Direction and orientation preferences in mouse superior colliculus and its retinal inputs align with topographic axes atop locally mixed tuning

Abstract

In mouse superior colliculus (SC), neurons are robustly tuned to motion direction and orientation, but it remains controversial whether these preferences are spatially organized, and how this organization relates to that found in the retinal input to the SC. We addressed these questions by combining two-photon calcium imaging of retinal boutons and SC neurons in superficial SC with Neuropixels recordings across the full depth of SC. We then asked how direction and orientation preferences depend on visual-field location and how tuning similarity among units depends on lateral and vertical distance in the SC. Retinal boutons were strongly tuned, and their preferences closely matched the retinal topographic organization of four motion directions and orientations previously described in the retina, rather than a global map in which a single direction or orientation dominates each visual-field location. With increasing depth, SC neurons progressively deviated from this organization. Superimposed on the identified topography, local clustering of tuning preferences in retinal boutons and SC neurons was weak and confined to very small spatial scales. Together, these results show that retinal inputs and neurons in mouse SC represent multiple directions and orientations for each location in the visual field, likely supporting flexible readout for diverse visually guided behaviors.