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Neuronal Correlates of Instrumental Learning in the Dorsal Striatum

¹Interdepartmental Neuroscience Program, Yale University; ²Division of Molecular Psychiatry, Yale University, Connecticut Mental Health Center, Abraham Ribicoff Research Facilities; and ³John B. Pierce Laboratory, New Haven, Connecticut

Submitted 24 March 2009; accepted in final form 11 May 2009

We recorded neuronal activity simultaneously in the medial and lateral regions of the dorsal striatum as rats learned an operant task. The task involved making head entries into a response port followed by movements to collect rewards at an adjacent reward port. The availability of sucrose reward was signaled by an acoustic stimulus. During training, animals showed increased rates of responding and came to move rapidly and selectively, following the stimulus, from the response port to the reward port. Behavioral "devaluation" studies, pairing sucrose with lithium chloride, established that entries into the response port were habitual (insensitive to devaluation of sucrose) from early in training and entries into the reward port remained goal-directed (sensitive to devaluation) throughout training. Learning-related changes in behavior were paralleled by changes in neuronal activity in the dorsal striatum, with an increasing number of neurons showing task-related firing over the training period. Throughout training, we observed more task-related neurons in the lateral striatum compared with those in the medial striatum. Many of these neurons fired at higher rates during initiation of movements in the presence of the stimulus, compared with similar movements in the absence of the stimulus. Learning was also accompanied by progressive increases in movement-related potentials and transiently increased theta-band oscillations (5–8 Hz) in simultaneously recorded field potentials. Together, these data suggest that representations of task-relevant stimuli and movements develop in the dorsal striatum during instrumental learning.

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