Anatomical and Sensory Experiential Determinants of Synaptic Plasticity in Layer 2/3 Pyramidal Neurons of Mouse Barrel Cortex

A minority of layer 2/3 (L2/3) pyramidal neurons exhibit spike-timing-dependent long-term potentiation (LTP) in normally reared adolescent mice. To determine whether particular subtypes of L2/3 neurons have a greater capacity for LTP than others, we correlated the morphological and electrophysiological properties of L2/3 neurons with their ability to undergo LTP by using a spike-timing-dependent protocol applied via layer 4 inputs from the neighboring barrel column. No correlation was found between the incidence of LTP and the cell's electrophysiological properties, nor with their laminar or columnar location. However, in cortex of normal, undeprived mice, neurons that exhibited LTP had dendrites that extended farther horizontally than those that showed no plasticity, and this horizontal spread was due to off-axis apical dendrites. From a sample of reconstructed neurons, two-thirds of neurons' dendritic arborizations reached into at least one adjacent barrel column. We also tested whether this relationship persisted following a short period of whisker deprivation. The probability of inducing LTP increased from 33% in cortex of undeprived mice to 53% following 7 days of whisker deprivation, and the incidence of LTD with the same protocol decreased from 49% to 9%. In deprived cortex, neurons exhibiting LTP did not extend any farther horizontally than those that showed no plasticity. Whisker deprivation did not affect horizontal spread of dendrites nor dendritic structure in general but did produced an increase in spine density, both on basal and on apical dendrites, suggesting a possible substrate for the increased levels of LTP observed in deprived cortex. J. Comp. Neurol. 519: 2090-2124, 2011. (C) 2010 Wiley-Liss, Inc.