Topographic axonal projection at single-cell precision supports local retinotopy in the mouse superior colliculus

Abstract

Retinotopy, like all long-range projections, can arise from the axons themselves or their targets, but the underlying connectivity pattern remains unknown at the fine scale. To address this question, we functionally mapped the spatial organization of the input axons and target neurons in the mouse retinocollicular pathway at single-cell resolution using in vivo two-photon calcium imaging. We found a near-perfect retinotopic tiling of retinal ganglion cell axon terminals, with an average error below 30 μm or 2 degrees of visual angle. The precision of retinotopy was relatively lower for local neurons in the superior colliculus. Subsequent data-driven modelling ascribed it to a low input convergence, on average 5.5 retinal ganglion cell inputs to a postsynaptic cell in the superior colliculus. These results indicate that retinotopy arises largely from topographically precise input from presynaptic cells, rather than elaborating local circuitry to reconstruct the topography by postsynaptic cells.