The Nucleus Accumbens Core Is Necessary for Responding to Incentive But Not Instructive Stimuli

An abundant literature has highlighted the importance of the nucleus accumbens core (NAcC) in behavioral tasks dependent on external stimuli. Yet, some studies have also reported the absence of involvement of the NAcC in stimuli processing. We aimed at comparing, in male rats, the underlying neuronal determinants of incentive and instructive stimuli in the same task. We developed a variant of a GO/NOGO task that reveals important differences in these two types of stimuli. The incentive stimulus invites the rat to engage in the task sequence. Once the rat has decided to initiate a trial, it remains engaged in the task until the end of the trial. This task revealed the differential contribution of the NAcC to responding to different types of stimuli: responding to the incentive stimulus depended on NAcC AMPA/NMDA and dopamine D1 receptors, but the retrieval of the response associated with the instructive stimuli (lever pressing on GO, withholding on NOGO) did not. Our electrophysiological study showed that more NAcC neurons responded more strongly to the incentive than the instructive stimuli. Furthermore, when animals did not respond to the incentive stimulus, the induced excitation was suppressed for most projection neurons, whereas interneurons were strongly activated at a latency preceding that found in projection neurons. This work provides insight on the underlying neuronal processes explaining the preferential implication of the NAcC in deciding whether and when to engage in reward-seeking rather than to decide which action to perform.SIGNIFICANCE STATEMENT The nucleus accumbens core (NAcC) is essential to process information carried by reward-predicting stimuli. Yet, stimuli have distinct properties: incentive stimuli orient the attention toward reward-seeking, whereas instructive stimuli inform about the action to perform. Our study shows that, in male rats, NAcC perturbation with glutamate or dopamine antagonists impeded responses to the incentive but not to the instructive stimulus. NAcC neuronal recordings revealed a stronger representation of incentive than instructive stimuli. Furthermore, we found that interneurons are recruited when rats fail to respond to incentive stimuli. This work provides insight on the underlying neuronal processes explaining the preferential implication of the NAcC in deciding whether and when to engage in reward-seeking rather than to decide which action to perform.