Fast oscillations in cortical‐striatal networks switch frequency following rewarding events and stimulant drugs

Oscillations may organize communication between components of large‐scale brain networks. Although gamma‐band oscillations have been repeatedly observed in cortical‐basal ganglia circuits, their functional roles are not yet clear. Here I show that, in behaving rats, distinct frequencies of ventral striatal local field potential oscillations show coherence with different cortical inputs. The ∼50 Hz gamma oscillations that normally predominate in awake ventral striatum are coherent with piriform cortex, whereas ∼80–100 Hz high‐gamma oscillations are coherent with frontal cortex. Within striatum, entrainment to gamma rhythms is selective to fast‐spiking interneurons, with distinct fast‐spiking interneuron populations entrained to different gamma frequencies. Administration of the psychomotor stimulant amphetamine or the dopamine agonist apomorphine causes a prolonged decrease in ∼50 Hz power and increase in ∼80–100 Hz power. The same frequency switch is observed for shorter epochs spontaneously in awake, undrugged animals and is consistently provoked for < 1 s following reward receipt. Individual striatal neurons can participate in these brief high‐gamma bursts with, or without, substantial changes in firing rate. Switching between discrete oscillatory states may allow different modes of information processing during decision‐making and reinforcement‐based learning, and may also be an important systems‐level process by which stimulant drugs affect cognition and behavior.