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Aberrant error processing in relation to symptom severity in obsessive–compulsive disorder: A multimodal neuroimaging study

BACKGROUND: Obsessive–compulsive disorder (OCD) is characterized by maladaptive repetitive behaviors that persist despite feedback. Using multimodal neuroimaging, we tested the hypothesis that this behavioral rigidity reflects impaired use of behavioral outcomes (here, errors) to adaptively adjust r...

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Autores principales: Agam, Yigal, Greenberg, Jennifer L., Isom, Marlisa, Falkenstein, Martha J., Jenike, Eric, Wilhelm, Sabine, Manoach, Dara S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Elsevier 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4096999/
https://www.ncbi.nlm.nih.gov/pubmed/25057466
http://dx.doi.org/10.1016/j.nicl.2014.06.002
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author Agam, Yigal
Greenberg, Jennifer L.
Isom, Marlisa
Falkenstein, Martha J.
Jenike, Eric
Wilhelm, Sabine
Manoach, Dara S.
author_facet Agam, Yigal
Greenberg, Jennifer L.
Isom, Marlisa
Falkenstein, Martha J.
Jenike, Eric
Wilhelm, Sabine
Manoach, Dara S.
author_sort Agam, Yigal
collection PubMed
description BACKGROUND: Obsessive–compulsive disorder (OCD) is characterized by maladaptive repetitive behaviors that persist despite feedback. Using multimodal neuroimaging, we tested the hypothesis that this behavioral rigidity reflects impaired use of behavioral outcomes (here, errors) to adaptively adjust responses. We measured both neural responses to errors and adjustments in the subsequent trial to determine whether abnormalities correlate with symptom severity. Since error processing depends on communication between the anterior and the posterior cingulate cortex, we also examined the integrity of the cingulum bundle with diffusion tensor imaging. METHODS: Participants performed the same antisaccade task during functional MRI and electroencephalography sessions. We measured error-related activation of the anterior cingulate cortex (ACC) and the error-related negativity (ERN). We also examined post-error adjustments, indexed by changes in activation of the default network in trials surrounding errors. RESULTS: OCD patients showed intact error-related ACC activation and ERN, but abnormal adjustments in the post- vs. pre-error trial. Relative to controls, who responded to errors by deactivating the default network, OCD patients showed increased default network activation including in the rostral ACC (rACC). Greater rACC activation in the post-error trial correlated with more severe compulsions. Patients also showed increased fractional anisotropy (FA) in the white matter underlying rACC. CONCLUSIONS: Impaired use of behavioral outcomes to adaptively adjust neural responses may contribute to symptoms in OCD. The rACC locus of abnormal adjustment and relations with symptoms suggests difficulty suppressing emotional responses to aversive, unexpected events (e.g., errors). Increased structural connectivity of this paralimbic default network region may contribute to this impairment.
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spelling pubmed-40969992014-07-23 Aberrant error processing in relation to symptom severity in obsessive–compulsive disorder: A multimodal neuroimaging study Agam, Yigal Greenberg, Jennifer L. Isom, Marlisa Falkenstein, Martha J. Jenike, Eric Wilhelm, Sabine Manoach, Dara S. Neuroimage Clin Article BACKGROUND: Obsessive–compulsive disorder (OCD) is characterized by maladaptive repetitive behaviors that persist despite feedback. Using multimodal neuroimaging, we tested the hypothesis that this behavioral rigidity reflects impaired use of behavioral outcomes (here, errors) to adaptively adjust responses. We measured both neural responses to errors and adjustments in the subsequent trial to determine whether abnormalities correlate with symptom severity. Since error processing depends on communication between the anterior and the posterior cingulate cortex, we also examined the integrity of the cingulum bundle with diffusion tensor imaging. METHODS: Participants performed the same antisaccade task during functional MRI and electroencephalography sessions. We measured error-related activation of the anterior cingulate cortex (ACC) and the error-related negativity (ERN). We also examined post-error adjustments, indexed by changes in activation of the default network in trials surrounding errors. RESULTS: OCD patients showed intact error-related ACC activation and ERN, but abnormal adjustments in the post- vs. pre-error trial. Relative to controls, who responded to errors by deactivating the default network, OCD patients showed increased default network activation including in the rostral ACC (rACC). Greater rACC activation in the post-error trial correlated with more severe compulsions. Patients also showed increased fractional anisotropy (FA) in the white matter underlying rACC. CONCLUSIONS: Impaired use of behavioral outcomes to adaptively adjust neural responses may contribute to symptoms in OCD. The rACC locus of abnormal adjustment and relations with symptoms suggests difficulty suppressing emotional responses to aversive, unexpected events (e.g., errors). Increased structural connectivity of this paralimbic default network region may contribute to this impairment. Elsevier 2014-06-17 /pmc/articles/PMC4096999/ /pubmed/25057466 http://dx.doi.org/10.1016/j.nicl.2014.06.002 Text en © 2014 The Authors. Published by Elsevier Inc. All rights reserved. http://creativecommons.org/licenses/by-nc-nd/3.0/ This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/3.0/).
spellingShingle Article
Agam, Yigal
Greenberg, Jennifer L.
Isom, Marlisa
Falkenstein, Martha J.
Jenike, Eric
Wilhelm, Sabine
Manoach, Dara S.
Aberrant error processing in relation to symptom severity in obsessive–compulsive disorder: A multimodal neuroimaging study
title Aberrant error processing in relation to symptom severity in obsessive–compulsive disorder: A multimodal neuroimaging study
title_full Aberrant error processing in relation to symptom severity in obsessive–compulsive disorder: A multimodal neuroimaging study
title_fullStr Aberrant error processing in relation to symptom severity in obsessive–compulsive disorder: A multimodal neuroimaging study
title_full_unstemmed Aberrant error processing in relation to symptom severity in obsessive–compulsive disorder: A multimodal neuroimaging study
title_short Aberrant error processing in relation to symptom severity in obsessive–compulsive disorder: A multimodal neuroimaging study
title_sort aberrant error processing in relation to symptom severity in obsessive–compulsive disorder: a multimodal neuroimaging study
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4096999/
https://www.ncbi.nlm.nih.gov/pubmed/25057466
http://dx.doi.org/10.1016/j.nicl.2014.06.002
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