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In a recent study, visual signals were recorded for the first time in starburst amacrine cells of the macaque retina, and, as for mouse and rabbit, a directional bias observed in calcium signals was recorded from near the dendritic tips. Stimulus motion from the soma toward the tip generated a larger calcium signal than motion from the tip toward the soma. Two mechanisms affecting the spatiotemporal summation of excitatory postsynaptic currents have been proposed to contribute to directional signaling at the dendritic tips of starbursts: (1) a “morphological” mechanism in which electrotonic propagation of excitatory synaptic currents along a dendrite sums bipolar cell inputs at the dendritic tip preferentially for stimulus motion in the centrifugal direction; (2) a “space–time” mechanism that relies on differences in the time-courses of proximal and distal bipolar cell inputs to favor centrifugal stimulus motion. To explore the contributions of these two mechanisms in the primate, we developed a realistic computational model based on connectomic reconstruction of a macaque starburst cell and the distribution of its synaptic inputs from sustained and transient bipolar cell types. Our model suggests that both mechanisms can initiate direction selectivity in starburst dendrites, but their contributions differ depending on the spatiotemporal properties of the stimulus. Specifically, the morphological mechanism dominates when small visual objects are moving at high velocities, and the space–time mechanism contributes most for large visual objects moving at low velocities.
OBJECTIVES/SPECIFIC AIMS: Müller cells, radial glial cells of the retina, are the principal repository of xanthophyll pigment (lutein, zeaxanthin, meso-zeaxanthin), which are modifiable by diet and visible clinically by autofluorescence imaging. To understand the structural basis of xanthophyll visualization in vivo, we used 3-dimensional electron microscopic reconstruction of Müller cells surrounding one cone in a healthy human fovea. METHODS/STUDY POPULATION: From a 21-year-old male organ donor, dissected retinas were rejuvenated by oxygenated Ames medium then fixed in 4% glutaraldehyde. A tissue block 3.5 mm2 centered on the fovea was prepared for Automated Tape Ultramicrotomy (Kasthuri et al., Cell 162: 648–661, 2015). From 1462 serial 65 nm horizontal sections, an area ~250×250 μm was imaged at 6 nm xy resolution. Images were stitched and aligned. TrackEM software on a pen display was used to trace, reconstruct, and display cone #5 (of 186) and its contacting Müller cells. RESULTS/ANTICIPATED RESULTS: Cone 5 is ensheathed by 2 types of Müller cells, outer and inner (Dacey, ARVO, 2016). The outer cell is first seen at the external limiting membrane (ELM) between cones 5 and 17. Moving inward from the ELM, it tightly wraps around cone 5’s fiber in a C-shape profile for 78 µm. This Müller cell also intermittently projects to neighboring cones, 2 of which were close to cone 5 at the ELM. As cone 5’s axon approaches the pedicle, it contorts into a corkscrew. The outer cell fluidly molds to this changing shape. At this level, this Müller cell doubles in volume to encompass not only cone 5, but also cone 17 and another Müller cell. In the final 17 µm of the block the Müller cell’s volume quickly dissipates as it sends a small projection towards the internal limiting membrane, eventually encasing an OFF midget bipolar cell also associated with cone 5. In contrast to this outer cell, an inner Müller cell adjoining cone 5 spans only 19 µm, interacting directly with cone 5 and the outer cell for 3.9 µm. DISCUSSION/SIGNIFICANCE OF IMPACT: Neural-glial relationships in a human fovea are visible through 3-dimensional volume EM. The volume of Müller cells in the fovea was impressive, consistent with a pivotal role in the health of cone photoreceptors and xanthophyll homeostasis. It is possible that individual glia also ensheath the post-receptoral neurons in a cone-driven circuit, supporting the concept that xanthophylls contribute to neural efficiency in vision.
