Horizontal cell nonlinearities create asymmetric texture processing in ON and OFF primate retinal outputs

The receptive fields of retinal neurons are the foundation for all downstream computations in the visual system, shaping our understanding of information processing across the visual hierarchy. Here, we provide an updated view of how receptive field surrounds of major primate retinal output pathways contribute to texture processing. We show that spatial structure in the receptive field surround enhances responses of ON parasol and ON midget retinal ganglion cells, but suppresses responses of their OFF counterparts. This leads to distinct roles in spatial encoding, with ON pathways acting as spatial integrators for texture and OFF pathways functioning as differentiators. Surprisingly, this asymmetry originates from nonlinear spatial integration in horizontal cells-neurons traditionally thought to integrate inputs linearly. Instead, we show that spatial structure in natural images robustly engages horizontal cells, which differentially modulate ON and OFF bipolar cells and, in turn, ON and OFF retinal ganglion cells. This updated view of the spatial sensitivity of key retinal output pathways raises questions about what information is available to downstream cortical circuits and how it is used to guide visual behavior.