Input-Specific Critical Periods for Experience-Dependent Plasticity in Layer 2/3 Pyramidal Neurons

Abstract

Critical periods for experience-dependent plasticity have been well characterized within sensory cortex, in which the ability of altered sensory input to drive firing rate changes has been demonstrated across brain areas. Here we show that rapid experience-dependent changes in the strength of excitatory synapses within mouse primary somatosensory cortex exhibit a critical period that is input specific and mechanistically distinct in layer 2/3 pyramidal neurons. Removal of all but a single whisker [single whisker experience (SWE)] can trigger the strengthening of individual glutamatergic synaptic contacts onto layer 2/3 neurons only during a short window during the second and third postnatal week. At both layer 4 and putative 2/3 inputs, SWE-triggered plasticity has a discrete onset, before which it cannot be induced. SWE synaptic strengthening is concluded at both inputs after the beginning of the third postnatal week, indicating that both types of inputs display a critical period for experience-dependent plasticity. Importantly, the timing of this critical period is both delayed and prolonged for layer 2/3-2/3 versus layer 4-2/3 excitatory synapses. Furthermore, plasticity at layer 2/3 inputs does not invoke the trafficking of calcium-permeable, GluR2-lacking AMPA receptors, whereas it sometimes does at layer 4 inputs. The dissociation of critical period timing and plasticity mechanisms at layer 4 and layer 2/3 synapses, despite the close apposition of these inputs along the dendrite, suggests remarkable specificity for the developmental regulation of plasticity in vivo.