Altered sensory experience induces targeted rewiring of local excitatory connections in mature neocortex

Experience-dependent plasticity in adulthood is slower than during development. Previous experience can accelerate adult cortical plasticity. However, the contributions of functional synaptic changes and modifications in neuronal structure to the acceleration of adult cortical plasticity remain unclear. If structural remodeling was important then it should be exhibited by neuronal connections that have altered during plasticity. We trimmed rodents' whiskers to induce experience-dependent plasticity and reconstructed pairs of layer 2/3 (L2/3) pyramidal neurons after electrophysiological recording. We reported recently that local excitatory connections strengthen without a change in synapse number in cortex with retained sensory input (spared) (Cheetham et al., 2007). Here, we show that strengthened connections are rewired. The rewiring involves remodeling of the axonal arbor of excitatory connections with only minor changes in postsynaptic dendritic trees. The axonal remodeling resulted in a greater length of presynaptic axon close to postsynaptic dendrites at existing local excitatory connections in spared cortex. In control cortex, the length of axon close to dendrite in unconnected pairs of L2/3 pyramidal neurons was similar to that in synaptically connected pairs of L2/3 pyramidal neurons. This finding suggests that the probability of forming a synapse and, therefore, establishing a connection, is not driven solely by the length of axon close to dendrite. The axonal remodeling that we describe is not associated with altered synapse number, but instead increases the number of sites where synapses could be formed between synaptically connected neurons with minimal structural changes. This enables rapid and cost-efficient rewiring of local excitatory connections when re-exposed to similarly altered sensory experience in adulthood.