Abstract

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.

Highlights

  • The nervous system is built from a large set of diverse neuronal cell types that work together to process information and generate behavior (Zeng and Sanes, 2017)

  • Transsynaptic tracing of retinal ganglion cells from targets of the superior colliculus To determine if visual features are selectively sampled by the two targeted output pathways of the mouse superior colliculus, we used rabies-based viral tools to label retinal ganglion cells innervating either the colliculo-parabigeminal or colliculo-pulvinar circuit

  • We injected the parabigeminal nucleus (Figure 1A67 C) or lateral pulvinar (Figure S1A-C) with herpes-simplex virus (HSV) expressing rabies-G, TVA and 68 mCherry, and subsequently injected EnvA-coated rabies virus coding for GCaMP6s (EnvA-SADΔG69 GCaMP6s) into the superficial layers of the superior colliculus

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Summary

Introduction

The nervous system is built from a large set of diverse neuronal cell types that work together to process information and generate behavior (Zeng and Sanes, 2017). The superficial gray and the optic layer form the most dorsal layers of the superior colliculus and are primarily innervated by the retina (May, 2006) These visual layers consist of several groups of neurons with diverse morphology, visual response properties and long-range targets that include the lateral pulvinar, lateral geniculate nucleus and parabigeminal nucleus. The different ganglion cell types that provide input to specific superior collicular output pathways have not been characterized. Using quantitative analysis of the retinal ganglion cell morphology and comparison of the visual response properties in the retina and target nuclei, we found strong specificity in the routing of visual information through the superior colliculus

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