Vision reconstructs the cellular composition of binocular circuitry during the critical period

High acuity binocularity is established in primary visual cortex during an early postnatal critical period. In contrast to current models for the developmental of binocular neurons, we find that the binocular network present at the onset of the critical period is dismantled and remade. Using longitudinal imaging of receptive field tuning (e.g. orientation selectivity) of thousands of layer 2/3 neurons through development, we show most binocular neurons present at critical-period onset are poorly tuned and rendered monocular. These are replenished by newly formed binocular neurons that are established by a vision-dependent recruitment of well-tuned ipsilateral inputs to contralateral monocular neurons with matched tuning properties. The binocular network in layer 4 is equally unstable but does not improve. Thus, vision instructs a new and more sharply tuned binocular network in layer 2/3 by exchanging one population of neurons for another and not by refining an extant network. One Sentence Summary Unstable binocular circuitry is transformed by vision into a network of highly tuned complex feature detectors in the cortex.