The effects of trauma on feedback processing: an MEG study

The cognitive impact of psychological trauma can manifest as a range of post-traumatic stress symptoms that are often attributed to impairments in learning from positive and negative outcomes, aka reinforcement learning. Research on the impact of trauma on reinforcement learning has mainly been inco...

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Main Authors: Abdulrahman S. Sawalma, Christian M. Kiefer, Frank Boers, N. Jon Shah, Nibal Khudeish, Irene Neuner, Mohammad M. Herzallah, Jürgen Dammers
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-11-01
Series:Frontiers in Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fnins.2023.1172549/full
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author Abdulrahman S. Sawalma
Abdulrahman S. Sawalma
Abdulrahman S. Sawalma
Christian M. Kiefer
Christian M. Kiefer
Frank Boers
N. Jon Shah
N. Jon Shah
N. Jon Shah
N. Jon Shah
Nibal Khudeish
Nibal Khudeish
Irene Neuner
Irene Neuner
Irene Neuner
Mohammad M. Herzallah
Mohammad M. Herzallah
Jürgen Dammers
Jürgen Dammers
author_facet Abdulrahman S. Sawalma
Abdulrahman S. Sawalma
Abdulrahman S. Sawalma
Christian M. Kiefer
Christian M. Kiefer
Frank Boers
N. Jon Shah
N. Jon Shah
N. Jon Shah
N. Jon Shah
Nibal Khudeish
Nibal Khudeish
Irene Neuner
Irene Neuner
Irene Neuner
Mohammad M. Herzallah
Mohammad M. Herzallah
Jürgen Dammers
Jürgen Dammers
author_sort Abdulrahman S. Sawalma
collection DOAJ
description The cognitive impact of psychological trauma can manifest as a range of post-traumatic stress symptoms that are often attributed to impairments in learning from positive and negative outcomes, aka reinforcement learning. Research on the impact of trauma on reinforcement learning has mainly been inconclusive. This study aimed to circumscribe the impact of psychological trauma on reinforcement learning in the context of neural response in time and frequency domains. Two groups of participants were tested - those who had experienced psychological trauma and a control group who had not - while they performed a probabilistic classification task that dissociates learning from positive and negative feedback during a magnetoencephalography (MEG) examination. While the exposure to trauma did not exhibit any effects on learning accuracy or response time for positive or negative feedback, MEG cortical activity was modulated in response to positive feedback. In particular, the medial and lateral orbitofrontal cortices (mOFC and lOFC) exhibited increased activity, while the insular and supramarginal cortices showed decreased activity during positive feedback presentation. Furthermore, when receiving negative feedback, the trauma group displayed higher activity in the medial portion of the superior frontal cortex. The timing of these activity changes occurred between 160 and 600 ms post feedback presentation. Analysis of the time-frequency domain revealed heightened activity in theta and alpha frequency bands (4–10 Hz) in the lOFC in the trauma group. Moreover, dividing the two groups according to their learning performance, the activity for the non-learner subgroup was found to be lower in lOFC and higher in the supramarginal cortex. These differences were found in the trauma group only. The results highlight the localization and neural dynamics of feedback processing that could be affected by exposure to psychological trauma. This approach and associated findings provide a novel framework for understanding the cognitive correlates of psychological trauma in relation to neural dynamics in the space, time, and frequency domains. Subsequent work will focus on the stratification of cognitive and neural correlates as a function of various symptoms of psychological trauma. Clinically, the study findings and approach open the possibility for neuromodulation interventions that synchronize cognitive and psychological constructs for individualized treatment.
