Motor skill training induces coordinated strengthening and weakening between neighboring synapses

Motor skill training promotes the formation of parallel fiber multiple-synapse boutons (MSBs) contacting dendritic spine pairs of Purkinje cells in the rat cerebellum. However, the dendritic origin of such spine pairs is unknown. Here, we used three-dimensional electron microscopy reconstruction of synaptic connectivity to demonstrate that motor skill training selectively induced MSBs contacting two spines arising from the same dendrite, consistent with strengthening of local synaptic efficacy. However, excitatory synapses near MSBs were smaller in motor-trained animals, suggesting compensatory depression of MSB-neighbor synapses. Concerted strengthening and weakening of adjacent synapses may enhance synaptic weight differences for information encoding while maintaining stable overall activity levels within local dendritic segments.