Direction and orientation preferences in mouse superior colliculus and its retinal inputs exhibit a topography of cardinal biases atop locally mixed tuning

In mouse superior colliculus (SC), neurons are robustly tuned to motion direction and orientation, but it remains controversial whether these preferences form global maps or are arranged in a salt-and-pepper fashion, 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 depend on lateral and vertical distance in the SC. Retinal boutons were strongly tuned and their preferences closely matched the retinal topographic organization of cardinal motion directions and orientations previously described for direction- and orientation-selective ganglion cells, showing that SC receives a highly ordered, retinocentric code for motion and edges. With increasing depth, SC neurons progressively deviated from this organization. On top of this cardinal topography, local clustering of tuning preferences in retinal boutons and SC neurons was weak and confined to very small spatial scales. We did not detect robust global maps of direction or orientation. Together, these results show that mouse SC inherits a topographic organization of cardinal directions and orientations from the retina, progressively diverts from this orderly organization with increasing distance from the retinal input, and exhibits broad coverage of directions and orientations at each visual location, likely supporting flexible readout for diverse visually guided behaviors.