Spatiotemporal input reorganization and enhancement of input-output gain sharpen cortical direction selectivity during development

In the primary visual cortex (V1) of carnivores and primates, early visual experience shapes the development of functional properties such as selectivity for direction of motion. However, it remains unclear which aspects of the cortical circuitry - synaptic and/or cell-intrinsic - are molded by the visual activity, and how. Therefore, we performed in vivo intracellular recordings from V1 simple cells in visually naive and experienced ferrets, and computed their membrane potential (Vm) spatiotemporal receptive fields and Vm-to-spike input-output transfer functions. Comparison across the two developmental stages revealed marked reorganization of inputs and a sharp enhancement of input-output gain in the experienced state, leading to prodigious amplification of direction selectivity at the spiking level. Simultaneously, we detected a lowering of spike thresholds and an intensification of gamma-band Vm oscillations, which might explain the enhancement of spiking. Thus, direction selectivity develops through combined processes of synaptic re-wiring and maturation of cell-intrinsic properties.