Using sensory information to trigger different behaviors relies on circuits that pass through brain regions. The rules by which parallel inputs are routed to downstream targets are poorly understood. The superior colliculus mediates a set of innate behaviors, receiving input from >30 retinal ganglion cell types and projecting to behaviorally important targets including the pulvinar and parabigeminal nucleus. Combining transsynaptic circuit tracing with in vivo and ex vivo electrophysiological recordings, we observed a projection-specific logic where each collicular output pathway sampled a distinct set of retinal inputs. Neurons projecting to the pulvinar or the parabigeminal nucleus showed strongly biased sampling from four cell types each, while six others innervated both pathways. The visual response properties of retinal ganglion cells correlated well with those of their disynaptic targets. These findings open the possibility that projection-specific sampling of retinal inputs forms a basis for the selective triggering of behaviors by the superior colliculus.

Summary 10The superior colliculus is an important node in the visual system that receives inputs from the retina and 11 distributes these visual features to various downstream brain nuclei. It remains unknown how these 12 circuits are wired to enable specific and reliable information processing. Here the retinal ganglion cells at 13 the beginning of two such circuits, one targeting the pulvinar and the other the parabigeminal nucleus, 14were labeled using mono-synaptically restricted rabies tracing. Instead of a fuzzy distribution of the 15 retinal outputs, we delineate clear preferences in how information is routed to these two targets. Three 16 retinal ganglion cell types selectively innervated circuits projecting to the pulvinar, six are preferentially 17 routed to the parabigeminal nucleus, and three innervate both circuits. This work argues that neural 18 circuits of the superior colliculus are based on a dedicated set of connections between specific retinal 19 ganglion cell types and different targets of the superior colliculus.