In the primate retina, parasol ganglion cells contribute to the primary visual pathway via the magnocellular division of the lateral geniculate nucleus, display ON and OFF concentric receptive field structure, nonlinear spatial summation, and high achromatic temporal–contrast sensitivity. Parasol cells may be homologous to the alpha-Y cells of nonprimate mammals where evidence suggests that N-methyl-D-aspartate (NMDA) receptor-mediated synaptic excitation as well as glycinergic disinhibition play critical roles in contrast sensitivity, acting asymmetrically in OFF- but not ON-pathways. Here, light-evoked synaptic currents were recorded in the macaque monkey retina in vitro to examine the circuitry underlying parasol cell receptive field properties. Synaptic excitation in both ON and OFF types was mediated by NMDA as well as α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA)/kainate glutamate receptors. The NMDA-mediated current–voltage relationship suggested high Mg2+ affinity such that at physiological potentials, NMDA receptors contributed ∼20% of the total excitatory conductance evoked by moderate stimulus contrasts and temporal frequencies. Postsynaptic inhibition in both ON and OFF cells was dominated by a large glycinergic “crossover” conductance, with a relatively small contribution from GABAergic feedforward inhibition. However, crossover inhibition was largely rectified, greatly diminished at low stimulus contrasts, and did not contribute, via disinhibition, to contrast sensitivity. In addition, attenuation of GABAergic and glycinergic synaptic inhibition left center–surround and Y-type receptive field structure and high temporal sensitivity fundamentally intact and clearly derived from modulation of excitatory bipolar cell output. Thus, the characteristic spatial and temporal–contrast sensitivity of the primate parasol cell arises presynaptically and is governed primarily by modulation of the large AMPA/kainate receptor-mediated excitatory conductance. Moreover, the negative feedback responsible for the receptive field surround must derive from a nonGABAergic mechanism.
Anatomical and physiological approaches are beginning to reveal the synaptic origins of parallel ON- and OFF-pathway retinal circuits for the transmission of short (S-) wavelength sensitive cone signals in the primate retina. Anatomical data suggest that synaptic output from S-cones is largely segregated; central elements of synaptic triads arise almost exclusively from the “blue-cone” bipolar cell, a presumed ON bipolar, whereas triad-associated contacts derive primarily from the “flat” midget bipolar cell, a hyperpolarizing, OFF bipolar. Similarly, horizontal cell connectivity is also segregated, with only the H2 cell-type receiving numerous contacts from S-cones. Negative feedback from long (L-) and middle (M-) wavelength sensitive cones via the H2 horizontal cells elicits an antagonistic surround in S-cones demonstrating that S versus L + M or “blue-yellow” opponency is first established in the S-cone. However, the S-cone output utilizes distinct synaptic mechanisms to create color opponency at the ganglion cell level. The blue-cone bipolar cell is presynaptic to the small bistratified, “blue-ON” ganglion cell. S versus L + M cone opponency arises postsynaptically by converging S-ON and LM-OFF excitatory bipolar inputs to the ganglion cell’s bistratified dendritic tree. The common L + M cone surrounds of the parallel S-ON and LM-OFF cone bipolar inputs appear to cancel resulting in “blue-yellow” antagonism without center-surround spatial opponency. By contrast, in midget ganglion cells, opponency arises by the differential weighting of cone inputs to the receptive field center versus surround. In the macula, the “private-line” connection from a midget ganglion cell to a single cone predicts that S versus L + M opponency is transmitted from the S-cone to the S-OFF midget bipolar and ganglion cell. Beyond the macula, OFF-midget ganglion cell dendritic trees enlarge and collect additional input from multiple L and M cones. Thus S-OFF opponency via the midget pathway would be expected to become more complex in the near retinal periphery as L and/or M and S cone inputs sum to the receptive field center. An important goal for further investigation will be to explore the hypothesis that distinct bistratified S-ON versus midget S-OFF retinal circuits are the substrates for human psychophysical detection mechanisms attributed to S-ON versus S-OFF perceptual channels.
Retinal ganglion cells (RGCs), the output neurons of the retina, have axons that project via the optic nerve to diverse targets in the brain. Typically, RGC axons do not branch before exiting the retina and thus do not provide it with synaptic feedback. Although a small subset of RGCs with intraretinal axon collaterals has been previously observed in human, monkey, cat, and turtle, their function remains unknown. A small, more recently identified population of RGCs expresses the photopigment melanopsin. These intrinsically photosensitive retinal ganglion cells (ipRGCs) transmit an irradiance-coding signal to visual nuclei in the brain, contributing both to image-forming vision and to several nonimage-forming functions, including circadian photoentrainment and the pupillary light reflex. In this study, using melanopsin immunolabeling in monkey and a genetic method to sparsely label the melanopsin cells in mouse, we show that a subgroup of ipRGCs have axons that branch en route to the optic disc, forming intraretinal axon collaterals that terminate in the inner plexiform layer of the retina. The previously described collateral-bearing population identified by intracellular dye injection is anatomically indistinguishable from the collateral-bearing melanopsin cells identified here, suggesting they are a subset of the melanopsin-expressing RGC type and may therefore share its functional properties. Identification of an anatomically distinct subpopulation in mouse, monkey, and human suggests this pathway may be conserved in these and other species (turtle and cat) with intraretinal axon collaterals. We speculate that ipRGC axon collaterals constitute a likely synaptic pathway for feedback of an irradiance signal to modulate retinal light responses.
