In primate retina, the midget, parasol, and small bistratified cell populations form the large majority of ganglion cells. In addition, there is a variety of low‐density wide‐field ganglion cell ...types that are less well characterized. Here we studied retinal ganglion cells in the common marmoset, Callithrix jacchus, using particle‐mediated gene transfer. Ganglion cells were transfected with an expression plasmid for the postsynaptic density 95–green fluorescent protein. The retinas were processed with established immunohistochemical markers for bipolar and/or amacrine cells to determine ganglion cell dendritic stratification. In total over 500 ganglion cells were classified based on their dendritic field size, morphology, and stratification in the inner plexiform layer. Over 17 types were distinguished, including midget, parasol, broad thorny, small bistratified, large bistratified, recursive bistratified, recursive monostratified, narrow thorny, smooth monostratified, large sparse, giant sparse (melanopsin) ganglion cells, and a group that may contain several as yet uncharacterized types. Assuming each characterized type forms a hexagonal mosaic, the midget and parasol cells account for over 80% of all ganglion cells in the central retina but only ∼50% of cells in the peripheral (>2 mm) retina. We conclude that the fovea is dominated by midget and parasol cells, but outside the fovea the ganglion cell diversity in marmoset is likely as great as that reported for nonprimate retinas. Taken together, the ganglion cell types in marmoset retina resemble those described previously in macaque retina with respect to morphology, stratification, and change in proportion across the retina.
Over 17 types of ganglion cell were distinguished in marmoset retina. The study shows that the fovea is dominated by midget and parasol cells, but outside the fovea wide‐field ganglion cell types make up a significant proportion of the total ganglion cell population. Scale bar = 100 μm.
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BFBNIB, FZAB, GIS, IJS, KILJ, NLZOH, NUK, OILJ, SAZU, SBCE, SBMB, UL, UM, UPUK
Directional responses in retinal ganglion cells are generated in large part by direction‐selective release of γ‐aminobutyric acid from starburst amacrine cells onto direction‐selective ganglion cells ...(DSGCs). The excitatory inputs to DSGCs are also widely reported to be direction‐selective, however, recent evidence suggests that glutamate release from bipolar cells is not directional, and directional excitation seen in patch‐clamp analyses may be an artifact resulting from incomplete voltage control. Here, we test this voltage‐clamp‐artifact hypothesis in recordings from 62 ON‐OFF DSGCs in the rabbit retina. The strength of the directional excitatory signal varies considerably across the sample of cells, but is not correlated with the strength of directional inhibition, as required for a voltage‐clamp artifact. These results implicate additional mechanisms in generating directional excitatory inputs to DSGCs.
Directional tuning of excitatory currents recorded in direction‐selective ganglion cells (DSGCs) is thought to be an artifact produced by the strong directional tuning of inhibitory inputs leading to directionally‐asymmetric voltage‐clamp errors. If this hypothesis is correct, then the strength of excitatory and inhibitory directional tuning should be positively correlated. The graph shows the results of experiments in a large sample of DSGCs that failed to detect the expected positive correlation.
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BFBNIB, FZAB, GIS, IJS, KILJ, NLZOH, NUK, OILJ, SAZU, SBCE, SBMB, UL, UM, UPUK
The ability to detect moving objects is an ethologically salient function. Direction-selective neurons have been identified in the retina, thalamus, and cortex of many species, but their homology has ...remained unclear. For instance, it is unknown whether direction-selective retinal ganglion cells (DSGCs) exist in primates and, if so, whether they are the equivalent to mouse and rabbit DSGCs. Here, we used a molecular/circuit approach in both sexes to address these issues. In mice, we identify the transcription factor Satb2 (special AT-rich sequence-binding protein 2) as a selective marker for three RGC types: On-Off DSGCs encoding motion in either the anterior or posterior direction, a newly identified type of Off-DSGC, and an Off-sustained RGC type. In rabbits, we find that expression of Satb2 is conserved in On-Off DSGCs; however, it has evolved to include On-Off DSGCs encoding upward and downward motion in addition to anterior and posterior motion. Next, we show that macaque RGCs express Satb2 most likely in a single type. We used rabies virus-based circuit-mapping tools to reveal the identity of macaque Satb2-RGCs and discovered that their dendritic arbors are relatively large and monostratified. Together, these data indicate Satb2-expressing On-Off DSGCs are likely not present in the primate retina. Moreover, if DSGCs are present in the primate retina, it is unlikely that they express Satb2.
The ability to detect object motion is a fundamental feature of almost all visual systems. Here, we identify a novel marker for retinal ganglion cells encoding directional motion that is evolutionarily conserved in mice and rabbits, but not in primates. We show in macaque monkeys that retinal ganglion cells (RGCs) that express this marker comprise a single type and are morphologically distinct from mouse and rabbit direction-selective RGCs. Our findings indicate that On-Off direction-selective retinal neurons may have evolutionarily diverged in primates and more generally provide novel insight into the identity and organization of primate parallel visual pathways.
Midget and parasol ganglion cells (GCs) represent the major output channels from the primate eye to the brain. On-type midget and parasol GCs exhibit a higher background spike rate and thus can ...respond more linearly to contrast changes than their Off-type counterparts. Here, we show that a calcium-permeable AMPA receptor (CP-AMPAR) antagonist blocks background spiking and sustained light-evoked firing in On-type GCs while preserving transient light responses. These effects are selective for On-GCs and are occluded by a gap-junction blocker suggesting involvement of AII amacrine cells (AII-ACs). Direct recordings from AII-ACs, cobalt uptake experiments, and analyses of transcriptomic data confirm that CP-AMPARs are expressed by primate AII-ACs. Overall, our data demonstrate that under some background light levels, CP-AMPARs at the rod bipolar to AII-AC synapse drive sustained signaling in On-type GCs and thus contribute to the more linear contrast signaling of the primate On- versus Off-pathway.
