Abstract:Parasol cells are one of the major types of primate retinal ganglion cells. The goal of this study was to describe the synaptic inputs that shape the light responses of the ON type of parasol cells, which are excited by increments in light intensity. A connectome from central macaque retina was generated by serial blockface scanning electron microscopy. Six neighboring ON parasol cells were reconstructed, and their synaptic inputs were analyzed. On average, they received 21% of their input from bipolar cells, … Show more
“…Although the synaptic inputs and outputs of the amacrine cells presynaptic to broad thorny cell 103 were not analyzed completely, it was apparent that they also made synaptic contacts with one another and with parasol cells identified previously (Patterson, Bordt, et al, 2020). Wiry Type 2 cell 182 made nine synapses onto four ON parasol cells and one onto another wiry amacrine cell, 4315.…”
In primates, broad thorny retinal ganglion cells are highly sensitive to small, moving stimuli. They have tortuous, fine dendrites with many short, spine-like branches that occupy three contiguous strata in the middle of the inner plexiform layer. The neural circuits that generate their responses to moving stimuli are not well-understood, and that was the goal of this study. A connectome from central macaque retina was generated by serial block-face scanning electron microscopy, a broad thorny cell was reconstructed, and its synaptic inputs were analyzed. It received fewer than 2% of its inputs from both ON and OFF types of bipolar cells; the vast majority of its inputs were from amacrine cells. The presynaptic amacrine cells were reconstructed, and seven types were identified based on their characteristic morphology. Two types of narrow-field cells, knotty bistratified Type 1 and wavy multistratified Type 2, were identified. Two types of medium-field amacrine cells, ON starburst and spiny, were also presynaptic to the broad thorny cell. Three types of wide-field amacrine cells, wiry Type 2, stellate wavy, and semilunar Type 2, also made synapses onto the broad thorny cell. Physiological experiments using a macaque retinal preparation in vitro confirmed that broad thorny cells received robust excitatory input from both the ON and the OFF pathways. Given the paucity of bipolar cell inputs, it is likely that amacrine cells provided much of the excitatory input, in addition to inhibitory input.
“…Although the synaptic inputs and outputs of the amacrine cells presynaptic to broad thorny cell 103 were not analyzed completely, it was apparent that they also made synaptic contacts with one another and with parasol cells identified previously (Patterson, Bordt, et al, 2020). Wiry Type 2 cell 182 made nine synapses onto four ON parasol cells and one onto another wiry amacrine cell, 4315.…”
In primates, broad thorny retinal ganglion cells are highly sensitive to small, moving stimuli. They have tortuous, fine dendrites with many short, spine-like branches that occupy three contiguous strata in the middle of the inner plexiform layer. The neural circuits that generate their responses to moving stimuli are not well-understood, and that was the goal of this study. A connectome from central macaque retina was generated by serial block-face scanning electron microscopy, a broad thorny cell was reconstructed, and its synaptic inputs were analyzed. It received fewer than 2% of its inputs from both ON and OFF types of bipolar cells; the vast majority of its inputs were from amacrine cells. The presynaptic amacrine cells were reconstructed, and seven types were identified based on their characteristic morphology. Two types of narrow-field cells, knotty bistratified Type 1 and wavy multistratified Type 2, were identified. Two types of medium-field amacrine cells, ON starburst and spiny, were also presynaptic to the broad thorny cell. Three types of wide-field amacrine cells, wiry Type 2, stellate wavy, and semilunar Type 2, also made synapses onto the broad thorny cell. Physiological experiments using a macaque retinal preparation in vitro confirmed that broad thorny cells received robust excitatory input from both the ON and the OFF pathways. Given the paucity of bipolar cell inputs, it is likely that amacrine cells provided much of the excitatory input, in addition to inhibitory input.
“…Data analysis and 3D rendering were performed using SBFSEM-tools, an open-source MATLAB (Mathworks) program developed in the Neitz lab (https://github.com/neitzlab/sbfsem-tools) [17,49]. Final figures were compiled in Adobe Illustrator.…”
Section: Data Analysis and Visualizationmentioning
Highlights d 3D reconstruction of the S-cone connectome revealed S-cone selective amacrine cells d S-cone amacrine cells receive excitatory input from only S-cone ON bipolar cells d S-cone amacrine cells make targeted inhibitory synapses onto ipRGCs d Resulting short-wavelength sensitivity is distinct from that mediated by melanopsin
“…For proximal dendrites, criteria included thin dendritic diameters, sparse radial branching, an absence of synaptic output sites and bipolar cell input, often at the end of short dendritic spine-like branches. Dendritic diameter and branching frequency in particular distinguished SACs from other S4 amacrine cells, such as the semilunar and wiry amacrine cells 56 . These morphological features reported previously and confirmed in our full SAC reconstructions served as a guide for confirming isolated branches as SACs 3,22,30,31 .…”
Section: Serial Electron Microscopymentioning
confidence: 92%
“…Stratification depth within in the inner plexiform layer (IPL) was calculated as previously described 56 . Briefly, markers were placed throughout the volume at the borders between the INL-IPL and IPL-GCL.…”
The detection of motion direction is a fundamental visual function and a classic model for neural computation. In the non-primate mammalian retina, direction selectivity arises in starburst amacrine cell (SAC) dendrites, which provide selective inhibition to ON and ON-OFF direction selective retinal ganglion cells (dsRGCs). While SACs are present in primates, their connectivity is unknown and the existence of primate dsRGCs remains an open question. Here we present a connectomic reconstruction of the primate ON SAC circuit from a serial electron microscopy volume of macaque central retina. We show that the structural basis for the SAC's ability to compute and confer directional selectivity on post-synaptic RGCs is conserved in primates and that SACs selectively target a single ganglion cell type, a candidate homolog to the mammalian ON-sustained dsRGCs that project to the accessory optic system and contribute to gaze-stabilizing reflexes. These results indicate that the capacity to compute motion direction is present in the retina, far earlier in the primate visual system than classically thought, and they shed light on the distinguishing features of primate motion processing by revealing the extent to which ancestral motion circuits are conserved.
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