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

TY - JOUR

T1 - Simultaneous EEG-fMRI reveals theta network alterations during reward feedback processing in borderline personality disorder

AU - Schauer, Paul A

AU - Rauh, Jonas

AU - Biedermann, Sarah V

AU - Haaf, Moritz

AU - Steinmann, Saskia

AU - Leicht, Gregor

AU - Mulert, Christoph

N1 - © 2021. The Author(s).

PY - 2021/8/30

Y1 - 2021/8/30

N2 - 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.

AB - 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.

KW - Adult

KW - Borderline Personality Disorder/diagnostic imaging

KW - Brain/diagnostic imaging

KW - Brain Mapping

KW - Case-Control Studies

KW - Electroencephalography/methods

KW - Feedback

KW - Female

KW - Gambling/diagnostic imaging

KW - Humans

KW - Impulsive Behavior/physiology

KW - Magnetic Resonance Imaging/methods

KW - Male

KW - Oscillometry

KW - Prefrontal Cortex/diagnostic imaging

KW - Probability

KW - Reward

KW - Signal Processing, Computer-Assisted

KW - Theta Rhythm

U2 - 10.1038/s41598-021-96209-7

DO - 10.1038/s41598-021-96209-7

M3 - SCORING: Journal article

C2 - 34462449

VL - 11

JO - SCI REP-UK

JF - SCI REP-UK

SN - 2045-2322

IS - 1

M1 - 17336

ER -