Defined cell types in superior colliculus make distinct contributions to prey capture behavior in the mouse

Abstract

The superior colliculus (SC) mediates rapid orienting to visual stimuli across species. To determine the specific circuits within the SC that drive orienting and approach behavior toward appetitive stimuli, we explored the role of three genetically defined cell types in mediating prey capture in mice. Chemogenetic inactivation of two classically defined cell types, the wide-field (WF) and narrow-field (NF) vertical neurons, revealed that they are involved in distinct aspects of prey capture. WF neurons were required for rapid prey detection and distant approach initiation, whereas NF neurons were required for continuous and accurate orienting during pursuit. In contrast, prey capture did not require parvalbumin-expressing (PV) neurons that have previously been implicated in fear responses. The visual coding of WF and NF cells in the awake mouse and their projection targets were consistent with their roles in prey detection versus pursuit. Thus, our studies link specific neural circuit connectivity and function with stimulus detection and orienting behavior, providing insight into visuomotor and attentional mechanisms mediated by superior colliculus. Highlights• This study provides the first demonstration of the role of specific cell populations in the superior colliculus in orienting and approach behavior.• A genetically targeted population of wide-field vertical neurons in the superior colliculus is required for rapid prey detection and initiation of long-distance approaches.• A genetically targeted population of narrow-field vertical neurons is required for approach initiation, accurate targeting, and approach continuity.• Visual response properties and projection targets of these cells are consistent with their role in prey capture, linking neural circuit connectivity and function with behavior.

A specialized reciprocal connectivity suggests a link between the mechanisms by which the superior colliculus and parabigeminal nucleus produce defensive behaviors in rodents

“…In the awake cat, the firing rate of PBG cells encodes for retinal position error, the distance formed between gaze direction and the location of the pursued target 18,71 . In addition, a recent report showed that the chemogenetic inactivation of narrow field cells in the SC diminishes orienting, pursuing and capture maneuvers in hunting mice 72 , while the inactivation of parvalbumin-positive cells that mediate escape responses 17 does not affect hunting behavior 72 . Since both cell types project to the PBG it would be interesting to find out whether they do it to different subdivisions.…”

An approach for long-term, multi-probe Neuropixels recordings in unrestrained rats

“…Chronic implantations are particularly crucial for experiments that examine behaviors involving unrestrained movement, such as some perceptual decision-making (Brunton et al, 2013) tasks, exploration (Tervo et al, 2014), navigation (Ito et al, 2015), escape (Juavinett et al, 2019), foraging (Davidson & El Hady, 2019), and prey-capture (Hoy et al, 2019). However, the deployment of these probes in experiments requiring chronic implantation has remained limited (Juavinett et al, 2019;Jun et al, 2017;Krupic et al, 2018).…”

An offset ON-OFF receptive field is created by gap junctions between distinct types of retinal ganglion cells

“…Recent work has shown that mice use vision to capture small, quickly moving prey objects, like crickets 27,28 , so perhaps precise edge localization with F-mini-ON RGCs plays a role in this behavior. Since the RF offset in F-mini-ON RGCs is along the vertical axis, our model showed enhanced object localization preferably along this axis (Fig.…”