Cognitive control involves theta power within trials and beta power across trials in the prefrontal-subthalamic network

Abstract

There is increasing evidence that the medial prefrontal cortex participates in conflict and feedback monitoring while the subthalamic nucleus adjusts actions. Yet how these two structures coordinate their activity during cognitive control remains poorly understood. We recorded from the human prefrontal cortex and the subthalamic nucleus simultaneously while participants (n = 22) performed a novel task involving high conflict trials, complete response inhibition trials, and trial-to-trial behavioural adaptations to conflict and errors. Overall, we found that within-trial adaptions to both conflict and complete response inhibition involved changes in the theta band while across-trial behavioural adaptations to both conflict and errors involved changes in the beta band (P < 0.05). Yet the role each region’s theta and beta oscillations played during the task differed significantly between the two sites. Trials that involved either within-trial conflict or complete response inhibition were associated with increased theta phase synchrony between the medial prefrontal cortex and the subthalamic nucleus (P < 0.05). Despite increased synchrony, however, increases in prefrontal theta power were associated with response inhibition, while increases in subthalamic theta power were associated with response execution (P < 0.05). In the beta band, post-response increases in prefrontal beta power were suppressed when the completed trial contained either conflict or an erroneous response (P < 0.05). Subthalamic beta power, on the other hand, was only modified during the subsequent trial that followed a conflict or error trial. Notably, these adaptation trials exhibited slower response times (P < 0.05), suggesting that both brain regions contribute to across-trial adaptations but do so at different stages of the adaptation process. Taken together, our data shed light on the mechanisms underlying within-trial and across-trial cognitive control and how disruption of this network can negatively impact cognition. More broadly, however, our data also demonstrate that the specific role of a brain region, rather than the frequency being utilized, governs the behavioural correlates of oscillatory activity.

Cortical network mechanisms of response inhibition

“…No STN activity was detected by our source reconstruction contrast, most likely because MEG is less sensitive to subcortical compared to cortical sources (Gross, 2019). Nonetheless, several studies with intracranial recordings detected beta-band oscillations within the STN (Kühn et al, 2004;Ray et al, 2012;Zavala et al, 2018;Fischer et al, 2018), also supporting the importance of beta-band oscillations in response inhibition.…”

Non-selective inhibition of inappropriate motor-tendencies during response-conflict by a fronto-subthalamic mechanism

“…Specifically, while the finding that conflict and action-stopping evoke low-frequency activity in mPFC, whereas the BG and the motor-system communicate in the β-band, is in line with the prior literature, no study so far offers any mechanism by which low-frequency interactions between mPFC and STN are translated into β-frequency interactions between the BG and M1. Interestingly, a recent study has found that low-frequency and β-band activity may influence conflict-adaptation at different times of the trial, and that cross-regional increases in synchrony at low frequencies are independent of the frequency of local activity in STN and prefrontal cortex during these adaptive behaviors (Zavala et al, 2018).…”

Cortico-subthalamic Coherence in a Patient With Dystonia Induced by Chorea-Acanthocytosis: A Case Report

“…The two phenomena could, therefore, be related. Low frequency coherence between the STN and medial prefrontal cortex has been the subject of a number of recent studies where it has been shown to be involved in adjustment of decision thresholds for high conflict trials during decision-making tasks (Zavala et al, 2014, 2016, 2018; Herz et al, 2017; Hell et al, 2018; Kelley et al, 2018). Interestingly, despite the fact that all these studies were done on PD patients with STN-DBS, low-frequency coherence between the STN and medial prefrontal cortex was not observed at rest in PD (Hirschmann et al, 2011; Litvak et al, 2011a) and instead both studies reported coherence with temporo-parietal areas in the same band with Litvak et al also reporting additional peak in the brainstem.…”