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.

Keywords: cognitive flexibility; nucleus accumbens; probabilistic reinforcement learning; rat; reversal learning.

Figure 1.

Histology and task acquisition. A, Left panels, Schematics of coronal section showing the range of acceptable location of infusions within the core (squares) and shell (circles) through the rostral–caudal extent of the NAc for all rats. Right panels, Photomicrographs of representative infusion placements in the shell and core. Bottom, Number of reversals completed per session over the course of training for rats trained on the probabilistic (B) and deterministic (C) reversal tasks. Error bars represent SEM.

Figure 2.

Inactivation of the NAc shell impairs probabilistic reversal performance. A, Microinfusions of baclofen and muscimol (Bac/Mus) reduced the number of reversals completed per 100 successful trials, relative to control treatments (n = 12). B, Shell inactivation caused a selective decrease in win–stay tendencies without affecting lose–shift behavior. C, Errors to achieve criterion performance during the initial discrimination and first reversal phase of the probabilistic reversal task after inactivation and control treatments. Shell inactivation increased the error rate during the first discrimination of the session, and this effect persisted during the first reversal. ★p < 0.05. Error bars represent SEM.

Figure 3.

Inactivation of the NAc core does not alter performance during probabilistic reversal learning. A, Number of reversals completed per 100 successful trials after saline or inactivation treatments within the NAc core (n = 11). B, Neither win–stay nor lose–shift tendencies were altered after NAc core inactivation relative to control treatments. C, Errors to achieve criterion performance during the initial discrimination and first reversal phase of the probabilistic reversal task after inactivation and control treatments. Core inactivation caused a slight but nonsignificant increase in the error rate during the first discrimination but had no effect on performance of the first reversal. Error bars represent SEM.

Figure 4.

Inactivation of the NAc shell, but not core, impairs reversal performance using assured outcomes A, Inactivation of the shell reduced the number of reversals completed per 100 successful trials, relative to control treatments (n = 6). B, Errors to achieve criterion performance during the initial discrimination, the first and second first reversal phases. As opposed to what was observed during probabilistic reversal learning, shell inactivation did not impair performance during the first discrimination or the first reversal of the session. However, these treatments did increase the error rate during the second reversal, after both levers had been associated with reward during the session. In contrast, inactivation of the core (n = 5) did not affect the number of reversals completed (C) or errors to criterion during the first three phases of the task (D). ★p < 0.05. Error bars represent SEM.