Polyaxonal A1 amacrine cells form a spatially extended network in primate retina

Inhibitory networks shape information processing in the brain by integrating signals across space, regulating neuronal responses, and controlling the flow of signals through neural circuits. Understanding these computations requires linking the structure of individual inhibitory neuron types to their functional properties and network connectivity. The retina provides a tractable system for meeting this challenge, yet the organization of many retinal inhibitory circuits remains poorly understood. Here, we identify a population of polyaxonal amacrine cells recorded using multielectrode arrays as A1 amacrine cells, a morphologically defined interneuron type in primate retina. This identification is supported by a correspondence between properties of morphologically-identified A1 cells from single cell recordings and putative A1 amacrines in the array recordings. We then identified recursive bistratified ganglion cells in the array recordings based on their electrical coupling to A1 cells, linking this inhibitory network to retinal output pathways. A1 and recursive bistratified cells also share an asymmetry in receptive-field organization, with larger On than Off centers. Finally, A1 spike amplitudes decline during bursts, and analyses of their electrical images suggest that this change may cause some spikes to fail to propagate through their extensive axonal arbors. These findings establish the cellular identity and network organization of a long-range inhibitory circuit in the primate retina and reveal how neuronal architecture, connectivity, and spike dynamics may jointly shape the transmission of visual information.