A dynamic sequence of visual processing initiated by gaze shifts

Animals move their head and eyes as they explore and sample the visual environment. Previous studies have demonstrated neural correlates of head and eye movements in rodent primary visual cortex (V1), but the sources and computational roles of these signals are unclear. We addressed this by combining measurement of head and eye movements with high density neural recordings in freely moving mice. V1 neurons responded primarily to gaze shifts, where head movements are accompanied by saccadic eye movements, rather than to head movements where compensatory eye movements stabilize gaze. A variety of activity patterns immediately followed gaze shifts, including units with positive, biphasic, or negative responses, and together these responses formed a temporal sequence following the gaze shift. Gaze shift transients appeared to represent the temporal response to the rapid onset of new visual input as they were greatly diminished in the dark for the vast majority of units and were similar to those evoked by sequentially flashed stimuli in head-fixed conditions. Notably, neurons responded in a sequence that matches their spatial frequency (SF) preference, from low to high SF tuning, consistent with coarse-to-fine processing of the visual scene following each gaze shift. Recordings in foveal V1 of freely gazing head-fixed marmosets revealed a similar sequence of temporal response following a saccade, as well as the progression of SF tuning. Together, our results demonstrate that active vision in both mice and marmosets consists of a dynamic temporal sequence of neural activity associated with visual sampling.