Synaptic and intrinsic mechanisms underlying development of cortical direction selectivity

Some neural circuits are constructed through an overproduction of initial connections followed by activity-dependent refinement. Under this paradigm, functional receptive fields would be expected to be narrowed from a diffuse immature condition to a sharper mature condition. Alternatively, neural activity might lead to formation of new connections, leading to expansion of an initially compact receptive field. In the simple cells of the ferret visual cortex undergoing developmental enhancement of direction selectivity, we found evidence for a mixed mechanism: an expansion of the spatiotemporal receptive fields along the temporal dimension combined with a narrowing in space-time through a marked loss of inputs with certain space-time selectivities. Further, the resulting increase in subthreshold direction selectivity was accompanied by increases in near-spike-threshold excitability and input-output gain that resulted in dramatically increased spiking responses. Increases in subthreshold membrane responses and the increased input-output spiking gain were both necessary to explain firing rates in experienced ferrets. These results demonstrate that cortical direction selectivity develops through a combination of plasticity in synaptic and cell-intrinsic properties.