Behavioural states control binocular vision through input-specific mechanisms

Binocular vision, fusing the overlapping visual field of the two eyes, is essential for high-acuity stereopsis, depth perception and goal-directed behaviours such as navigation and prey hunting. However, under certain behavioural conditions, an animal’s needs may be better served by reduced binocular and enhanced monocular vision, allowing for greater attention to stimuli in the visual periphery. Whether binocular vision, like other forms of sensory processing, undergoes behavioural state-dependent changes is unknown, although classic studies suggest that binocular processing in the adult visual cortex is fixed. Here, by combining behavioural tracking with calcium imaging in layer 2/3 excitatory neurons in the binocular zone of the primary visual cortex (bV1) of adult mice, we show that binocularity and binocular integration change rapidly according to an animal’s arousal state and that these state-dependent changes are driven by eye-/input-specific cellular mechanisms. Specifically, responses of bV1 neurons to contralateral eye stimulation are strongly enhanced during high arousal states, significantly more than upon ipsilateral eye stimulation, and binocular integration in these neurons shifts from a sublinear to a supralinear regime at high arousal. Furthermore, by combining computational modelling and calcium imaging in afferent thalamic and callosal axons, we show that the state-dependent shifts in bV1 can be explained by differential strengthening of afferent inputs to bV1 neurons. Since previous work revealed that neurons in the monocular zone of the primary visual cortex exhibit enhanced responses to contralateral inputs at high arousal, we propose that this state-dependent modulation in bV1 neurons serves to adapt an animal’s visual perception to its behavioural demands by enhancing peripheral vision during sudden arousal to improve perception of potential threats and facilitate faster evasive actions.