Synaptic inputs to broad thorny ganglion cells in macaque retina

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. These are the identified wide‐field and medium‐field amacrine cells that made synapses onto a broad thorny ganglion cell (purple) in central macaque retina. The wide field amacrine cells included three wiry amacrine cells (green), a semilunar cell (aqua), and a stellate wavy cell (yellow). The medium‐field cells included a starburst amacrine cell (red) and a spiny amacrine cell (orange). These amacrine cell inputs are expected to mediate the responses of the broad thorny ganglion cells to stimuli outside their classical receptive fields.