Trace eyeblink conditioning (EBC) is an associative learning task in which a stimulus-free trace period separates the presentation of a behaviorally neutral conditioned stimulus (CS; whisker stimulation) from a behaviorally salient unconditioned stimulus (US; air puff to the eye). Repeated pairings of the CS with the US results in the emergence of the conditioned response (CR; eyeblink after CS presentation and before US presentation). The goal of these experiments was to determine whether the caudate nucleus (CN) plays a role in retrieval of previously acquired trace EBC after memory consolidation. Lesions of the CN were made 1 month after initial trace EBC. CN-lesioned rabbits performed fewer adaptive CRs and more short-latency non-adaptive responses than sham-lesioned controls. They were not able to improve their CR performance after consolidation as were controls. Single-unit recordings taken from separate cohorts of rabbits demonstrated that neurons in the CN were still responsive to the CS and US 1 month after initial trace EBC, particularly in the medial and ventral CN on trials when a CR occurred. The proportion of rate-increasing neurons was higher in trace-conditioned than in pseudoconditioned rabbits. Neurons in regions destroyed in the behavioral experiment demonstrated prolonged firing during the trace period, which might underlie the results from the behavioral experiment. These data demonstrate that the CN plays an important role in retrieval of a previously learned associative task after memory consolidation has occurred.
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