Parallel processing of visual information begins at the first synapse in the retina between the photoreceptors and bipolar cells. Ten bipolar cell types have been previously described in the primate retina: one rod and nine cone bipolar types. In this paper, we describe an 11th type of bipolar cell identified in Golgi-stained macaque retinal whole mount and vertical section. Axonal stratification depth, in addition to dendritic and axonal morphology, distinguished the “giant” cell from all previously well-recognized bipolar cell types. The giant bipolar cell had a very large and sparsely branched dendritic tree and a relatively large axonal arbor that costratified with the DB4 bipolar cell near the center of the inner plexiform layer. The sparseness of the giant bipolar’s dendritic arbor indicates that, like the blue cone bipolar, it does not contact all the cones in its dendritic field. Giant cells contacting the same cones as midget bipolar cells, which are known to contact single long-wavelength (L) or medium-wavelength (M) cones, demonstrate that the giant cell does not exclusively contact short-wavelength (S) cones and, therefore, is not a variant of the previously described blue cone bipolar. This conclusion is further supported by measurement of the cone contact spacing for the giant bipolar. The giant cell contacts an average of about half the cones in its dendritic field (mean ± s.d. = 52 ± 17.6%; n = 6), with a range of 27–82%. The dendrites from single or neighboring giant cells that converge onto the same cones suggest that the giant cell may selectively target a subset of cones with a highly variable local density, such as the L or M cones.
Human, macaque monkey, and rat retinas were immunostained with a polyclonal antibody preparation against purified recoverin, a 23-kD calcium-binding protein isolated from bovine retina that localizes to rods and cones (Dizhoor et al., 1991). In addition to immunoreactive photoreceptors, we have identified subpopulations of recoverin-positive bipolar cells in all three species. Results from immunostaining with progressive dilutions of anti-recoverin and preadsorption of the antibody with a dilution series of purified recoverin showed that photoreceptors and bipolar cells had similar affinities for the antibody and suggested that the molecule recognized by the antibody in both cell types is recoverin. Immunoreactivity for recoverin and protein kinase C, a selective marker for all rod bipolar cells, was found in separate bipolar cell populations. Recoverin immunoreactivity is therefore a characteristic of certain cone bipolar cell types.
In rat retina, anti-recoverin labeled two morphologically distinct subpopulations of cone bipolar cells whose axonal arbors stratified at different depths in the inner plexiform layer (IPL). The bipolar cells labeled with anti-recoverin did not correspond to those that were reactive for calbindin, another cone bipolar cell marker.
Human and monkey retinas also had two populations of cone bipolar cells that were recoverin-positive. One population showed a distinct pattern of narrow bistratification at the outer border of the IPL and a regular mosaic arrangement of its axonal arbors, suggesting that the entire population of a single cone bipolar type was labeled. Cell density, dendritic morphology, and axonal-field size and stratification indicate that anti-recoverin selectively stains the flat midget (presumed OFF-center) cone bipolar cell type observed previously in Golgi preparations. By contrast the second bipolar cell population had axonal stratification in the inner half of the IPL and showed an unusual but consistent morphology and spatial distribution. Individual cells were intensely stained but were present at an extremely low density (~2−5 cells/mm2). These cells had multibranched dendritic trees characteristic of the diffuse bipolar cell class, but very small axonal fields in the size range of the midget bipolar class. Neither of the two recoverin-positive bipolar cell types in monkey was labeled with anti-calbindin or anti-cholecystokinin. An antibody preparation against bovine pineal hydroxyindole-O-methyltransferase (HIOMT) labeled photoreceptors and bipolar cells that closely resembled the recoverin-positive bipolar cells in human and rat retinas. Preadsorption of this antibody preparation with purified recoverin abolished immunostaining of the bipolar cells, suggesting that the anti-HIOMT preparation contains antibodies against recoverin, which is known to be present in the bovine pineal gland.
