Thalamocortical Projections onto Behaviorally Relevant Neurons Exhibit Plasticity during Adult Motor Learning

Layer 5 neurons of the neocortex receive direct and relatively strong input from the thalamus. However, the intralaminar distribution of these inputs and their capacity for plasticity in adult animals are largely unknown. In slices of the primary motor cortex (M1), we simultaneously recorded from pairs of corticospinal neurons associated with control of distinct motor outputs: distal forelimb versus proximal forelimb. Activation of ChR2-expressing thalamocortical afferents in M1 before motor learning produced equivalent responses in monosynaptic excitation of neurons controlling the distal and proximal forelimb, suggesting balanced thalamic input at baseline. Following skilled grasp training, however, thalamocortical input shifted to bias activation of corticospinal neurons associated with control of the distal forelimb. This increase was associated with a cell-specific increase in mEPSC amplitude but not presynaptic release probability. These findings demonstrate distinct and highly segregated plasticity of thalamocortical projections during adult learning. [Display omitted] •Thalamocortical layer 5 circuits exhibit learning-related plasticity in adulthood•Motor learning strengthens input selectively onto task-relevant L5 neurons•The quantal amplitude of thalamocortical layer 5 inputs increases with learning•The release probability of thalamocortical layer 5 inputs is unaffected by learning Biane et al. investigate thalamocortical signaling to the layer 5 motor cortex in adult animals, finding that synaptic input is distributed evenly across distinct subpopulations of corticospinal neurons at baseline but exhibits plasticity selectively onto task-related neurons in adulthood with motor learning.