Simultaneous EEG-fMRI reveals theta network alterations during reward feedback processing in borderline personality disorder

Abstract Previous studies using imaging techniques such as electroencephalography (EEG) or functional magnetic resonance imaging (fMRI) have identified neurophysiological markers of impaired feedback processing in patients with Borderline Personality Disorder (BPD). These mainly include reduced osci...

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Main Authors: Paul A. Schauer, Jonas Rauh, Sarah V. Biedermann, Moritz Haaf, Saskia Steinmann, Gregor Leicht, Christoph Mulert
Format: Article
Language:English
Published: Nature Portfolio 2021-08-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-021-96209-7
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author Paul A. Schauer
Jonas Rauh
Sarah V. Biedermann
Moritz Haaf
Saskia Steinmann
Gregor Leicht
Christoph Mulert
author_facet Paul A. Schauer
Jonas Rauh
Sarah V. Biedermann
Moritz Haaf
Saskia Steinmann
Gregor Leicht
Christoph Mulert
author_sort Paul A. Schauer
collection DOAJ
description Abstract Previous studies using imaging techniques such as electroencephalography (EEG) or functional magnetic resonance imaging (fMRI) have identified neurophysiological markers of impaired feedback processing in patients with Borderline Personality Disorder (BPD). These mainly include reduced oscillatory activity in the theta frequency range in the EEG and altered activations in frontal and striatal regions in fMRI studies. The aim of the present study is to integrate these results using a coupling of simultaneously recorded EEG and fMRI. Simultaneous EEG (64-channel) and fMRI (3-Tesla Siemens Prisma) was recorded whilst participants (19 BPD patients and 18 controls) performed a gambling task. Data was analysed for the two imaging techniques separately as well as in a single-trial coupling of both modalities. Evoked theta oscillatory power as a response to loss feedback was reduced in BPD patients. EEG-fMRI coupling revealed an interaction between feedback valence and group in prefrontal regions centering in the dorsolateral prefrontal cortex (dlPFC), with healthy controls showing stronger modulation by theta responses during loss when compared to gain feedback and the opposite effect in BPD patients. Our results show multiple alterations in the processing of feedback in BPD, which were partly linked to impulsivity. The dlPFC was identified as the seed of theta-associated activation differences.
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spelling doaj.art-0860e531bc0b461da5b56d12d45934582022-12-21T22:59:47ZengNature PortfolioScientific Reports2045-23222021-08-0111111010.1038/s41598-021-96209-7Simultaneous EEG-fMRI reveals theta network alterations during reward feedback processing in borderline personality disorderPaul A. Schauer0Jonas Rauh1Sarah V. Biedermann2Moritz Haaf3Saskia Steinmann4Gregor Leicht5Christoph Mulert6Psychiatry Neuroimaging Branch, Department of Psychiatry and Psychotherapy, Center of Psychosocial Medicine, University Medical Center Hamburg-EppendorfPsychiatry Neuroimaging Branch, Department of Psychiatry and Psychotherapy, Center of Psychosocial Medicine, University Medical Center Hamburg-EppendorfDepartment of Psychiatry and Psychotherapy, Center of Psychosocial Medicine, University Medical Center Hamburg-EppendorfPsychiatry Neuroimaging Branch, Department of Psychiatry and Psychotherapy, Center of Psychosocial Medicine, University Medical Center Hamburg-EppendorfPsychiatry Neuroimaging Branch, Department of Psychiatry and Psychotherapy, Center of Psychosocial Medicine, University Medical Center Hamburg-EppendorfPsychiatry Neuroimaging Branch, Department of Psychiatry and Psychotherapy, Center of Psychosocial Medicine, University Medical Center Hamburg-EppendorfPsychiatry Neuroimaging Branch, Department of Psychiatry and Psychotherapy, Center of Psychosocial Medicine, University Medical Center Hamburg-EppendorfAbstract Previous studies using imaging techniques such as electroencephalography (EEG) or functional magnetic resonance imaging (fMRI) have identified neurophysiological markers of impaired feedback processing in patients with Borderline Personality Disorder (BPD). These mainly include reduced oscillatory activity in the theta frequency range in the EEG and altered activations in frontal and striatal regions in fMRI studies. The aim of the present study is to integrate these results using a coupling of simultaneously recorded EEG and fMRI. Simultaneous EEG (64-channel) and fMRI (3-Tesla Siemens Prisma) was recorded whilst participants (19 BPD patients and 18 controls) performed a gambling task. Data was analysed for the two imaging techniques separately as well as in a single-trial coupling of both modalities. Evoked theta oscillatory power as a response to loss feedback was reduced in BPD patients. EEG-fMRI coupling revealed an interaction between feedback valence and group in prefrontal regions centering in the dorsolateral prefrontal cortex (dlPFC), with healthy controls showing stronger modulation by theta responses during loss when compared to gain feedback and the opposite effect in BPD patients. Our results show multiple alterations in the processing of feedback in BPD, which were partly linked to impulsivity. The dlPFC was identified as the seed of theta-associated activation differences.https://doi.org/10.1038/s41598-021-96209-7
spellingShingle Paul A. Schauer
Jonas Rauh
Sarah V. Biedermann
Moritz Haaf
Saskia Steinmann
Gregor Leicht
Christoph Mulert
Simultaneous EEG-fMRI reveals theta network alterations during reward feedback processing in borderline personality disorder
Scientific Reports
title Simultaneous EEG-fMRI reveals theta network alterations during reward feedback processing in borderline personality disorder
title_full Simultaneous EEG-fMRI reveals theta network alterations during reward feedback processing in borderline personality disorder
title_fullStr Simultaneous EEG-fMRI reveals theta network alterations during reward feedback processing in borderline personality disorder
title_full_unstemmed Simultaneous EEG-fMRI reveals theta network alterations during reward feedback processing in borderline personality disorder
title_short Simultaneous EEG-fMRI reveals theta network alterations during reward feedback processing in borderline personality disorder
title_sort simultaneous eeg fmri reveals theta network alterations during reward feedback processing in borderline personality disorder
url https://doi.org/10.1038/s41598-021-96209-7
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