Mosaic properties of midget and parasol ganglion cells in the marmoset retina

2005 ◽  
Vol 22 (4) ◽  
pp. 395-404 ◽  
Author(s):  
BRETT A. SZMAJDA ◽  
ULRIKE GRÜNERT ◽  
PAUL R. MARTIN

We measured mosaic properties of midget and parasol ganglion cells in the retina of a New World monkey, the common marmosetCallithrix jacchus. We addressed the functional specialization of these populations for color and spatial vision, by comparing the mosaic of ganglion cells in dichromatic (“red–green color blind”) and trichromatic marmosets. Ganglion cells were labelled by photolytic amplification of retrograde marker (“photofilling”) following injections into the lateral geniculate nucleus, or by intracellular injection in anin vitroretinal preparation. The dendritic-field size, shape, and overlap of neighboring cells were measured. We show that in marmosets, both midget and parasol cells exhibit a radial bias, so that the long axis of the dendritic field points towards the fovea. The radial bias is similar for parasol cells and midget cells, despite the fact that midget cell dendritic fields are more elongated than are those of parasol cells. The dendritic fields of midget ganglion cells from the same (ON or OFF) response-type array show very little overlap, consistent with the low coverage of the midget mosaic in humans. No large differences in radial bias, or overlap, were seen on comparing retinae from dichromatic and trichromatic animals. These data suggest that radial bias in ganglion cell populations is a consistent feature of the primate retina. Furthermore, they suggest that the mosaic properties of the midget cell population are associated with high spatial resolution rather than being specifically associated with trichromatic color vision.

1992 ◽  
Vol 9 (3-4) ◽  
pp. 279-290 ◽  
Author(s):  
Dennis M. Dacey ◽  
Sarah Brace

AbstractIntracellular 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.


1996 ◽  
Vol 13 (6) ◽  
pp. 1011-1029 ◽  
Author(s):  
Elizabeth S. Yamada ◽  
Luiz Carlos L. Silveira ◽  
V. Hugh Perry

AbstractMale Cebus monkeys are all dichromats, but about two thirds of the females are trichromats. M and P retinal ganglion cells were studied in the male Cebus monkey to investigate the relationship of their morphology to retinal eccentricity. Retinal ganglion cells were retrogradely labeled after optic nerve deposits of biocytin to reveal their entire dendritic tree. Cebus M and P ganglion cell morphology revealed by biocytin retrograde filling is similar to that described for macaque and human M and P ganglion cells obtained by in vitro intracellular injection of HRP and neurobiotin. We measured 264 and 441 M and P ganglion cells, respectively. M ganglion cells have larger dendritic field and cell body size than P ganglion cells at any comparable temporal or nasal eccentricity. Dendritic trees of both M and P ganglion cells are smaller in the nasal than in the temporal region at eccentricities greater than 5 mm and 2 mm for M and P ganglion cells, respectively. The depth of terminal dendrites allows identification of both inner and outer subclasses of M and P ganglion cells. The difference in dendritic tree size between inner and outer cells is small or absent. Comparison between Cebus and Macaca shows that M and P ganglion cells have similar sizes in the central retinal region. The results support the view that M and P pathways are similarly organized in diurnal dichromat and trichromat primates.


1993 ◽  
Vol 10 (6) ◽  
pp. 1081-1098 ◽  
Author(s):  
Dennis M. Dacey

AbstractIn 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.


1996 ◽  
Vol 13 (2) ◽  
pp. 335-352 ◽  
Author(s):  
Heath D. Wilder ◽  
Ulrike Grünert ◽  
Barry B. Lee ◽  
Paul R. Martin

