Widespread and Multifaceted Binocular Integration in the Mouse Primary Visual Cortex

Abstract

The brain combines two-dimensional images received from the two eyes to form a percept of three-dimensional surroundings. This process of binocular integration in the primary visual cortex (V1) serves as a useful model for studying how neural circuits generate emergent properties from multiple input signals. Here, we perform a thorough characterization of binocular integration using electrophysiological recordings in the V1 of awake adult male and female mice by systematically varying the orientation and phase disparity of monocular and binocular stimuli. We reveal widespread binocular integration in mouse V1 and demonstrate that the three commonly studied binocular properties—ocular dominance, interocular matching, and disparity selectivity—are independent of each other. For individual neurons, the responses to monocular stimulation can predict the average amplitude of binocular response but not its selectivity. Finally, the extensive and independent binocular integration of monocular inputs is seen across cortical layers in both regular-spiking and fast-spiking neurons, regardless of stimulus design. Our data indicate that the current model of simple feedforward convergence is inadequate to account for binocular integration in mouse V1, thus suggesting an indispensable role played by intracortical circuits in binocular computation.SIGNIFICANCE STATEMENTBinocular integration is an important step of visual processing that takes place in the visual cortex. Studying the process by which V1 neurons become selective for certain binocular disparities is informative about how neural circuits integrate multiple information streams at a more general level. Here, we systematically characterize binocular integration in mice. Our data demonstrate more widespread and complex binocular integration in mouse V1 than previously reported. Binocular responses cannot be explained by a simple convergence of monocular responses, contrary to the prevailing model of binocular integration. These findings thus indicate that intracortical circuits must be involved in the exquisite computation of binocular disparity, which would endow brain circuits with the plasticity needed for binocular development and processing.