Single-cell precision of axonal projection from the retina to the superior colliculus in mice

Retinotopy is generally preserved across the visual system, but its cellular-level organization remains elusive. How precisely is topographic information transmitted from the retina? To address this question, here we combined experimental and computational modelling approaches. First, using two-photon calcium imaging of retinal ganglion cell (RGC) axons as well as local neurons in the superior colliculus (SC), we performed functional mapping of the retinocollicular projection at a single-cell resolution in awake mice. The tiling patterns of RGC axon terminals and their corresponding receptive fields (RFs) turned out to be nearly identical, and showed a significantly better agreement than the tiling patterns of SC somata and their RFs. This indicates a higher precision of retinotopy for RGC axons than for SC neurons. To better quantify the organization of the retinocollicular pathway, we next performed a computational modelling analysis based on the experimental data. By comparing the observed and simulated retinotopy patterns, we identified that 1) a jitter of RGC projection to a target location in SC is as small as 27 µm; and 2) individual SC neurons integrate inputs from around 5.5 RGCs on average, leading to a relatively less precise retinotopy on the postsynaptic side. These results highlight the precision of wiring in the brain even for a long-range projection such as the retinocollicular pathway, and suggest that retinotopy arises largely from topographically precise projection of presynaptic cells, rather than elaborating local circuitry to reconstruct the topography by postsynaptic cells.