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Feedback-Related Negativity and Frontal Midline Theta Reflect Dissociable Processing of Reinforcement.

ABSTRACT: Prediction errors (PEs) encode representations of rewarding and aversive experiences and are critical to reinforcement processing. The feedback-related negativity (FRN), a component of the event-related potential (ERP) that is sensitive to valenced feedback, is believed to reflect PE signals. Reinforcement is also studied using frontal midline theta (FM?) activity, which peaks around the same time as the FRN and increases in response to unexpected events compared to expected events. We recorded EEG while participants completed a monetary incentive delay (MID) task that included positive reinforcement and negative reinforcement conditions with multiple levels of the outcome, as well as control conditions that had no reinforcement value. Despite the overlap of FRN and FM?, these measures indexed dissociable cognitive processing. The FRN was sensitive to errors in both positive and negative reinforcement but not in control conditions, while frontal theta instead was sensitive to outcomes in positive reinforcement and control conditions, but not in negative reinforcement conditions. The FRN was sensitive to the point level of feedback in both positive and negative reinforcement, while FM? was not influenced by the feedback point level. Results are consistent with recent results indicating that the FRN is influenced by unsigned PEs (i.e., a salience signal). In contrast, we suggest that our findings for frontal theta are consistent with hypotheses suggesting that the neural generators of FM? are sensitive to both negative cues and the need for control.

SUBMITTER: Rawls E

PROVIDER: S-EPMC6962175 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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Feedback-Related Negativity and Frontal Midline Theta Reflect Dissociable Processing of Reinforcement.

Rawls Eric E Miskovic Vladimir V Moody Shannin N SN Lee Yoojin Y Shirtcliff Elizabeth A EA Lamm Connie C

Frontiers in human neuroscience 20200109

Prediction errors (PEs) encode representations of rewarding and aversive experiences and are critical to reinforcement processing. The feedback-related negativity (FRN), a component of the event-related potential (ERP) that is sensitive to valenced feedback, is believed to reflect PE signals. Reinforcement is also studied using frontal midline theta (FMΘ) activity, which peaks around the same time as the FRN and increases in response to unexpected events compared to expected events. We recorded ...[more]

PMID: 31998100

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Project description:Frontal-midline theta (FMT) oscillations are increased in amplitude during cognitive control tasks. Since these tasks often conflate cognitive control and cognitive effort, it remains unknown if FMT amplitude maps onto cognitive control or effort. To address this gap, we utilized the glucose facilitation effect to manipulate cognitive effort without changing cognitive control demands. We performed a single-blind, crossover human study in which we provided participants with a glucose drink (control session: volume-matched water) to reduce cognitive effort and improve performance on a visuospatial working memory task. Following glucose consumption, participants performed the working memory task at multiple time points of a 3-h window to sample across the rise and fall of blood glucose. Using high-density electroencephalography (EEG), we calculated FMT amplitude during the delay period of the working memory task. Source localization analysis revealed that FMT oscillations originated from bilateral prefrontal cortex. We found that glucose increased working memory accuracy during the high working memory load condition but decreased FMT amplitude. The decrease in FMT amplitude coincided with both peak blood glucose elevation and peak performance enhancement for glucose relative to water. Therefore, the positive association between glucose consumption and task performance provided causal evidence that the amplitude of FMT oscillations may correspond to cognitive effort, rather than cognitive control. Due to the COVID-19 pandemic, data collection was terminated prematurely; the preliminary nature of these findings due to small sample size should be contextualized by rigorous experimental design and use of a novel causal perturbation to dissociate cognitive effort and cognitive control.NEW & NOTEWORTHY We investigated whether frontal-midline theta (FMT) oscillations tracked with cognitive control or cognitive effort by simultaneous manipulation of cognitive control demands in a working memory task and causal perturbation of cognitive effort using glucose consumption. Facilitation of performance from glucose consumption corresponded with decreased FMT amplitude, which provided preliminary causal evidence for a relationship between FMT amplitude with cognitive effort.

Project description:BackgroundFrontal midline theta (FMT) oscillations (4-8 Hz) are strongly related to cognitive and executive control during mental tasks such as memory processing, arithmetic problem solving or sustained attention. While maintenance of temporal order information during a working memory (WM) task was recently linked to FMT phase, a positive correlation between FMT power, WM demand and WM performance was shown. However, the relationship between these measures is not well understood, and it is unknown whether purposeful FMT phase manipulation during a WM task impacts FMT power and WM performance. Here we present evidence that FMT phase manipulation mediated by transcranial alternating current stimulation (tACS) can block WM demand-related FMT power increase (FMTΔpower) and disrupt normal WM performance.MethodsTwenty healthy volunteers were assigned to one of two groups (group A, group B) and performed a 2-back task across a baseline block (block 1) and an intervention block (block 2) while 275-sensor magnetoencephalography (MEG) was recorded. After no stimulation was applied during block 1, participants in group A received tACS oscillating at their individual FMT frequency over the prefrontal cortex (PFC) while group B received sham stimulation during block 2. After assessing and mapping phase locking values (PLV) between the tACS signal and brain oscillatory activity across the whole brain, FMT power and WM performance were assessed and compared between blocks and groups.ResultsDuring block 2 of group A but not B, FMT oscillations showed increased PLV across task-related cortical areas underneath the frontal tACS electrode. While WM task-related FMTΔpower and WM performance were comparable across groups in block 1, tACS resulted in lower FMTΔpower and WM performance compared to sham stimulation in block 2.ConclusiontACS-related manipulation of FMT phase can disrupt WM performance and influence WM task-related FMTΔpower. This finding may have important implications for the treatment of brain disorders such as depression and attention deficit disorder associated with abnormal regulation of FMT activity or disorders characterized by dysfunctional coupling of brain activity, e.g., epilepsy, Alzheimer's or Parkinson's disease (AD/PD).

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Feedback-Related Negativity and Frontal Midline Theta Reflect Dissociable Processing of Reinforcement.

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Feedback-Related Negativity and Frontal Midline Theta Reflect Dissociable Processing of Reinforcement.

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