Communication between the Anterior Cingulate Cortex and Ventral Tegmental Area during a Cost-Benefit Reversal Task

Abstract

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.

Training-Induced Circuit-Specific Excitatory Synaptogenesis is Required for Effort Control

“…ACC is known to receive VGluT1 inputs from the Claustrum (CLA) and Hippocampus (Chia et al, 2020;Kol et al, 2020;Qadir et al, 2018;White et al, 2018). Moreover, it also receives a plethora of neuromodulatory inputs from the Ventral Tegmental Area (VTA) and the Raphe nuclei (Sun et al, 2019;Elston et al, 2019). In the future, investigation of the ACC-DMS neurons and their functional connectivity will expand our knowledge of this critical circuit required for effort/reward evaluation and adaptability of instrumental actions.…”

ACC Theta Improves Hippocampal Contextual Processing during Remote Recall

“…For example, the VTA entrains both areas during working memory (Fujisawa and Buzsá ki, 2011) and could do the same during remote recall. However, it is worth mentioning that the ACC can also drive VTA activity during high-effort responses (Elston and Bilkey, 2017;Elston et al, 2019), and one could argue that remote recall is a high-effort cognitive process. All these possibilities require further experimentation to evaluate, but given the data presented here, the simplest explanation is that the ACC is driving CA1 activity via theta oscillations during remote recall.…”

Neural Representation of Costs and Rewards in Decision Making

“…However, it is now known that the involvement of the dopaminergic system in the reward encoding process does not mean that this system gives animals pleasurable feelings [18][19][20]. Later research has suggested that, apart from dopaminergic system, other brain areas such as the anterior cingulate cortex (ACC), prefrontal cortex, and limbic systems, etc., are also involved in the encoding of rewards for the decision-making process [21][22][23][24]. Finding multiple brain regions that could encode the reward does not imply the failure of seeking a congruent pattern with incongruent results.…”

“…For those neurons with activity that is correlated with the predicted task value, a pattern can be seen as to whether the value is modulated by probability or reward size [24]. Interestingly, the connections between the VTA and ACC appear to be important outcome learning and action execution, with the ACC-to-VTA signalling being involved in anticipatory choice and the VTA-to-ACC signalling being involved in error detection [23]. This is consistent with the idea that ACC is a site for action selection for the acquisition of rewards.…”