Graphical Abstract Highlights d Anticipatory decision making is associated with increased ACC/VTA signaling d Sustaining behavior toward a new default is associated with ACC/VTA signaling d Error-related feedback integration is associated with increased VTA/ACC signaling d Error-related VTA/ACC signaling is predictive of subsequent choice adaptation Correspondence telston@nurhopsi.org In Brief Elston et al. find that the initiation and persistence of non-default behavior are associated with increases in top-down, ACC-to-VTA signaling. Additionally, the authors show that error-related feedback integration and subsequent behavioral adaptation accompany increases in bottom-up, VTA-to-ACC signaling. These results indicate that bidirectional ACC-VTA signaling is important for behavioral flexibility. SUMMARYThe anterior cingulate cortex (ACC) is implicated in value-based decision making, anticipation, and adaptation; however, how ACC activity modulates these behaviors is unclear. One possibility is via the ACC's connections with the ventral tegmental area (VTA), a dopaminergic region implicated in motivation and feedback processing. We tested this by monitoring ACC and VTA local field potentials in rats performing a cost-benefit reversal task that elicited both value-based and anticipatory choices. Partial directed coherence analyses revealed that elevated 4-Hz ACC-to-VTA signaling accompanied decisions that appeared to be anticipatory. ACCto-VTA signaling also occurred post-reversal, consistent with it being involved in the initiation of non-default behavior. An analysis of 4-Hz signals in the other direction (VTA-to-ACC) revealed that it was elevated when the rats committed errors and that this signal was followed by behavioral adaptation. Together, these findings suggest that bidirectional communication between the ACC and VTA supports behavioral flexibility.
Schizophrenia is associated with deficits in memory, behavioural flexibility, and motivation, which can result in difficulties in decision-making. The anterior cingulate cortex (ACC) and ventral tegmental area (VTA) are two brain regions that are involved in decision-making, and display dysfunction in schizophrenia. We investigated ACC and VTA activity in the maternal immune activation (MIA) model of a schizophrenia risk factor. Control and MIA rats completed a cost-benefit decision-making task in a continuous T-maze, choosing between a high cost and high reward (HCHR), and a low cost and low reward (LCLR), option. A choice reversal occurred halfway through each session. Single unit activity in the ACC and local field potentials (LFPs) in the VTA were monitored. Overall, MIA and control rats made a similar proportion of HCHR and LCLR choices across the whole recording session, suggesting similar levels of motivation. However, MIA rats made different decisions than controls during periods of increased uncertainty. This appeared to reflect memory deficits and behavioural inflexibility. MIA animals displayed an increase in ACC activity associated with cost, an increase in synchrony of ACC neurons to the VTA theta oscillation, and a decrease in coherence in the delta frequency between the ACC and VTA. These changes suggest that MIA animals may be biased towards focussing on the cost rather than the benefits of the task, a change also seen in schizophrenia. Here, however, the MIA animals may be able to increase motivation to maintain behaviour despite this change.
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