An intrinsic neural eye tracker in primary visual cortex

Summary Humans and other primates rely on eye movements to explore visual scenes and to track moving objects. As a result, the image that is projected onto the retina – and propagated throughout the visual cortical hierarchy – is almost constantly changing and makes little sense without taking into account the momentary direction of gaze. How is this achieved in the visual system? Here we show that in primary visual cortex (V1), the earliest stage of cortical vision, neural representations carry an embedded “eye tracker” that signals the direction of gaze associated with each image. Using chronically implanted multi-electrode arrays, we recorded the activity of neurons in V1 during tasks requiring fast (exploratory) and slow (pursuit) eye movements. Neurons were stimulated with flickering, full-field luminance noise at all times. As in previous studies 1-4, we observed neurons that were sensitive to gaze direction during fixation, despite comparable stimulation of their receptive fields. We trained a decoder to translate neural activity into metric estimates of (stationary) gaze direction. This decoded signal not only tracked the eye accurately during fixation, but also during fast and slow eye movements, even though the decoder had not been exposed to data from these behavioural states. Moreover, this signal lagged the real eye by approximately the time it took for new visual information to travel from the retina to cortex. Using simulations, we show that this V1 eye position signal could be used to take into account the sensory consequences of eye movements and map the fleeting positions of objects on the retina onto their stable position in the world.