State-dependent plasticity of the corticostriatal pathway

Plasticity at corticostriatal synapses is thought to underlie both normal and aberrant forms of reinforcement-driven learning. Studies in brain slices have found bidirectional, spike-timing dependent plasticity in striatum; however it is not known whether similar rules govern corticostriatal plasticity in awake behaving animals. To assess whether behavioral state is a key regulator of plasticity in this pathway, we examined the effects of 5 Hz cortical stimulation trains on evoked striatal field potentials, in either anesthetized or awake, unrestrained rats. Consistent with prior studies we observed long-term potentiation in intact, barbiturate-anesthetized animals. However, when an identical stimulation pattern was applied to the same animals while awake, long-term depression was observed instead. Our results demonstrate that the rules governing corticostriatal plasticity depend critically on behavioral state, and suggest that the dynamic context of cortical-basal ganglia loops must be considered while investigating synaptic mechanisms underlying reinforcement learning and neurological disorders.