Impulsive Choices Emerge When the Anterior Cingulate Cortex Fails to Encode Deliberative Strategies

Abstract

Impulsive individuals excessively discount the value of delayed rewards, and this is thought to reflect deficits in brain regions critical for impulse control such as the anterior cingulate cortex (ACC). Delay discounting (DD) is an established measure of cognitive impulsivity, referring to the devaluation of rewards delayed in time. This study used male Wistar rats performing a DD task to test the hypothesis that neural activity states in ACC ensembles encode strategies that guide decision-making. Optogenetic silencing of ACC neurons exclusively increased impulsive choices at the 8 s delay by increasing the number of consecutive low-value, immediate choices. In contrast to shorter delays where animals preferred the delay option, no immediate or delay preference was detected at 8 s. These data suggest that ACC was critical for decisions requiring more deliberation between choice options. To address the role of ACC in this process, large-scale multiple single-unit recordings were performed and revealed that 4 and 8 s delays were associated with procedural versus deliberative neural encoding mechanisms, respectively. The 4 and 8 s delay differed in encoding of strategy corresponding to immediate and delay run termination. Specifically, neural ensemble states at 4 s were relatively stable throughout the choice but exhibited temporal evolution in state space during the choice epoch that resembled ramping during the 8 s delay. Collectively, these findings indicate that ensemble states in ACC facilitate strategies that guide decision-making, and impulsivity increases with disruptions of deliberative encoding mechanisms.