Preferential involvement by nucleus accumbens shell in mediating probabilistic learning and reversal shifts

Abstract

Different subregions of nucleus accumbens (NAc) have been implicated in reward seeking, promoting flexible approach responses, suppressing nonrewarded actions, and facilitating shifts between different discrimination strategies. Interestingly, the NAc does not appear to mediate shifting between stimulus-reward associations (i.e., reversal learning) when reinforcement is predictable. How these nuclei may facilitate flexible response strategies when reward delivery is uncertain remains unclear. We investigated the effects of inactivation of the NAc shell and core on probabilistic reversal learning using an operant task wherein a "correct" response delivered reward on 80% of trials, and an "incorrect" response was reinforced on 20% of trials. Reinforcement contingencies were reversed repeatedly within a session. In well-trained rats, shell inactivation reduced the number of reversals completed and selectively reduced win-stay behavior. This impairment was apparent during the first discrimination, indicating a more general deficit in the use of probabilistic reward feedback to guide action selection. Shell inactivation also impaired reversal performance on a similar task where correct/incorrect choices always/never delivered reward. However, this impairment only emerged after both levers had been associated with reward. Inactivation of NAc core did not impair reversal performance but increased latencies to approach the response levers. These results suggest the NAc shell and core facilitate reward seeking in a distinct yet complementary manner when the relationship between specific actions and reward is uncertain or ambiguous and cognitive flexibility is required. The core promotes approach toward reward-associated stimuli, whereas the shell refines response selection to those specific actions more likely to yield reward. © 2014 the authors.