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spelling doaj.art-59ae504fd4344cdd89e817248e46ec902023-11-02T09:29:19ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2023-11-011710.3389/fnins.2023.11725491172549The effects of trauma on feedback processing: an MEG studyAbdulrahman S. Sawalma0Abdulrahman S. Sawalma1Abdulrahman S. Sawalma2Christian M. Kiefer3Christian M. Kiefer4Frank Boers5N. Jon Shah6N. Jon Shah7N. Jon Shah8N. Jon Shah9Nibal Khudeish10Nibal Khudeish11Irene Neuner12Irene Neuner13Irene Neuner14Mohammad M. Herzallah15Mohammad M. Herzallah16Jürgen Dammers17Jürgen Dammers18Institute of Neuroscience and Medicine (INM-4), Forschungszentrum Jülich GmbH, Jülich, GermanyFaculty of Medicine, RWTH Aachen University, Aachen, GermanyPalestinian Neuroscience Initiative, Al-Quds University, Abu Dis, PalestineInstitute of Neuroscience and Medicine (INM-4), Forschungszentrum Jülich GmbH, Jülich, GermanyFaculty of Mathematics, Computer Science and Natural Sciences, RWTH Aachen University, Aachen, GermanyInstitute of Neuroscience and Medicine (INM-4), Forschungszentrum Jülich GmbH, Jülich, GermanyInstitute of Neuroscience and Medicine (INM-4), Forschungszentrum Jülich GmbH, Jülich, GermanyInstitute of Neuroscience and Medicine (INM-11), Jülich Aachen Research Alliance (JARA), Forschungszentrum Jülich GmbH, Jülich, GermanyJülich Aachen Research Alliance (JARA)-Brain – Translational Medicine, Aachen, GermanyDepartment of Neurology, University Hospital RWTH Aachen, Aachen, GermanyInstitute of Neuroscience and Medicine (INM-4), Forschungszentrum Jülich GmbH, Jülich, GermanyFaculty of Medicine, RWTH Aachen University, Aachen, GermanyInstitute of Neuroscience and Medicine (INM-4), Forschungszentrum Jülich GmbH, Jülich, GermanyJülich Aachen Research Alliance (JARA)-Brain – Translational Medicine, Aachen, GermanyDepartment of Psychiatry, Psychotherapy and Psychosomatics, RWTH Aachen University, Aachen, GermanyPalestinian Neuroscience Initiative, Al-Quds University, Abu Dis, PalestineCenter for Molecular and Behavioral Neuroscience, Rutgers University, Newark, NJ, United StatesInstitute of Neuroscience and Medicine (INM-4), Forschungszentrum Jülich GmbH, Jülich, GermanyFaculty of Medicine, RWTH Aachen University, Aachen, GermanyThe cognitive impact of psychological trauma can manifest as a range of post-traumatic stress symptoms that are often attributed to impairments in learning from positive and negative outcomes, aka reinforcement learning. Research on the impact of trauma on reinforcement learning has mainly been inconclusive. This study aimed to circumscribe the impact of psychological trauma on reinforcement learning in the context of neural response in time and frequency domains. Two groups of participants were tested - those who had experienced psychological trauma and a control group who had not - while they performed a probabilistic classification task that dissociates learning from positive and negative feedback during a magnetoencephalography (MEG) examination. While the exposure to trauma did not exhibit any effects on learning accuracy or response time for positive or negative feedback, MEG cortical activity was modulated in response to positive feedback. In particular, the medial and lateral orbitofrontal cortices (mOFC and lOFC) exhibited increased activity, while the insular and supramarginal cortices showed decreased activity during positive feedback presentation. Furthermore, when receiving negative feedback, the trauma group displayed higher activity in the medial portion of the superior frontal cortex. The timing of these activity changes occurred between 160 and 600 ms post feedback presentation. Analysis of the time-frequency domain revealed heightened activity in theta and alpha frequency bands (4–10 Hz) in the lOFC in the trauma group. Moreover, dividing the two groups according to their learning performance, the activity for the non-learner subgroup was found to be lower in lOFC and higher in the supramarginal cortex. These differences were found in the trauma group only. The results highlight the localization and neural dynamics of feedback processing that could be affected by exposure to psychological trauma. This approach and associated findings provide a novel framework for understanding the cognitive correlates of psychological trauma in relation to neural dynamics in the space, time, and frequency domains. Subsequent work will focus on the stratification of cognitive and neural correlates as a function of various symptoms of psychological trauma. Clinically, the study findings and approach open the possibility for neuromodulation interventions that synchronize cognitive and psychological constructs for individualized treatment.https://www.frontiersin.org/articles/10.3389/fnins.2023.1172549/fulltraumaPTSDmagnetoencephalographyfeedback-based learningspatio-temporal cluster permutation test
spellingShingle Abdulrahman S. Sawalma
Abdulrahman S. Sawalma
Abdulrahman S. Sawalma
Christian M. Kiefer
Christian M. Kiefer
Frank Boers
N. Jon Shah
N. Jon Shah
N. Jon Shah
N. Jon Shah
Nibal Khudeish
Nibal Khudeish
Irene Neuner
Irene Neuner
Irene Neuner
Mohammad M. Herzallah
Mohammad M. Herzallah
Jürgen Dammers
Jürgen Dammers
The effects of trauma on feedback processing: an MEG study
Frontiers in Neuroscience
trauma
PTSD
magnetoencephalography
feedback-based learning
spatio-temporal cluster permutation test
title The effects of trauma on feedback processing: an MEG study
title_full The effects of trauma on feedback processing: an MEG study
title_fullStr The effects of trauma on feedback processing: an MEG study
title_full_unstemmed The effects of trauma on feedback processing: an MEG study
title_short The effects of trauma on feedback processing: an MEG study
title_sort effects of trauma on feedback processing an meg study
topic trauma
PTSD
magnetoencephalography
feedback-based learning
spatio-temporal cluster permutation test
url https://www.frontiersin.org/articles/10.3389/fnins.2023.1172549/full
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