Characterization of visual response properties and connectivity of Wide-field vertical neurons in the mouse superior colliculus

Abstract

Vision is a sense that serves different ethological functions across species. Visual information can be used to either detect preys or predators and generate orienting or escaping responses. The superior colliculus has been implicated in the orchestration of these behaviors. Within this structure, at the interface between the visual and the multisensory layers, lay the wide-field vertical neurons (WFV). WFV are a conserved morphologically defined cell-type found across many taxa from reptiles to highly visual mammals, independently of their visual ecology. In mammals, these neurons receive direct inputs from the retina and the primary visual cortex, and have the pulvinar as a known target, however, their brain-wide connectivity remains to be identified. These cells display peculiar response properties, but despite their ubiquity and unique morphology, their contribution to vision remains elusive. In this study, we have characterized WFV morphology, connection, and visual response properties in vivo in the laboratory mouse. Viral intersectional approaches revealed their projection patterns. Two-photon calcium imaging in awake mice using a transgenic Cre-line targeting specifically WFV (NTSR1-Cre) confirmed their unique response properties. WFV showed a strong preference for small moving stimuli and a slight bias for certain directions. Interestingly, visual responses to distinct visual stimuli showed variable degrees of adaptation upon repeated presentation. In addition, Cre-dependent rabies tracing unraveled a variety of sources of input which had not been described previously. These results place WFV as a major integrator of visual information in the superior colliculus. Their adaptation to looming stimulus suggest a role in ethologically relevant function in avoiding inappropriate responses, while sustained responses to small moving stimulus might be linked to attentional processes and orienting behaviors. Taken together, this initial characterization paves the way to elucidate the role of these neurons in visual behavior.