Feedforward and feedback population dynamics during binocular conflict in mouse visual cortex

Abstract

Binocular rivalry arises when incongruent images are presented to the two eyes, producing stochastic alternations in perceptual dominance. While rivalry has been extensively studied in species with highly developed binocular vision, it is unclear whether similar representational dynamics occur in the mouse, a model system that allows large-scale cellular and circuit-level measurements. Here we used two-photon calcium imaging in awake mice to examine the population dynamics of primary visual cortex (V1) and long-range feedback axons from retrosplenial cortex (RSC) during presentation of dichoptically incongruent drifting gratings and natural movies. At the single-cell level, incongruent stimulation increased trial-to-trial variability of visually evoked responses relative to monocular stimulation. Linear SVM decoders trained on monocular responses revealed that during prolonged incongruent stimulation, V1 population activity alternated stochastically between representations of the two competing stimuli in a contrast-dependent manner. Decoder confidence was independent of pupil-indexed arousal state suggesting the dynamics observed may depend mostly on feedforward mechanisms. Transition analyses showed that switches in decoder output were typically driven by the emergence of responses to the ipsilateral stimulus, consistent with release from suppression of the non-dominant population. During incongruent presentation of natural movies, similar representational alternations were observed, indicating that rivalry-like dynamics were not dependent on orientation-selective adaptation. Imaging of RSC[->]V1 feedback axons revealed retinotopically specific, eye and orientation-selective signals that also alternated in dominance across time. These results establish the mouse as a model of rivalry-like cortical dynamics, demonstrate that both feedforward and feedback circuits contribute to representational alternation during binocular conflict, and provide a framework for mechanistic dissection of bistable perception.