Posterior cingulate cortex targeted real‐time fMRI neurofeedback recalibrates functional connectivity with the amygdala, posterior insula, and default‐mode network in PTSD
Abstract Background Alterations within large‐scale brain networks—namely, the default mode (DMN) and salience networks (SN)—are present among individuals with posttraumatic stress disorder (PTSD). Previous real‐time functional magnetic resonance imaging (fMRI) and electroencephalography neurofeedbac...
Main Authors: | , , , , , , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
Wiley
2023-03-01
|
Series: | Brain and Behavior |
Subjects: | |
Online Access: | https://doi.org/10.1002/brb3.2883 |
_version_ | 1797870950197231616 |
---|---|
author | Jonathan M. Lieberman Daniela Rabellino Maria Densmore Paul A. Frewen David Steyrl Frank Scharnowski Jean Théberge Richard W. J. Neufeld Christian Schmahl Rakesh Jetly Sandhya Narikuzhy Ruth A. Lanius Andrew A. Nicholson |
author_facet | Jonathan M. Lieberman Daniela Rabellino Maria Densmore Paul A. Frewen David Steyrl Frank Scharnowski Jean Théberge Richard W. J. Neufeld Christian Schmahl Rakesh Jetly Sandhya Narikuzhy Ruth A. Lanius Andrew A. Nicholson |
author_sort | Jonathan M. Lieberman |
collection | DOAJ |
description | Abstract Background Alterations within large‐scale brain networks—namely, the default mode (DMN) and salience networks (SN)—are present among individuals with posttraumatic stress disorder (PTSD). Previous real‐time functional magnetic resonance imaging (fMRI) and electroencephalography neurofeedback studies suggest that regulating posterior cingulate cortex (PCC; the primary hub of the posterior DMN) activity may reduce PTSD symptoms and recalibrate altered network dynamics. However, PCC connectivity to the DMN and SN during PCC‐targeted fMRI neurofeedback remains unexamined and may help to elucidate neurophysiological mechanisms through which these symptom improvements may occur. Methods Using a trauma/emotion provocation paradigm, we investigated psychophysiological interactions over a single session of neurofeedback among PTSD (n = 14) and healthy control (n = 15) participants. We compared PCC functional connectivity between regulate (in which participants downregulated PCC activity) and view (in which participants did not exert regulatory control) conditions across the whole‐brain as well as in a priori specified regions‐of‐interest. Results During regulate as compared to view conditions, only the PTSD group showed significant PCC connectivity with anterior DMN (dmPFC, vmPFC) and SN (posterior insula) regions, whereas both groups displayed PCC connectivity with other posterior DMN areas (precuneus/cuneus). Additionally, as compared with controls, the PTSD group showed significantly greater PCC connectivity with the SN (amygdala) during regulate as compared to view conditions. Moreover, linear regression analyses revealed that during regulate as compared to view conditions, PCC connectivity to DMN and SN regions was positively correlated to psychiatric symptoms across all participants. Conclusion In summary, observations of PCC connectivity to the DMN and SN provide emerging evidence of neural mechanisms underlying PCC‐targeted fMRI neurofeedback among individuals with PTSD. This supports the use of PCC‐targeted neurofeedback as a means by which to recalibrate PTSD‐associated alterations in neural connectivity within the DMN and SN, which together, may help to facilitate improved emotion regulation abilities in PTSD. |
first_indexed | 2024-04-10T00:35:25Z |
format | Article |
id | doaj.art-95425af0578844d4af9956d1c095e36c |
institution | Directory Open Access Journal |
issn | 2162-3279 |
language | English |
last_indexed | 2024-04-10T00:35:25Z |
publishDate | 2023-03-01 |
publisher | Wiley |
record_format | Article |
series | Brain and Behavior |