Intracellular injections of Neurobiotin were used to determine whether the major ganglion cell classes of the macaque monkey retina, the magnocellular-projecting parasol, and the parvocellular-projecting midget cells showed evidence of cellular coupling similar to that recently described for cat retinal ganglion cells. Ganglion cells were labeled with the fluorescent dye acridine orange in an in vitro, isolated retina preparation and were selectively targeted for intracellular injection under direct microscopic control. The macaque midget cells, like the beta cells of the cat's retina, showed no evidence of tracer coupling when injected with Neurobiotin. By contrast, Neurobiotin-filled parasol cells, like cat alpha cells, showed a distinct pattern of tracer coupling to each other (homotypic coupling) and to amacrine cells (heterotypic coupling).
In instances of homotypic coupling, the injected parasol cell was surrounded by a regular array of 3–6 neighboring parasol cells. The somata and proximal dendrites of these tracer-coupled cells were lightly labeled and appeared to costratify with the injected cell. Analysis of the nearest-neighbor distances for the parasol cell clusters showed that dendritic-field overlap remained constant as dendritic-field size increased from 100–400 μm in diameter.
At least two amacrine cell types showed tracer coupling to parasol cells. One amacrine type had a small soma and thin, sparsely branching dendrites that extended for 1–2 mm in the inner plexiform layer. A second amacrine type had a relatively large soma, thick main dendrites, and distinct, axon-like processes that extended for at least 2–3 mm in the inner plexiform layer. The main dendrites of the large amacrine cells were closely apposed to the dendrites of parasol cells and may be the site of Neurobiotin transfer between the two cell types. We suggest that the tracer coupling between neighboring parasol cells takes place indirectly via the dendrites of the large amacrine cells and provides a mechanism, absent in midget cells, for increasing parasol cell receptive-field size and luminance contrast sensitivity.
We characterized the light response, morphology, and receptive-field structure of a distinctive amacrine cell type (Dacey, 1989), termed here the Al amacrine, by applying intracellular recording and staining methods to the macaque monkey retina in vitro. A1 cells show two morphologically distinct components: a highly branched and spiny dendritic tree, and a more sparsely branched axon-like tree that arises from one or more hillock-like structures near the soma and extends for several millimeters beyond the dendritic tree. Intracellular injection of Neurobiotin reveals an extensive and complex pattern of tracer coupling to neighboring A1 amacrine cells, to two other amacrine cell types, and to a single ganglion cell type. The A1 amacrine is an ON-OFF cell, showing a large (10–20 mV) transient depolarization at both onset and offset of a photopic, luminance modulated stimulus. A burst of fast, large-amplitude (Σ60 mV) action potentials is associated with the depolarizations at both the ON and OFF phase of the response. No evidence was found for an inhibitory receptive-field surround. The spatial extent of the ON-OFF response was mapped by measuring the strength of the spike discharge and/or the amplitude of the depolarizing slow potential as a function of the position of a bar or spot of light within the receptive field. Receptive fields derived from the slow potential and associated spike discharge corresponded in size and shape. Thus, the amplitude of the slow potential above spike threshold was well encoded as spike frequency. The diameter of the receptive field determined from the spike discharge was Σ10% larger than the spiny dendritic field. The correspondence in size between the spiking receptive field and the spiny dendritic tree suggests that light driven signals are conducted to the soma from the dendritic tree but not from the axon-like arbor. The function of the axon-like component is unknown but we speculate that it serves a classical output function, transmitting spikes distally from initiation sites near the soma.
In in-vitro preparations of both macaque and human retina, intracellular injections of Neurobiotin and horseradish peroxidase were used to characterize the morphology, depth of stratification, and mosaic organization of a type of bistratified ganglion cell. This cell type, here called the small bistratified cell, has been shown to project to the parvocellular layers of the dorsal lateral geniculate nucleus (Rodieck, 1991) and is therefore likely to show color-opponent response properties.
In both human and macaque, the two dendritic tiers of the bistratified cell are narrowly stratified close to the inner and outer borders of the inner plexiform layer. The inner tier is larger in diameter and more densely branched than the outer tier and gives rise to distinct spine-like branchlets bearing large, often lobulated heads. By contrast the smaller, outer tier is sparsely branched and relatively spine-free.
