Frontal Oscillatory Dynamics Predict Feedback Learning and Action Adjustment

Abstract

Abstract■ Frontal oscillatory dynamics in the theta (4-8 Hz) and beta (20-30 Hz) frequency bands have been implicated in cognitive control processes. Here we investigated the changes in coordinated activity within and between frontal brain areas during feedback-based response learning. In a time estimation task, participants learned to press a button after specific, randomly selected time intervals (300-2000 msec) using the feedback after each button press (correct, too fast, too slow). Consistent with previous findings, theta-band activity over medial frontal scalp sites (presumably reflecting medial frontal cortex activity) was stronger after negative feedback, whereas beta-band activity was stronger after positive feedback. Theta-band power predicted learning only after negative feedback, and beta-band power predicted learning after positive and negative feedback. Furthermore, negative feedback increased theta-band intersite phase synchrony (a millisecond resolution measure of functional connectivity) among right lateral prefrontal, medial frontal, and sensorimotor sites. These results demonstrate the importance of frontal theta-and beta-band oscillations and intersite communication in the realization of reinforcement learning. ■

Complementary roles of cortical oscillations in automatic and controlled processing during rapid serial tasks

“…These results are therefore consistent with the idea that right frontal theta oscillations are important for coordinating different brain regions across different frequency bands during action monitoring and cognitive control throughout task performance (Cavanagh et al, 2009;Cohen, 2011;Gevins et al, 1997;Igarashi et al, 2013;Ishii et al, 1999;Jensen and Tesche, 2002;Mizuhara and Yamaguchi, 2007;Sauseng et al, 2010;van de Vijver et al, 2011). Conversely, for "go" responses, no frontal theta peak sources were found and only minimal theta activity (using peak locations from other response types) were observedconsistent with the hypothesis that prepotent responding is driven by Type 1 automatic processes with minimal action monitoring and cognitive control required.…”

Neurophysiological differences in reward processing in anhedonics

“…In this sense, it has been proposed that medial frontal theta activity represents the broad coordination of several brain regions implicated in action monitoring and control processes (Cavanagh et al, 2010). Accordingly, theta power increases seem to be relevant for task switching (Cunillera et al, 2012), for improving learning (van de Vijver et al, 2011), and for future behavioral adjustments (Cavanagh, Cohen, & Allen, 2009;Cavanagh et al, 2010;Womelsdorf et al, 2010).…”

“…Accordingly, these signals in the mPFC might help the organism to detect potential cognitive conflicts arising from previous expectations and unexpected outcomes, enhancing action monitoring and control processes (Botvinick, Cohen, & Carter, 2004;Holroyd & Coles, 2002;Ridderinkhof, Ullsperger, Crone, & Nieuwenhuis, 2004). In this regard, it has been proposed that increases of the medial-frontal theta component may represent a general top-down mechanism operating over expectation violation and behavioral adaptation in order to improve performance and learning (Cavanagh et al, 2010;Cunillera et al, 2012;Tzur & Berger, 2009;van de Vijver, Ridderinkhof, & Cohen, 2011;Womelsdorf, Johnston, Vinck, & Everling, 2010).…”

The American Marketing Association

“…Beta oscillations upon reward delivery have been related to improved learning of stimulus materials or task contingencies (i.e., reinforcement learning; Cohen, Elger, and Ranganath 2007); the increase in beta band oscillations following positive reinforcement has been suggested to function as a mechanism to strengthen the current representations of value and reward, thereby influencing future behavior (Van de Vijver, Ridderinkhof, and Cohen 2011). Indeed, beta oscillations following reward delivery have been found to be predictive of improved memory performance for the rewarded stimuli (Kawasaki and Yamaguchi 2013).…”

“…Research has shown that medial-frontal EEG oscillations (regular cyclic voltage changes) in the beta frequency range (12-30 Hz;Cohen, Elger, and Ranganath 2007;HajiHosseini, Rodríguez-Fornells, and Marco-Pallarés 2012;Kawasaki and Yamaguchi 2013;Marco-Pallares et al 2008;Van de Vijver, Ridderinkhof, and Cohen 2011) are associated with reward processing, while lower frequencies (most prominently theta, 4-8 Hz) are more related to losses and other negative outcomes (Cavanagh, Cohen, and Allen 2009;Cavanagh et al 2010;Cohen, Elger, and Ranganath 2007;Marco-Pallares et al 2008;Van de Vijver, Ridderinkhof, and Cohen 2011). Indeed, Lucchiari and Pravettoni (2012) recently observed that beta activity seems to be modulated by the experience of pleasure associated with a favorite brand, whereas theta modulation seems to reflect the lack of this experience.…”