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Active gaze behavior organizes V1 activity in freely-moving marmosets

Jingwen LiiD, Vikram Pal SinghiD, Alexander C. HukiD, Jude F. MitchelliD, Cory Thomas MilleriD

Abstract

Human and nonhuman primates rely heavily on vision to actively explore and navigate their environment. Although primate visual cortex has been studied extensively in head-fixed animals, little is known about how the primate visual system supports natural, active vision in freely moving animals. Here, we address this gap in the primary visual cortex (V1) by leveraging a head-mounted eye-tracking system while simultaneously recording the activity of ensembles of single V1 neurons in freely moving marmosets. Our results reveal that primate neural activity is tightly driven by visual input and organized by the temporal structure of natural gaze behavior, and these gaze-related responses are largely abolished in the absence of visual input. We further show that distinct phases of gaze movement, i.e. rapid redirection (gaze shift) and subsequent stabilization (fixation), engage separable suppression and enhancement of the V1 responses. The enhancement during fixation was clearly linked to visual input. Moreover, the amplitudes of naturally-occurring gaze shifts organize RF input across successive fixations, and adaptively shapes fixation-associated enhancement. These findings define the dynamics in V1 that link natural gaze behavior and stimulus-driven responses in freely moving primates. The work opens a previously inaccessible but fundamental regime of primate vision and establishes freely moving paradigms as a foundation for understanding real-world visual processing during ethologically relevant behaviors.

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