Contributions of superior colliculus and primary visual cortex to visual spatial detection in freely moving mice

Visual spatial detection is a crucial first step in vision to guide decision-making and action.1,2,3,4 However, its neural basis in freely behaving animals remains unclear due to challenges in controlling visual input and monitoring eye- and head-position.5,6 Studies in head-fixed mice have shown that both the superior colliculus (SC) and primary visual cortex (V1), two key visual processing hubs in mammals, contribute to visual spatial detection.7,8,9 Yet their relative roles in freely moving animals are poorly understood. Here, we developed a novel approach to study the neural mechanisms of visual spatial detection in unrestrained mice. We combined closed-loop presentation of visual stimuli with neural recordings, optogenetic manipulation, and simultaneous monitoring of eye and head position. Our results show that SC cells are more predictive of reaction times than V1 cells. Furthermore, SC neurons exhibit more sustained activity than V1 neurons during visual spatial detection. Optogenetic SC and V1 silencing causes pervasive and remarkably localized perturbations of visual detection performance. SC silencing has a stronger impact on visual detection than V1 silencing. These results highlight the distinct activity patterns in two principal early visual processing centers and establish their relative causal contributions to visual spatial detection.