Compartmentalized versus Global Synaptic Plasticity on Dendrites Controlled by Experience

Synapses in the brain are continuously modified by experience, but the mechanisms are poorly understood. In vitro and theoretical studies suggest threshold-lowering interactions between nearby synapses that favor clustering of synaptic plasticity within a dendritic branch. Here, a fluorescently tagged AMPA receptor-based optical approach was developed permitting detection of single-synapse plasticity in mouse cortex. Sensory experience preferentially produced synaptic potentiation onto nearby dendritic synapses. Such clustering was significantly reduced by expression of a phospho-mutant AMPA receptor that is insensitive to threshold-lowering modulation for plasticity-driven synaptic incorporation. In contrast to experience, sensory deprivation caused homeostatic synaptic enhancement globally on dendrites. Clustered synaptic potentiation produced by experience could bind behaviorally relevant information onto dendritic subcompartments; global synaptic upscaling by deprivation could equally sensitize all dendritic regions for future synaptic input. ► Recent history of in vivo synaptic plasticity is identified at individual spines ► Sensory experience drives compartmentalized synaptic potentiation ► Sensory deprivation drives global synaptic upscaling ► Plasticity threshold controls compartmentalized synaptic potentiation