amacrine cells have already become committed at E13.
Another would be unequal expression or detection of the retrovirally
inserted marker among the cell classes.
Are the retinas of lower mammals more complex than those
of primates?
For many years the belief has existed that the retinas of lower
animals are complex, carrying out sophisticated analyses of the visual
input, whereas those of primates are simple, with more complex analyses
deferred to their highly developed visual cortices. This may well be
true for frogs and birds, which have remarkably complex retinas (Dubin,
1970; Dowling, 1987). Anatomy suggests, and electrophysiological
experiments directly confirm, that frog retinas contain very
sophisticated inner retinal mechanisms (Maturana et al., 1960). Among
mammals, however, this is less clear. The types of bipolar and amacrine
cells found thus far in rats, rabbits, cats, and monkeys are remarkably
similar. This extends even to cells as anatomically distinctive as the
starburst and AII amacrines (for review, see Wässle and Boycott,
1991).
If many individual elements are the same, how about the overall
populations of bipolar and amacrine cells? Figure
8 shows that these, too, are quite
similar in the mouse, rabbit, and monkey. The monkey has more
horizontal cells, and slightly fewer amacrine cells, but in no sense
are monkey retinas "bipolar-dominated". To be sure, the monkey
fovea may be an exception; the comparison shown in Figure 8 is for a
point 5 mm away from the fovea, chosen because the densities of cones
was near that found in the mouse and rabbit. However, the fovea
occupies <1% of the area of the monkey's retina. Over most of its
area, the cell populations in the monkey retina are similar to those of
a mouse or rabbit.
View larger version (26K):
[in this window]
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|
Figure 8.
The distribution of classes of cells in the mouse,
rabbit, and monkey. Data for the mouse average the central and
peripheral retinas. Data for the rabbit are from Strettoi and Masland
(1995). Data for the monkey are from Martin and Grünert
(1992).
|
|
Interestingly, the density of cones in the mouse retina is in the same
order of magnitude as the density of cones in the monkey at 3-4 mm
from the fovea (Table 1; Wikler and Rakic, 1990). It could be that
cones, which appeared first during evolution (Okano et al., 1992;
Goldsmith, 1994), dictated the major rules of retinal organization.
Possibly a certain density of cones, common to monkeys and mice, brings
with it populations of connected retinal neurons that remain in
constant numerical proportions. After all, the only retinal cells
exclusive to the rod pathway are rod bipolars. Since outside the fovea
the density of cones is similar in monkeys and mice, cone bipolars are
expected to be in close proportions in the two species, as well as the
numerous types of cone-driven amacrine cells.
| |
FOOTNOTES |
Received May 26, 1998; revised Aug. 6, 1998; accepted Aug. 10, 1998.
This work was supported by Korea-USA cooperative science program grant
975-0500-001-2 from The Korea Science and Engineering Foundation
and an Italy-USA grant from the Consiglio Nazionale delle
Ricerche of Italy. We are grateful to Dr. Ann Yee for helping with the
electron microscopic analysis, Rebecca Rockhill for helping with
confocal microscopy, and Alberto Bertini for printing micrographs. R.H.M. is a Research to Prevent Blindness Senior Investigator.
Correspondence should be addressed to Dr. Richard Masland, Wellman 429, Massachusetts General Hospital, Boston, MA 02114.
| |
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V. Resta, E. Novelli, F. Di Virgilio, and L. Galli-Resta
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D. R. Lazzell, R. Belizaire, P. Thakur, D. M. Sherry, and R. Janz
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U. E. A. Pesch, J. E. Fries, S. Bette, H. Kalbacher, B. Wissinger, C. Alexander, and K. Kohler
OPA1, the Disease Gene for Autosomal Dominant Optic Atrophy, Is Specifically Expressed in Ganglion Cells and Intrinsic Neurons of the Retina
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S. Xu, Y. Wang, H. Zhao, L. Zhang, W. Xiong, K.-W. Yau, H. Hiel, E. Glowatzki, D. K. Ryugo, and D. Valle
PHR1, a PH Domain-Containing Protein Expressed in Primary Sensory Neurons
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R. H. Farkas, J. Qian, J. L. Goldberg, H. A. Quigley, and D. J. Zack
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J. S. Stahl
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M. Ettaiche, N. Guy, P. Hofman, M. Lazdunski, and R. Waldmann
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L. Yang, D. Bula, J. G. Arroyo, and D. F. Chen
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M. Akimoto, E. Filippova, P. J. Gage, X. Zhu, C. M. Craft, and A. Swaroop
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M. S. Grubb and I. D. Thompson
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C. Rossi, E. Strettoi, and L. Galli-Resta
The Spatial Order of Horizontal Cells Is Not Affected by Massive Alterations in the Organization of Other Retinal Cells
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S. M. Carcieri, A. L. Jacobs, and S. Nirenberg
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J.-J. Pang, F. Gao, and S. M. Wu
Light-Evoked Excitatory and Inhibitory Synaptic Inputs to ON and OFF {alpha} Ganglion Cells in the Mouse Retina
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X. Zhu, B. Brown, A. Li, A. J. Mears, A. Swaroop, and C. M. Craft
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T. Inoue, M. Hojo, Y. Bessho, Y. Tano, J. E. Lee, and R. Kageyama
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G. S. Yang, M. Schmidt, Z. Yan, J. D. Lindbloom, T. C. Harding, B. A. Donahue, J. F. Engelhardt, R. Kotin, and B. L. Davidson
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S. L. Znoiko, R. K. Crouch, G. Moiseyev, and J.-x. Ma
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G. H. Jacobs, J. A. Fenwick, and G. A. Williams
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N. Francis and E. S. Deneris
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Y. Tsukamoto, K. Morigiwa, M. Ueda, and P. Sterling
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M. Guldenagel, J. Ammermuller, A. Feigenspan, B. Teubner, J. Degen, G. Sohl, K. Willecke, and R. Weiler
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N. L. Brown, S. Patel, J. Brzezinski, and T. Glaser
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Top
Abstract
Introduction
