A projection specific logic to sampling visual inputs in mouse superior colliculus

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.

Context-dependent modulation of natural approach behaviour in mice

“…In the zebrafish, defined RGC types with specific stimulus selectivity have indeed been shown to underlie prey approach [40], while conditional, visual stimulus feature-driven decisions to approach or avoid and their conditional modulation are computed and encoded in the optic tectum [6,9], homologous to the superior colliculus. In the mouse, almost ninety per cent of RGCs project to the superior colliculus [41], which contains cells with response properties similar to those found in the retina [42][43][44] and is known to mediate visual attention [2,45] and orienting in ethological contexts in rodents [46][47][48][49]. In particular, the topographically mapped circuitry of the superficial superior colliculus that connects information from specific regions in the visual field to ipsilateral versus contralateral motor outputs that drive spatial orienting behaviour, is ideally organized to mediate the behaviours quantified here [50][51][52].…”

Control of Orienting Movements and Locomotion by Projection-Defined Subsets of Brainstem V2a Neurons

“…A large part of our study relies on projection-based manipulations of neuronal subtypes. While retrogradely transported HSV and AAVretro vectors have already proven to be extremely powerful tools [45,[47][48][49], notably owing to their restricted entry at terminals [45,54,55], there are potential concerns that deserve clarification. First, if wild HSVs can prevent a single cell from being infected by multiple viruses [56], the replication-deficient ones used here are deprived of viral genome [44] and allow multiple infections [46] (Figure S4).…”

“…For the rest of the study, we focused on the head rotation, body orientation, and control of the hindlimbs since these actions are piloted by spinal circuits and may therefore be under a common control by branched RS neurons. We first combined a Cre-dependent retrogradely transported herpes-simplex virus (HSV) [44,45], injected into the 2 nd cervical segment (C2), with cholera toxin B (CTB) injected into the 2 nd lumbar segment (L2; Figure 4F).…”

Learning speed and detection sensitivity controlled by distinct cortico-fugal neurons in visual cortex

“…For example, many vertebrates can learn to alter their behavior in response to the detection of arbitrary visual stimuli in order to obtain a reward or avoid punishment ( Llinás, 1976 ; Prusky and Douglas, 2004 ; Skinner, 1963 ; Valente, 2012 ). A major challenge to our understanding of the neuronal basis of this elemental form of sensory-based and goal-directed behavior is that any visual stimulus evokes neuronal activity across multiple brain structures ( Macé et al, 2018 ; Seabrook et al, 2017 ) and, within each structure, across diverse types of neurons ( Harris and Mrsic-Flogel, 2013 ; Harris and Shepherd, 2015 ; Reinhard et al, 2019 ).…”