Spherical Code of Retinal Orientation-Selectivity Enables Decoding in Ensembled and Retinotopic Operation

Selectivity to orientations of edges is seen at the earliest stages of visual processing, in retinal orientation-selective ganglion cells (OSGCs), thought to prefer vertical or horizontal orientation. However, as stationary edges are projected on the hemispherical retina as lines of longitude or latitude, how edge orientation is encoded, and decoded by the brain, is unknown. Here, by mapping the OS of thousands of OSGCs at known retinal locations in mice, we identified three OSGC types whose preferences match two longitudinal fields, and a fourth type matching two latitudinal fields, the members of each field-pair being non-orthogonal. A geometric decoder revealed that two OS sensors yield optimal orientation decoding when approaching the deviation from orthogonality we observed for OSGC field-pairs. Retinotopically-organized decoding generated type-specific variation in decoding efficiency across the visual field. OS tuning was greater in the dorsal retina, possibly reflecting an evolutionary adaptation to an environmental gradient of edges.