In human retina, the small bistratified cells range in dendritic field diameter from ∼50 µm in central retina to ∼400 µm in the far periphery. The human small bistratified cells are about 20% larger in dendritic-field diameter than their counterparts in the macaque. However, when the difference in retinal magnification between human and macaque is taken into account, the small bistratified cells are similar in size in both species. In macaque, the small bistratified cell has a dendritic-field size that is ~10% larger than that of the magnocellular-projecting parasol ganglion cell. Human small bistratified ganglion cells tend to have smaller dendritic-field diameters than parasol cells. This is because parasol ganglion cells are larger in human than in macaque retina (Dacey & Petersen, 1992).
In macaque retina, intracellular injections of Neurobiotin revealed heterotypic tracer coupling to a distinct mosaic of amacrine cells and probable homotypic coupling to an array of neighboring ganglion cells around the perimeter of the injected cell's dendritic tree. The amacrine cell mosaic had a density of 1700 cells/mm2 in peripheral retina. Individual amacrines had small, densely branched and bistratified dendritic fields. From the homotypic coupling, it was possible to estimate for the small bistratified cell a coverage factor of ~1.8, and a density of ~1% of the total ganglion cells in central retina, increasing to ~6–10% in the retinal periphery.
The estimated density, dendritic-field size, and depth of stratification all suggest that the small bistratified ganglion cell type is the morphological counterpart of the common short-wavelength sensitive or ‘blue-ON’ physiological type.
The A1 cell is an axon-bearing amacrine cell of the primate retina with a diffusely stratified, moderately branched dendritic tree (∼400 μm diameter). Axons arise from proximal dendrites forming a second concentric, larger arborization (>4 mm diameter) of thin processes with bouton-like swellings along their length. A1 cells are ON-OFF transient cells that fire a brief high frequency burst of action potentials in response to light (Stafford & Dacey, 1997). It has been hypothesized that A1 cells receive local input to their dendrites, with action potentials propagating output via the axons across the retina, serving a global inhibitory function. To explore this hypothesis we recorded intracellularly from A1 cells in an in vitro macaque monkey retina preparation. A1 cells have an antagonistic center-surround receptive field structure for the ON and OFF components of the light response. Blocking the ON pathway with L-AP4 eliminated ON center responses but not OFF center responses or ON or OFF surround responses. Blocking GABAergic inhibition with picrotoxin increased response amplitudes without affecting receptive field structure. TTX abolished action potentials, with little effect on the sub-threshold light response or basic receptive field structure. We also used multi-photon laser scanning microscopy to record light-induced calcium transients in morphologically identified dendrites and axons of A1 cells. TTX completely abolished such calcium transients in the axons but not in the dendrites. Together these results support the current model of A1 function, whereby the dendritic tree receives synaptic input that determines the center-surround receptive field; and action potentials arise in the axons, which propagate away from the dendritic field across the retina.
To further characterize the H1 and H2 horizontal
cell populations in macaque monkey retinae, cells were
injected with the tracer Neurobiotin following intracellular
recordings. Tracer coupling between cells of the same type
revealed all H1 or H2 cells in small patches around the
injected cell. The mosaics of their cell bodies and the
tiling of the retina with their dendrites were analyzed.
Morphological differences between the H1 and H2 cells observable
in Neurobiotin-labeled patches made it possible to recognize
H1 and H2 cells in retinae immunolabeled for the calcium-binding
proteins parvalbumin and calbindin, and thus to study their
relative spatial densities across the retina. These data,
together with the intracellularly stained patches, show
that H1 cells outnumber H2 cells at all eccentricities.
There is, however, a change in the relative proportions
of H1 and H2 cells with eccentricity: close to the fovea
the ratio of H1 to H2 cells is ∼4 to 1, in midperipheral
retina ∼3 to 1, and in peripheral retina ∼2 to
1. In both the Neurobiotin-stained and the immunostained
retinae, about 3–5% of the H2 cells were obviously
misplaced into the ganglion cell layer. Several features
of the morphology of the misplaced H2 cells suggest that
they represent the so-called “biplexiform ganglion
cells” previously described in Golgi studies of primate
To study the detailed morphology of human retinal
ganglion cells, we used intracellular injection of horseradish
peroxidase and Neurobiotin to label over 1000 cells in
an in vitro, wholemount preparation of the human
retina. This study reports on the morphology of 119 wide-field
bistratified and 42 diffuse ganglion cells. Cells were
analyzed quantitatively on the basis of dendritic-field
size, soma size, and the extent of dendritic branching.
