Functional recomposition of excitatory synaptic inputs to individual neurons in ferret visual cortex after the onset of visual experience.

Abstract

During early visual cortex development, the onset of visual experience initiates a period of rapid dendritic growth and excitatory synapse formation that coincides with the functional maturation of visually driven neuronal response properties. How this surge in the number of excitatory synaptic inputs refines the initial functional network structure to generate coherent, yet adaptable, single-neuron responses remains unclear. To address this issue, we examined the functional properties and spatial organization of individual dendritic spines of layer 2/3 neurons in ferret visual cortex before and after the onset of visual experience. Our findings indicate that this initial period of visual experience is marked by a dramatic and selective functional and spatial recomposition of the visually naive excitatory synaptic network. This reorganization leads to an increase in the proportion and tuning strength of orientation- and direction-selective inputs and markedly expands the population of binocular inputs, particularly those with highly aligned responses across both eyes. This refinement follows distinct developmental trajectories of contralateral vs. ipsilateral inputs, as well as monocular vs. binocular inputs, that reshape the functional organization of excitatory synaptic inputs to individual neurons. In parallel, synaptic inputs are spatially reorganized, with co-tuned inputs becoming locally clustered along dendrites as a coarser branch-level organization present at eye opening is remodeled. Together, these rapid changes appear to be organized as a scaffold-and-integration process through which visual experience expands and reorganizes the excitatory synaptic network. This process enhances tuning selectivity and supports the emergence of a robust binocular representation while maintaining functional input diversity.