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•AII amacrine cells express calcium-permeable AMPA receptors (CP-AMPARs)•Blocking CP-AMPARs suppresses sustained, light-driven signals in On-ganglion cells•CP-AMPARs on AII-ACs may support the linear signaling specific to On-ganglion cells
Percival et al. describe how a night vision circuit contributes to functional asymmetries in signaling of the On- and Off-type midget and parasol ganglion cells, the major output neurons of the primate retina.
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GEOZS, IJS, IMTLJ, KILJ, KISLJ, NLZOH, NUK, OILJ, PNG, SAZU, SBCE, SBJE, UILJ, UL, UM, UPCLJ, UPUK, ZAGLJ, ZRSKP
Visual signals are segregated into parallel pathways at the first synapse in the retina between cones and bipolar cells. Within the OFF pathways of mammals, the selective expression of AMPA or ...kainate-type glutamate receptors in the dendrites of different OFF-bipolar cell types is thought to contribute to formation of distinct temporal channels. AMPA receptors, with rapid recovery from desensitization, are proposed to transmit high temporal frequency signals, whereas kainate receptors (KARs) are presumed to encode lower temporal frequencies. Here we studied the glutamate receptors expressed by OFF-bipolar cells in slice preparations of macaque monkey retina, where the low (midget/parvocellular) and high-frequency (parasol/magnocellular) temporal channels are well characterized. We found that all OFF-bipolar types receive input primarily through KARs and that KAR antagonists block light-evoked input to both OFF-midget and OFF-parasol ganglion cells. KAR subunits were differentially expressed in OFF-bipolar types; the diffuse bipolar (DB) cells, DB2 and DB3b, expressed GluK1 and showed transient responses to glutamate and the KAR agonist, ATPA. In contrast, flat midget bipolar, DB1, and DB3a cells lacked GluK1 and showed relatively sustained responses. Finally, we found that the KAR accessory protein, Neto1, is expressed at the base of cone pedicles but is not colocalized with the GluK1 subunit. In summary, the results indicate that transient signaling in the OFF pathway of macaques is not dependent on AMPA receptors and that heterogeneity of KARs and accessory proteins may contribute to the formation of parallel temporal channels.
The roles of the midget and parasol pathways as the anatomical foundation for high‐acuity vision at the fovea are well established. There is also evidence for the presence of other (non‐midget, ...non‐parasol) ganglion cell types in the foveal retina, but it is not established whether these cells receive input from cone photoreceptors in the central few degrees of the visual field, i.e. the region most important for conscious visual perception. To address this question, we targeted injections of retrograde tracer to the koniocellular layers in the posterior aspect of the lateral geniculate nucleus, where the central visual field is represented, in marmoset monkeys (Callithrix jacchus). Labeled ganglion cells were photofilled to reveal their dendritic morphology. Potential inputs to foveal koniocellular cells from diffuse bipolar cells were investigated in vertical sections through the fovea of marmoset and macaque (Macaca fascicularis) monkey retinas using immunohistochemistry. Forty koniocellular‐projecting ganglion cells were analysed. We used an established model of marmoset foveal topography to show that all these koniocellular‐projecting cells receive cone inputs from the central‐most 6°, with about half the cells receiving input from below 2° eccentricity, in the rod‐free central bouquet of cones at the foveola. In addition, all diffuse bipolar types investigated were present in the fovea at stratification depths similar to those of their counterparts in the peripheral retina. We conclude that the diverse visual representations established for koniocellular pathways in the peripheral retina are also a feature of the fovea, suggesting that koniocellular pathways contribute to foveal vision.
The fovea in the center of the retina, where the density of cone photoreceptors is maximal, is responsible for high‐acuity and color vision. This study shows that over ten parallel ganglion cell pathways are present in the fovea and thus contribute to visual function in the center of the visual field. The figure shows some of the retinal ganglion cell types found in the fovea of marmoset monkeys.
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BFBNIB, DOBA, FZAB, GIS, IJS, IZUM, KILJ, NLZOH, NUK, OILJ, PILJ, PNG, SAZU, SBCE, SBMB, SIK, UILJ, UKNU, UL, UM, UPUK
Three well characterized pathways in primate vision (midget-parvocellular, parasol-magnocellular, bistratified-koniocellular) have been traced from the first synapse in the retina, through the visual ...thalamus (lateral geniculate nucleus, LGN), to the visual cortex. Here we identify a pathway from the first synapse in the retina to koniocellular layer K1 in marmoset monkeys (Callithrix jacchus). Particle-mediated gene transfer of an expression plasmid for the postsynaptic density 95-green fluorescent protein (PSD95-GFP) was used to label excitatory synapses on retinal ganglion cells and combined with immunofluorescence to identify the presynaptic bipolar cells. We found that axon terminals of one type of diffuse bipolar cell (DB6) provide dominant synaptic input to the dendrites of narrow thorny ganglion cells. Retrograde tracer injections into the LGN and photofilling of retinal ganglion cells showed that narrow thorny cells were preferentially labeled when koniocellular layer K1 was targeted. Layer K1 contains cells with high sensitivity for rapid movement, and layer K1 sends projections to association visual areas as well as to primary visual cortex. We hypothesize that the DB6-narrow thorny-koniocellular pathway contributes to residual visual functions ("blindsight") that survive injury to primary visual cortex in adult or early life.
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