Abstract
Modifications of synaptic inputs and cell-intrinsic properties both contribute to neuronal plasticity and development. To better understand these mechanisms, we undertook an intracellular analysis of the development of direction selectivity in the ferret visual cortex, which occurs rapidly over a few days after eye opening. We found strong evidence of developmental changes in linear spatiotemporal receptive fields of simple cells, implying alterations in circuit inputs. Further, this receptive field plasticity was accompanied by increases in near-spike-threshold excitability and input-output gain that resulted in dramatically increased spiking responses in the experienced state. Increases in subthreshold membrane responses induced by the receptive field plasticity and the increased input-output spiking gain were both necessary to explain the elevated firing rates in experienced ferrets. These results demonstrate that cortical direction selectivity develops through a combination of plasticity in inputs and in cell-intrinsic properties.
Highlights
A major principle of developmental neuroscience is the concept of initial overproduction of connections followed by activity-dependent pruning (Brown et al, 1976; Changeux and Danchin, 1976; Huttenlocher, 1979; Purves and Lichtman, 1980; Miller et al, 1989; Petanjek et al, 2011)
In cortical simple cells in the visually experienced state, direction selectivity is thought to arise from spatiotemporally selective inputs activating the cell at varying spatial positions and temporal latencies (DeAngelis et al, 1993a; Jagadeesh et al, 1993; McLean et al, 1994; Livingstone, 1998)
A direction-selective simple cell with its inputs organized in this manner exhibits a stereotypical “slant” in its spatiotemporal receptive field
Summary
A major principle of developmental neuroscience is the concept of initial overproduction of connections followed by activity-dependent pruning (Brown et al, 1976; Changeux and Danchin, 1976; Huttenlocher, 1979; Purves and Lichtman, 1980; Miller et al, 1989; Petanjek et al, 2011). Overproduction of inputs should produce receptive or motor fields that are initially broad and diffuse and that become selective as synapses are pruned by correlational processes that depend on the animal’s own experiences (Miller et al, 1989) It is unclear if synaptic overproduction followed by pruning underlie the development of response selectivities in the mammalian visual cortex (V1). It has been demonstrated that a set of inputs activating the cell at varying spatial positions and temporal latencies following a specific spatiotemporal order underlies direction selectivity in the visually mature state (DeAngelis et al, 1993a; Jagadeesh et al, 1993; McLean et al, 1994; Livingstone, 1998) It remains unclear how this very precise spatiotemporal pattern emerges during development. Spatiotemporal receptive fields may be initially compact and obtain selectivity, at least in part, by expanding with experience
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