Vision Changes the Cellular Composition of Binocular Circuitry during the Critical Period

High acuity stereopsis emerges during an early postnatal critical period when binocular neurons in the primary visual cortex sharpen their receptive field tuning properties. We find that this sharpening is achieved by dismantling the binocular circuit present at critical period onset and building it anew. Longitudinal imaging of receptive field tuning (e.g., orientation selectivity) of thousands of neurons reveals that most binocular neurons present in layer 2/3 at critical period onset are poorly tuned and are rendered monocular. In parallel, new binocular neurons are established by conversion of well-tuned monocular neurons as they gain matched input from the other eye. These improvements in binocular tuning in layer 2/3 are not inherited from layer 4 but are driven by the experience-dependent sharpening of ipsilateral eye responses. Thus, vision builds a new and more sharply tuned binocular circuit in layer 2/3 by cellular exchange and not by refining the original circuit. •Improvements in ipsilateral eye tuning change binocularity during the critical period•Poorly tuned binocular neurons are rendered monocular•Conversion of sharply tuned monocular neurons establishes new binocular neurons•Vision drives this sharpening and binocular conversion in layer 2/3 and not 4 Tan et al. demonstrate that visually evoked responses of binocular neurons improve across the critical period. This is caused by changing the cellular composition of the binocular pool. Poorly tuned binocular neurons become monocular, while sharply tuned monocular neurons gain matched responses to the other eye and become binocular.