Eye-specific drive and binocular suppression in mouse visual cortex during critical period development

Abstract

A key function of cortical sensory circuits is to integrate information from multiple sources to build a unified representation of the external environment. The binocular region of the mouse primary visual cortex (bV1) is a valuable model for studying sensory integration, as visual response properties of inputs from the contralateral (contra) and ipsilateral (ipsi) eye onto bV1 neurons become matched to one another over development. While the alignment of visual responses from each eye during this developmental critical period has been well-characterized, it remains unclear how this interocular alignment influences, and is influenced by, the binocularly driven responses of bV1 neurons. Here, we recorded the monocular and binocular visual response properties of layer 2/3 bV1 neurons by performing chronic two-photon calcium imaging at multiple time points spanning the ocular-dominance critical period. We found that ipsi driven responses strengthened in bV1 neurons alongside a concurrent increase in binocular suppression. Binocular tuning properties were more strongly aligned with contra responses than with ipsi responses throughout development but became progressively better matched to ipsi responses. Additionally, the explained variance of ipsi input to predicting binocular tuning increased. In chronically tracked bV1 neurons, the preferred orientation of ipsi eye driven responses was less stable than that of contra eye driven responses, and in well-tuned stable binocular neurons, ipsi and contra preferences became progressively better matched. Using population-based decoding analyses, we found that while monocular and binocular visual encoding remained stable, there was increased generalizability between visual encoding by binocular and ipsi eye driven responses. Overall, our data suggest a reciprocal interaction between ipsi development and binocular responses, such that ipsi visual inputs dynamically structure excitatory as well as putative inhibitory drive onto binocular neurons during the critical period to generate the circuitry that implements integrated binocular vision.