AbstractWe studied the anatomical substrates of spatial vision in a New World monkey, the marmoset Callithrix jacchus. This species has good visual acuity and a foveal specialization which is qualitatively similar to that of humans and other Old World primates.We measured the spatial density of retinal ganglion cells and photoreceptors, and calculated the relative numbers of these cell populations. We find that ganglion cells outnumber photoreceptors by between 2.4:1 and 4.2:1 in the fovea. The peak sampling density of ganglion cells is close to 550,000 cells/mm2. This value falls by almost 1000-fold between the fovea and peripheral retina; a value which approaches recent estimates of the centroperipheral ganglion cell gradient for human and macaque monkey retina and primary visual cortex. The marmoset shows a sex-linked polymorphism of color vision: all male and some female marmosets are dichromats. Six of the retinas used in the present study came from animals whose chromatic phenotype was identified in electrophysiological experiments and confirmed by polymerase chain reaction (PCR) amplification of cone opsin encoding genes. One animal was a trichromat and the others were dichromats. Antibodies against short wavelength-sensitive (SWS) cones labeled close to 8% of all cones near the fovea of onedichromat animal, consistent with electrophysiological evidence that the SWS system is present inall marmosets. The topography and spatial density of cone photoreceptors and ganglion cells was similar to that reported for macaque retina, and we found no obvious difference between dichromatic and trichromatic marmoset retinas. These results reinforce the view that the main determinate of primate foveal topography is the requirement for maximal spatial resolution.


2000 ◽  
Vol 17 (4) ◽  
pp. 567-578 ◽  
Author(s):  
BETH B. PETERSON ◽  
DENNIS M. DACEY

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.


2002 ◽  
Vol 19 (4) ◽  
pp. 453-465 ◽  
Author(s):  
BIN LIN ◽  
PAUL R. MARTIN ◽  
ULRIKE GRÜNERT

The response properties of postreceptoral sensory neurones are determined by the properties of their input neurones, by intrinsic membrane properties, and by the properties of neurotransmitter receptors on the soma and dendritic tree. We previously showed that inhibitory neurotransmitter (GABAA and glycine) receptors on a well-characterised sensory neurone, the parasol ganglion cell in the primate retina, are segregated towards the distal part of the dendritic tree. Here we studied the distribution of excitatory ionotropic glutamate receptor subunits on the dendrites of parasol cells in the retina of a New World monkey, the marmoset, Callithrix jacchus. Individual ganglion cells were intracellularly injected in an in vitro retinal wholemount preparation. Ionotropic glutamate receptor subunits, including AMPA (GluR1-4), kainate (GluR6/7), NMDA (NR1C2′) subunits, and the orphan receptors δ1 and δ2 were visualized with immunocytochemical methods. Immunoreactive puncta that colocalized with the dendrites of ganglion cells were analyzed using standard and/or confocal light microscopy. Colocalized puncta were present on parasol dendrites for all subunits studied, but their density was much lower (approximately 1/5) than previously reported for inhibitory (GABA and glycine) receptors. Segregation of the glutamate receptor clusters (GluR1, GluR6/7 subunits) to the peripheral dendrites was less marked than that shown for GABA and glycine receptor clusters. No sign of segregation of colocalized puncta to the peripheral part of the dendritic field was seen with antibodies to the GluR2, GluR2/3, GluR4, δ1/2, or NR1C2′ subunits. The results suggest that although there is diverse expression of glutamate receptor subtypes, the glutamatergic synapses form only a small proportion of the total synaptic input to primate ganglion cells. They further suggest that the processes which control distribution of excitatory and inhibitory synapses on the dendritic field of ganglion cells are, at least to some extent, independent.


1978 ◽  
Vol 203 (1152) ◽  
pp. 269-291 ◽  

Neurofibrillar methods stain a class of horizontal cells in the cat retina which are shown to be identical with the A-type horizontal cell of Golgistaining. Thus all of the A-type cells of a single retina can be observed. On this basis the changes in density and dendritic field size of A-type horizontal cells with respect to retinal eccentricity were measured. The decrease in density from centre to periphery is balanced by a corresponding increase in size of the dendritic field. Consequently each retinal pointindependent of retinal position — is covered by the dendritic fields of three or four A-type horizontal cells. The nuclei and nucleoli of B-type horizontal cells could also be recognized in neurofibrillar-stained material and thus their distribution was determined. The density ratio B-type: A-type is 2.8 + 0.4 and does not vary much from the centre to the periphery of the retina. Each retinal point is also covered by four B-type horizontal cells. Thus a single cone can contact a maximum of eight horizontal cells. The rate of density decrease from centre to periphery is closely similar in cones and horizontal cells but greater in ganglion cells.