Bistratified cells were similar in dendritic-field diameter
(mean ± s.d. = 682 ± 130 μm)
and soma diameter (mean ± s.d. = 18 ±
3.3 μm) but showed a broad distribution in the extent
of dendritic branching (mean ± s.d. branch
point number = 67 ± 32; range = 15–167). Differences
in the extent of branching and in dendritic morphology
and the pattern of branching suggest that the human retina
may contain at least three types of wide-field bistratified
cells. Diffuse ganglion cells comprised a largely homogeneous
group whose dendrites ramified throughout the inner plexiform
layer. The diffuse cells had similar dendritic-field diameters
(mean ± s.d. = 486 ± 113 μm),
soma diameters (mean ± s.d. = 16 ±
2.3 μm), and branch points numbers (mean ± s.d.
= 92 ± 32). The majority had densely branched dendritic
trees and thin, very spiny dendrites with many short, fine,
twig-like thorny processes. Five of the diffuse cells had
much more sparsely branched dendritic trees (<50 branch
points) and less spiny dendrites, suggesting that there
are possibly two types of diffuse ganglion cells in human
retina. Although the presence of a diversity of large bistratified
and diffuse ganglion cells has been observed in a variety
of mammalian retinas, little is known about the number
of cell types, their physiological properties, or their
central projections. Some of the human wide-field bistratified
cells in the present study, however, show morphological
similarities to monkey large bistratified cells that are
known to project to the superior colliculus.
To determine the number of wide-field, monostratified
ganglion cell classes present in the human retina, we analyzed
a large sample of ganglion cells by intracellular staining
in an in vitro, whole-mount preparation of the
retina. Over 1000 cells were labeled by horseradish peroxidase
or Neurobiotin; some 200 cells had wide dendritic trees
narrowly or broadly stratified within either the inner
(ON) or outer (OFF) portion of the inner plexiform layer.
Based on dendritic-field size and the pattern and extent
of dendritic branching, we have distinguished six wide-field
cell groups. The giant very sparse ganglion cells included
both inner and outer stratifying cells and were unique
both for their extremely large dendritic field (mean diameter
= 1077 μm) and extremely sparsely branched dendrites.
Four of the cell groups had similarly large dendritic fields,
ranging in mean diameter from 737 to 791 μm, but differed
in the pattern and extent of dendritic branching, with
the number of dendritic branch points ranging from a mean
of 33 to 129. Of these four groups, the large very sparse
group and the large dense group included both inner and
outer stratifying cells, while the large sparse and large
moderate groups consisted of inner stratifying cells only.
The thorny monostratified ganglion cells were distinct
from the other cells in having medium size dendritic fields
(mean diameter = 517 μm) and moderately branched, inner
stratifying dendritic trees with many thin, spiny, twig-like
branchlets. All six groups had medium-size cell bodies,
with mean soma diameters ranging from 17 to 21 μm.
Though the physiological properties and central projections
of human wide-field, monostratified ganglion cells are
not known, some of the cells resemble macaque ganglion
cells known to project to the lateral geniculate nucleus,
the pretectum, or the superior colliculus.
Ganglion cells with intraretinal axon collaterals
have been described in monkey (Usai et al., 1991), cat
(Dacey, 1985), and turtle (Gardiner & Dacey, 1988)
retina. Using intracellular injection of horseradish peroxidase
and Neurobiotin in in vitro whole-mount preparations
of human retina, we filled over 1000 ganglion cells, 19
of which had intraretinal axon collaterals and wide-field,
spiny dendritic trees stratifying in the inner half of
the inner plexiform layer. The axons were smooth and thin
(∼2 μm) and gave off thin (<1 μm), bouton-studded
terminal collaterals that extended vertically to terminate
in the outer half of the inner plexiform layer. Terminal
collaterals were typically 3–300 μm in length,
though sometimes as long as 700 μm, and were present
in clusters, or as single branched or unbranched varicose
processes with round or somewhat flattened lobular terminal
boutons 1–2 μm in diameter. Some cells had a
single axon whereas other cells had a primary axon that
gave rise to 2–4 axon branches. Axons were located
either in the optic fiber layer or just beneath it in the
ganglion cell layer, or near the border of the ganglion
cell layer and the inner plexiform layer. This study shows
that in the human retina, intraretinal axon collaterals
are associated with a morphologically distinct ganglion
cell type. The synaptic connections and functional role
of these cells are not yet known. Since distinct ganglion
cell types with intraretinal axon collaterals have also
been found in monkey, cat, and turtle, this cell type may
be common to all vertebrate retinas.
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