Behavioral modulation and molecular definition of wide-field vertical cells in the mouse superior colliculus.

Abstract

Visual information can have different meanings across species and the same visual stimulus can drive appetitive or aversive behavior. The superior colliculus (SC), a visual center located in the midbrain has been involved in driving such behaviors. Within this structure, the wide-field vertical cell (WFV) is a conserved morphological cell-type that is present in species ranging from reptiles to cats (Basso et al., 2021). Here we report our investigation of the connectivity of the WFV, their visual responses and how these responses are modulated by locomotion in male and female laboratory mice. We also address the molecular definition of these cells and attempt to reconcile recent findings acquired by RNA sequencing of single cells in the SC with the Ntsr1-Cre GN209 transgenic mouse line which was previously used to investigate WFV. We use viral strategies to reveal WFV inputs and outputs and confirm their unique response properties using in vivo two-photon imaging. Among the stimuli tested, WFV prefer looming stimuli, a small moving spot, and upward moving visual stimuli. We find that only visual responses driven by a looming stimulus show a significant modulation by locomotion. We identify several inputs to the WFV as potential candidates for this modulation. These results suggest that WFV integrate information across multiple brain regions and are subject to behavioral modulation. Taken together, our results pave the way to elucidate the role of these neurons in visual behavior and allow us to interrogate the definition of cell-types in the light of new molecular definitions.Significant statement Understanding how neuronal response preferences emerge remains a fundamental goal in neuroscience. Our ability to target neuron subpopulations and their embedding in circuits has greatly evolved over the last decades with the development of new tools including transgenic mouse lines and RNA sequencing methods. Here we focus on wide-field vertical cells (WFV) which are found in the superior colliculus, a visual center in the midbrain that is highly conserved across species. Our findings challenge earlier definitions of this cell-type and reconcile them with more modern approaches. Due to their conservation and connectivity, WFV present a model of choice to investigate how neurons gain their response specificity and relationships between structure, function, implication in behavior and molecular profiles.