2000 ◽  
Vol 17 (3) ◽  
pp. 437-448 ◽  
Author(s):  
JOSEPH MACRI ◽  
PAUL R. MARTIN ◽  
ULRIKE GRÜNERT

The inhibitory neurotransmitter gamma aminobutyric acid (GABA) has been shown to influence the responses of ganglion cells in the mammalian retina. Consistently, GABAA receptor subunits have been localized to different ganglion cell types. In this study, the distribution of the α1 subunit of the GABAA receptor on the dendrites of midget and parasol ganglion cells was investigated quantitatively in the retina of a New World monkey, the marmoset. Ganglion cells were injected with Neurobiotin in a live in vitro retinal whole-mount preparation. Retinal pieces were then processed with an antibody against the α1 subunit of the GABAA receptor. Strong punctate immunoreactivity indicative of synaptic localization is present in the ON and OFF sublamina of the inner plexiform layer. Many of the immunoreactive puncta coincide with the dendrites of both midget and parasol ganglion cells. Immunoreactive puncta are present on distal and proximal dendrites of ON and OFF cells of both ganglion cell types. On average, parasol cells show a slight increase in the spatial density of immunoreactive puncta with distance from the soma, whereas the density of immunoreactive puncta on midget cells stays even. Parasol ganglion cells show a slightly higher average density of immunoreactive puncta (0.083 puncta/μm dendrite) than midget cells (0.054 puncta/μm dendrite).


1984 ◽  
Vol 52 (6) ◽  
pp. 999-1013 ◽  
Author(s):  
Y. Fukuda ◽  
C. F. Hsiao ◽  
M. Watanabe ◽  
H. Ito

The action spike activities of single ganglion cells were recorded from the nasal retina of the intact eye of anesthetized and immobilized cats. Each ganglion cell was identified as a Y-, X-, or W-cell on the basis of its axonal conduction velocity, its receptive-field properties, and the level of maintained activity. Of about 100 ganglion cells physiologically identified and penetrated with horseradish peroxidase (HRP)-containing glass microelectrodes, 21 cells were subsequently identified in flat-mount preparations of the retinas and processed for detection of HRP. Of a total of nine Y-cells recovered, four had been penetrated at the soma and five at the axon. All had the morphology of the alpha-cell of Boycott and Wassle. Eight X-cells recovered. All had been penetrated at the soma and showed beta-cell morphology. Four W-cells were penetrated at the soma and recovered. Two off-tonic W-cells had small somas (15-16 micron in diam) and sparse dendritic fields, resembling gamma-cells of Boycott and Wassle. They are also similar to “G4” and “G18” of Kolb et al.'s classification. One on-tonic W-cell had somewhat larger soma (18 micron) with a relatively densely branched dendritic field. This corresponds to delta-cell of Boycott and Wassle or to “G15” of Kolb et al. One on-off phasic W-cell had a medium-sized soma (25.3 micron) with a fanlike dendritic expansion characteristic of the “unilateral horizontal broad range cell” of Shkolnik-Yarros or of “G22” of Kolb et al. Alternatively, all these W-cells can be called medium-sized gamma-cells. Among all three classes of ganglion cells, a positive correlation was found between the diameter of the receptive-field center and the dendritic field. Assuming that in the cat retina 1 degree of visual angle = 230 micron, dendritic fields of Y-cells seemed larger than their physiologically determined receptive-field centers. By contrast, the reverse relation was found between these two dimensions in X-cells. Axon diameters ranged from 4.0 to 5.6 micron (mean, 4.5 micron) in Y-cells and from 1.9 to 2.7 micron (mean, 2.2 micron) in X-cells. Three W-cells showed axon diameters of 0.6, 1.1, and 1.8 micron. The axon diameter distributions made from axons labeled by massive injections of HRP into the optic nerve fiber layer showed a pattern of distribution similar to that obtained from physiologically identified Y-, X-, and W-cell axons.


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