Trial-by-trial coupling of concurrent electroencephalogram and functional magnetic resonance imaging identifies the dynamics of performance monitoring

Department of Neurophysiology and Pathophysiology, University of Hamburg, Hamburg, Hamburg, Germany
The Journal of Neuroscience : The Official Journal of the Society for Neuroscience (Impact Factor: 6.34). 01/2006; 25(50):11730-7. DOI: 10.1523/JNEUROSCI.3286-05.2005
Source: PubMed


Goal-directed behavior requires the continuous monitoring and dynamic adjustment of ongoing actions. Here, we report a direct coupling between the event-related electroencephalogram (EEG), functional magnetic resonance imaging (fMRI), and behavioral measures of performance monitoring in humans. By applying independent component analysis to EEG signals recorded simultaneously with fMRI, we found the single-trial error-related negativity of the EEG to be systematically related to behavior in the subsequent trial, thereby reflecting immediate behavioral adjustments of a cognitive performance monitoring system. Moreover, this trial-by-trial EEG measure of performance monitoring predicted the fMRI activity in the rostral cingulate zone, a brain region thought to play a key role in processing of response errors. We conclude that investigations of the dynamic coupling between EEG and fMRI provide a powerful approach for the study of higher order brain functions.

    • "A classical view postulates a leading role of anterior cingulate cortex (ACC). This largely stems from scalp-electroencephalography (EEG) studies that have identified the ACC as the generator of an error-related negativity potential occurring around 100 ms after behavioral errors (Gehring et al. 1993;Dehaene et al. 1994;Debener et al. 2005). An alternative hypothesis posits that signals coming from the AI may be the actual input to the error-monitoring network (Sridharan et al. 2008;Ham et al. 2013) and may reflect an error-awareness signal (Ullsperger et al. 2010;Klein et al. 2013). "
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    ABSTRACT: The ability to monitor our own errors is mediated by a network that includes dorsomedial prefrontal cortex (dmPFC) and anterior insula (AI). However, the dynamics of the underlying neurophysiological processes remain unclear. In particular, whether AI is on the receiving or driving end of the error-monitoring network is unresolved. Here, we recorded intracerebral electroencephalography signals simultaneously from AI and dmPFC in epileptic patients while they performed a stop-signal task. We found that errors selectively modulated broadband neural activity in human AI. Granger causality estimates revealed that errors were immediately followed by a feedforward influence from AI onto anterior cingulate cortex and, subsequently, onto presupplementary motor area. The reverse pattern of information flow was observed on correct responses. Our findings provide the first direct electrophysiological evidence indicating that the anterior insula rapidly detects and conveys error signals to dmPFC, while the latter might use this input to adapt behavior following inappropriate actions.
    No preview · Article · Jan 2016 · Cerebral Cortex
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    • "Using a flanker task, Botvinick et al. (1999) found that incongruent (high-conflict) trials following congruent (lowconflict ) trials produced greater error-related anterior cingulate cortex (ACC) activation than did incongruent trials following other incongruent trials. The neural generator of ERN has been intimately linked to the ACC (van Veen & Carter, 2002; Ridderinkhof et al. 2004; Debener et al. 2005), and there are robust findings of error-related ACC abnormalities in OCD patients (Ursu et al. 2003; Fitzgerald et al. 2005; Maltby et al. 2005). Importantly, ERN has repeatedly been shown to be hyperactive in individuals with OCD compared to controls (Gehring et al. 2000; Johannes et al. 2001; Santesso et al. 2006; Endrass et al. 2008, 2010, 2014; Hajcak et al. 2008; Hanna et al. 2012; Carrasco et al. 2013; Klawohn et al. 2014; Weinberg et al. 2015) reviewed in (Mathews et al. 2012). "
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    ABSTRACT: Background: Obsessive-compulsive disorder (OCD) is associated with an abnormally large error-related negativity (ERN), an electrophysiological measure of error monitoring in response to performance errors, but it is unclear if hoarding disorder (HD) also shows this abnormality. This study aimed to determine whether the neurophysiological mechanisms underlying error monitoring are similarly compromised in HD and OCD. Method: We used a visual flanker task to assess ERN in response to performance errors in 14 individuals with HD, 27 with OCD, 10 with HD+OCD, and 45 healthy controls (HC). Age-corrected performance and ERN amplitudes were examined using analyses of variance and planned pairwise group comparisons. Results: A main effect of hoarding on ERN (p = 0.031) was observed, indicating ERN amplitudes were attenuated in HD relative to non-HD subjects. A group × age interaction effect on ERN was also evident. In HD-positive subjects, ERN amplitude deficits were significantly greater in younger individuals (r = -0.479, p = 0.018), whereas there were no significant ERN changes with increasing age in OCD and HC participants. Conclusions: The reduced ERN in HD relative to OCD and HC provides evidence that HD is neurobiologically distinct from OCD, and suggests that deficient error monitoring may be a core pathophysiological feature of HD. This effect was particularly prominent in younger HD participants, further suggesting that deficient error monitoring manifests most strongly early in the illness course and/or in individuals with a relatively early illness onset.
    Full-text · Article · Sep 2015 · Psychological Medicine
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    • "Event-related potential (ERP) studies have identified the error-related negativity (ERN), an initial negative ERP component following errors (Falkenstein et al. 1990), with maximal amplitude at fronto-central electrode sites (Gehring et al. 1993; Falkenstein et al. 2000). The ERN is generally associated with the unconscious awareness of error (Nieuwenhuis et al. 2001), although it has also been related to subjective appraisal of accuracy (Scheffers and Coles, 2000) and remedial action (Gehring et al. 1993; Debener et al. 2005). The error positivity (Pe) is a positive ERP component following the ERN and is maximal at parieto-central electrode sites (Falkenstein et al. 1991; Falkenstein et al. 2000). "
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    ABSTRACT: Metacognitive abnormalities have been implicated in the experience of psychotic symptoms; however, the process through which this occurs remains unclear. The aim of this study was to clarify the association of self-reported schizotypy with metacognitive beliefs and neural activity related to higher-order cognition. Event-related potentials (ERPs) including the error-related negativity (ERN) and error positivity (Pe) were recorded during a Flanker task in 20 controls and 22 individuals with high self-reported schizotypy on the Schizotypal Personality Questionnaire-Brief Revised (SPQ-BR). Participants continuously evaluated their task performance and completed the Metacognitions Questionnaire-30 (MCQ-30). The high schizotypy group demonstrated higher scores on all subscales of the MCQ-30. In contrast, task performance, accuracy of self-performance evaluation, and amplitudes of the ERN and Pe did not differ between groups. The MCQ-30 factors that measure cognitive confidence and positive beliefs about worry significantly predicted SPQ-BR total score, whereas ERPs did not. High self-reported schizotypy appears to be more associated with dysfunctional metacognitive beliefs than physiological abnormalities in brain areas related to metacognition.
    Full-text · Article · Sep 2015
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