spelling | doaj.art-95425af0578844d4af9956d1c095e36c2023-03-14T17:46:48ZengWileyBrain and Behavior2162-32792023-03-01133n/an/a10.1002/brb3.2883Posterior cingulate cortex targeted real‐time fMRI neurofeedback recalibrates functional connectivity with the amygdala, posterior insula, and default‐mode network in PTSDJonathan M. Lieberman0Daniela Rabellino1Maria Densmore2Paul A. Frewen3David Steyrl4Frank Scharnowski5Jean Théberge6Richard W. J. Neufeld7Christian Schmahl8Rakesh Jetly9Sandhya Narikuzhy10Ruth A. Lanius11Andrew A. Nicholson12Department of Psychiatry and Behavioural NeurosciencesMcMaster University HamiltonOntarioCanadaImaging, Lawson Health Research Institute LondonOntarioCanadaImaging, Lawson Health Research Institute LondonOntarioCanadaDepartment of NeuroscienceWestern University LondonOntarioCanadaDepartment of Cognition, Emotion, and Methods in PsychologyUniversity of Vienna ViennaAustriaDepartment of Cognition, Emotion, and Methods in PsychologyUniversity of Vienna ViennaAustriaImaging, Lawson Health Research Institute LondonOntarioCanadaDepartment of NeuroscienceWestern University LondonOntarioCanadaDepartment of Psychosomatic Medicine and PsychotherapyCentral Institute of Mental Health MannheimHeidelberg University HeidelbergGermanyThe Institute of Mental Health ResearchUniversity of Ottawa, Royal Ottawa Hospital OntarioCanadaDepartment of Psychiatry and Behavioural NeurosciencesMcMaster University HamiltonOntarioCanadaImaging, Lawson Health Research Institute LondonOntarioCanadaDepartment of Psychiatry and Behavioural NeurosciencesMcMaster University HamiltonOntarioCanadaAbstract Background Alterations within large‐scale brain networks—namely, the default mode (DMN) and salience networks (SN)—are present among individuals with posttraumatic stress disorder (PTSD). Previous real‐time functional magnetic resonance imaging (fMRI) and electroencephalography neurofeedback studies suggest that regulating posterior cingulate cortex (PCC; the primary hub of the posterior DMN) activity may reduce PTSD symptoms and recalibrate altered network dynamics. However, PCC connectivity to the DMN and SN during PCC‐targeted fMRI neurofeedback remains unexamined and may help to elucidate neurophysiological mechanisms through which these symptom improvements may occur. Methods Using a trauma/emotion provocation paradigm, we investigated psychophysiological interactions over a single session of neurofeedback among PTSD (n = 14) and healthy control (n = 15) participants. We compared PCC functional connectivity between regulate (in which participants downregulated PCC activity) and view (in which participants did not exert regulatory control) conditions across the whole‐brain as well as in a priori specified regions‐of‐interest. Results During regulate as compared to view conditions, only the PTSD group showed significant PCC connectivity with anterior DMN (dmPFC, vmPFC) and SN (posterior insula) regions, whereas both groups displayed PCC connectivity with other posterior DMN areas (precuneus/cuneus). Additionally, as compared with controls, the PTSD group showed significantly greater PCC connectivity with the SN (amygdala) during regulate as compared to view conditions. Moreover, linear regression analyses revealed that during regulate as compared to view conditions, PCC connectivity to DMN and SN regions was positively correlated to psychiatric symptoms across all participants. Conclusion In summary, observations of PCC connectivity to the DMN and SN provide emerging evidence of neural mechanisms underlying PCC‐targeted fMRI neurofeedback among individuals with PTSD. This supports the use of PCC‐targeted neurofeedback as a means by which to recalibrate PTSD‐associated alterations in neural connectivity within the DMN and SN, which together, may help to facilitate improved emotion regulation abilities in PTSD.https://doi.org/10.1002/brb3.2883default mode networkfMRI neurofeedbackposterior cingulate cortexposttraumatic stress disorder |
