Conflict and adaptation signals in the anterior cingulate cortex and ventral tegmental area

Abstract

The integration and utilization of feedback in order to determine which decision strategy to use in different contexts is the core of executive function. The anterior cingulate cortex (ACC) is central to these processes but how feedback is made available to the ACC is unclear. To address this question, we trained rats with implants in the ACC and the ventral tegmental area (VTA), a dopaminergic brain region implicated in feedback processing, in a spatial decision reversal task with rule switching occurring approximately every 12 trials. Following a rule switch, the rats had to shift and sustain responses to the alternative side in order to obtain reward. Partial directed coherence (PDC) models of signal directionality between the ACC and VTA indicated that VTA → ACC communication (near 4 Hz) increased immediately prior to incorrect choices and during post-error decisions. This increase did not occur during correct choices. These data indicate that the VTA provides a feedback-driven, bottom-up modulating signal to the ACC which may be involved in assessing, and correcting for, decision conflict.

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

“…See also Figure S2. prediction error (PE)-like signaling (Hyman, Holroyd and Seamans, 2017), which serves to update ACC task representations, thereby adapting future behavior. This later PE-adaptation interpretation fits with our own prior work (Elston et al, 2018), as well as a significant body of work by others (e.g., Ellwood et al, 2017;Holroyd and Coles, 2008;Kroener et al, 2009;Ma et al, 2014;Narayanan et al, 2013;Ott and Nieder, 2017;Parker et al, 2014). However, future studies that causally manipulate the VTA dopaminergic projection to the ACC while simultaneously recording whole ensembles of ACC neurons will be necessary to test this hypothesis.…”

“…We also found elevated VTA-to-ACC signaling in the reward region (i.e., at the outcome) of post-reversal LCLR choices. Considering that the majority of post-reversal LCLR choices occurred during the trials immediately after the reversal and that the rats rapidly adapted their subsequent choice behavior (Figures 2A and 2B), this finding appears to replicate our prior finding (Elston et al, 2018) that elevated 4-Hz VTA-to-ACC signaling is associated with error detection and subsequent behavioral adaptation.…”

“…Another interpretation suggested by prior studies of mesocortical signaling (Ellwood et al, 2017;Elston et al, 2018) is that the post-reversal VTA-to-ACC signal might be involved in the modification of the current ACC task model. Because post-reversal LCLR decisions likely reflect errors and the rats rapidly adapted their subsequent decision patterns post-error, it is possible that the post-reversal mesocortical signals we observed reflect decision conflict and feedback integration (Elston et al, 2018). Another possibility is that the increased post-LCLR VTA-to-ACC communication could be due to Data are from the same session and rat as the trajectory-mapped power and coherence in Figures 5.…”

“…We then determined the mean VTA and ACC power and coherence in the 2-to 5-Hz (hence, 4-Hz) band for each maze region for each trial within each session. In order to pool trials across animals, we used a regression approach (Elston et al, 2018;Ma et al, 2014) to control for between-subject variance (see STAR Methods) and conducted subsequent spectral analyses on the residuals unless specifically noted. Only free choices were included in the subsequent analyses.…”

“…To further clarify the directionality of the VTA-ACC signaling as inferred from LFP data, we used PDC modeling (Baccalá and Sa-meshima, 2001;Boykin et al, 2012), which exploits the predictability of one brain area at one point in time by another brain area at a different time point in the frequency domain. The advantage of PDC modeling over other methods we have used to assess directionality, such as amplitude cross-correlations (Adhikari et al, 2010;Elston and Bilkey, 2017;Elston et al, 2018), is that it allows for testing the possibility of simultaneous, bi-directional communication, which is likely to occur between two reciprocally connected structures like the ACC and VTA. We fitted PDC models in the 2-to 5-Hz (hence, 4-Hz) frequency band for each maze region of each trial for each animal separately.…”