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Summary To interpret visual-motion events, the underlying computation must involve internal reference to the motion status of the observer’s head. We show here that layer 6 (L6) principal neurons in mouse primary visual cortex (V1) receive a diffuse, vestibular-mediated synaptic input that signals the angular velocity of horizontal rotation. Behavioral and theoretical experiments indicate that these inputs, distributed over a network of 100 L6 neurons, provide both a reliable estimate and, therefore, physiological separation of head-velocity signals. During head rotation in the presence of visual stimuli, L6 neurons exhibit postsynaptic responses that approximate the arithmetic sum of the vestibular and visual-motion response. Functional input mapping reveals that these internal motion signals arrive into L6 via a direct projection from the retrosplenial cortex. We therefore propose that visual-motion processing in V1 L6 is multisensory and contextually dependent on the motion status of the animal’s head., Highlights • Inputs onto V1 L6 neurons convey head-motion information • These L6 signals are widespread and provide a reliable estimate of angular velocity • In L6 neurons, vestibular and visual inputs sum during sensory processing • At least in part, V1 L6 head-motion signals are conveyed via an RSP-V1 pathway, V1 layer 6 neurons receive a widespread head-motion signal that is integrated with visual input during visual-motion processing. These V1 head-motion inputs project from the retrosplenial cortex, a multisensory area involved in spatial navigation and contextual processing.