spellingShingle | Jonathan M. Lieberman Daniela Rabellino Maria Densmore Paul A. Frewen David Steyrl Frank Scharnowski Jean Théberge Richard W. J. Neufeld Christian Schmahl Rakesh Jetly Sandhya Narikuzhy Ruth A. Lanius Andrew A. Nicholson Posterior cingulate cortex targeted real‐time fMRI neurofeedback recalibrates functional connectivity with the amygdala, posterior insula, and default‐mode network in PTSD Brain and Behavior default mode network fMRI neurofeedback posterior cingulate cortex posttraumatic stress disorder |
title | Posterior cingulate cortex targeted real‐time fMRI neurofeedback recalibrates functional connectivity with the amygdala, posterior insula, and default‐mode network in PTSD |
title_full | Posterior cingulate cortex targeted real‐time fMRI neurofeedback recalibrates functional connectivity with the amygdala, posterior insula, and default‐mode network in PTSD |
title_fullStr | Posterior cingulate cortex targeted real‐time fMRI neurofeedback recalibrates functional connectivity with the amygdala, posterior insula, and default‐mode network in PTSD |
title_full_unstemmed | Posterior cingulate cortex targeted real‐time fMRI neurofeedback recalibrates functional connectivity with the amygdala, posterior insula, and default‐mode network in PTSD |
title_short | Posterior cingulate cortex targeted real‐time fMRI neurofeedback recalibrates functional connectivity with the amygdala, posterior insula, and default‐mode network in PTSD |
title_sort | posterior cingulate cortex targeted real time fmri neurofeedback recalibrates functional connectivity with the amygdala posterior insula and default mode network in ptsd |
topic | default mode network fMRI neurofeedback posterior cingulate cortex posttraumatic stress disorder |
url | https://doi.org/10.1002/brb3.2883 |
work_keys_str_mv | AT jonathanmlieberman posteriorcingulatecortextargetedrealtimefmrineurofeedbackrecalibratesfunctionalconnectivitywiththeamygdalaposteriorinsulaanddefaultmodenetworkinptsd AT danielarabellino posteriorcingulatecortextargetedrealtimefmrineurofeedbackrecalibratesfunctionalconnectivitywiththeamygdalaposteriorinsulaanddefaultmodenetworkinptsd AT mariadensmore posteriorcingulatecortextargetedrealtimefmrineurofeedbackrecalibratesfunctionalconnectivitywiththeamygdalaposteriorinsulaanddefaultmodenetworkinptsd AT paulafrewen posteriorcingulatecortextargetedrealtimefmrineurofeedbackrecalibratesfunctionalconnectivitywiththeamygdalaposteriorinsulaanddefaultmodenetworkinptsd AT davidsteyrl posteriorcingulatecortextargetedrealtimefmrineurofeedbackrecalibratesfunctionalconnectivitywiththeamygdalaposteriorinsulaanddefaultmodenetworkinptsd AT frankscharnowski posteriorcingulatecortextargetedrealtimefmrineurofeedbackrecalibratesfunctionalconnectivitywiththeamygdalaposteriorinsulaanddefaultmodenetworkinptsd AT jeantheberge posteriorcingulatecortextargetedrealtimefmrineurofeedbackrecalibratesfunctionalconnectivitywiththeamygdalaposteriorinsulaanddefaultmodenetworkinptsd AT richardwjneufeld posteriorcingulatecortextargetedrealtimefmrineurofeedbackrecalibratesfunctionalconnectivitywiththeamygdalaposteriorinsulaanddefaultmodenetworkinptsd AT christianschmahl posteriorcingulatecortextargetedrealtimefmrineurofeedbackrecalibratesfunctionalconnectivitywiththeamygdalaposteriorinsulaanddefaultmodenetworkinptsd AT rakeshjetly posteriorcingulatecortextargetedrealtimefmrineurofeedbackrecalibratesfunctionalconnectivitywiththeamygdalaposteriorinsulaanddefaultmodenetworkinptsd AT sandhyanarikuzhy posteriorcingulatecortextargetedrealtimefmrineurofeedbackrecalibratesfunctionalconnectivitywiththeamygdalaposteriorinsulaanddefaultmodenetworkinptsd AT ruthalanius posteriorcingulatecortextargetedrealtimefmrineurofeedbackrecalibratesfunctionalconnectivitywiththeamygdalaposteriorinsulaanddefaultmodenetworkinptsd AT andrewanicholson posteriorcingulatecortextargetedrealtimefmrineurofeedbackrecalibratesfunctionalconnectivitywiththeamygdalaposteriorinsulaanddefaultmodenetworkinptsd |