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Mild traumatic brain injury impairs the coordination of intrinsic and motor-related neural dynamics

Mild traumatic brain injury (mTBI) poses a considerable burden on healthcare systems. Whilst most patients recover quickly, a significant number suffer from sequelae that are not accompanied by measurable structural damage. Understanding the neural underpinnings of these debilitating effects and dev...

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Autores principales: Rier, Lukas, Zamyadi, Rouzbeh, Zhang, Jing, Emami, Zahra, Seedat, Zelekha A., Mocanu, Sergiu, Gascoyne, Lauren E., Allen, Christopher M., Scadding, John W., Furlong, Paul L., Gooding-Williams, Gerard, Woolrich, Mark W., Evangelou, Nikos, Brookes, Matthew J., Dunkley, Benjamin T.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Elsevier 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8517919/
https://www.ncbi.nlm.nih.gov/pubmed/34653838
http://dx.doi.org/10.1016/j.nicl.2021.102841
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author Rier, Lukas
Zamyadi, Rouzbeh
Zhang, Jing
Emami, Zahra
Seedat, Zelekha A.
Mocanu, Sergiu
Gascoyne, Lauren E.
Allen, Christopher M.
Scadding, John W.
Furlong, Paul L.
Gooding-Williams, Gerard
Woolrich, Mark W.
Evangelou, Nikos
Brookes, Matthew J.
Dunkley, Benjamin T.
author_facet Rier, Lukas
Zamyadi, Rouzbeh
Zhang, Jing
Emami, Zahra
Seedat, Zelekha A.
Mocanu, Sergiu
Gascoyne, Lauren E.
Allen, Christopher M.
Scadding, John W.
Furlong, Paul L.
Gooding-Williams, Gerard
Woolrich, Mark W.
Evangelou, Nikos
Brookes, Matthew J.
Dunkley, Benjamin T.
author_sort Rier, Lukas
collection PubMed
description Mild traumatic brain injury (mTBI) poses a considerable burden on healthcare systems. Whilst most patients recover quickly, a significant number suffer from sequelae that are not accompanied by measurable structural damage. Understanding the neural underpinnings of these debilitating effects and developing a means to detect injury, would address an important unmet clinical need. It could inform interventions and help predict prognosis. Magnetoencephalography (MEG) affords excellent sensitivity in probing neural function and presents significant promise for assessing mTBI, with abnormal neural oscillations being a potential specific biomarker. However, growing evidence suggests that neural dynamics are (at least in part) driven by transient, pan-spectral bursting and in this paper, we employ this model to investigate mTBI. We applied a Hidden Markov Model to MEG data recorded during resting state and a motor task and show that previous findings of diminished intrinsic beta amplitude in individuals with mTBI are largely due to the reduced beta band spectral content of bursts, and that diminished beta connectivity results from a loss in the temporal coincidence of burst states. In a motor task, mTBI results in diminished burst amplitude, altered modulation of burst probability during movement, and a loss in connectivity in motor networks. These results suggest that, mechanistically, mTBI disrupts the structural framework underlying neural synchrony, which impairs network function. Whilst the damage may be too subtle for structural imaging to see, the functional consequences are detectable and persist after injury. Our work shows that mTBI impairs the dynamic coordination of neural network activity and proposes a potent new method for understanding mTBI.
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spelling pubmed-85179192021-10-21 Mild traumatic brain injury impairs the coordination of intrinsic and motor-related neural dynamics Rier, Lukas Zamyadi, Rouzbeh Zhang, Jing Emami, Zahra Seedat, Zelekha A. Mocanu, Sergiu Gascoyne, Lauren E. Allen, Christopher M. Scadding, John W. Furlong, Paul L. Gooding-Williams, Gerard Woolrich, Mark W. Evangelou, Nikos Brookes, Matthew J. Dunkley, Benjamin T. Neuroimage Clin Regular Article Mild traumatic brain injury (mTBI) poses a considerable burden on healthcare systems. Whilst most patients recover quickly, a significant number suffer from sequelae that are not accompanied by measurable structural damage. Understanding the neural underpinnings of these debilitating effects and developing a means to detect injury, would address an important unmet clinical need. It could inform interventions and help predict prognosis. Magnetoencephalography (MEG) affords excellent sensitivity in probing neural function and presents significant promise for assessing mTBI, with abnormal neural oscillations being a potential specific biomarker. However, growing evidence suggests that neural dynamics are (at least in part) driven by transient, pan-spectral bursting and in this paper, we employ this model to investigate mTBI. We applied a Hidden Markov Model to MEG data recorded during resting state and a motor task and show that previous findings of diminished intrinsic beta amplitude in individuals with mTBI are largely due to the reduced beta band spectral content of bursts, and that diminished beta connectivity results from a loss in the temporal coincidence of burst states. In a motor task, mTBI results in diminished burst amplitude, altered modulation of burst probability during movement, and a loss in connectivity in motor networks. These results suggest that, mechanistically, mTBI disrupts the structural framework underlying neural synchrony, which impairs network function. Whilst the damage may be too subtle for structural imaging to see, the functional consequences are detectable and persist after injury. Our work shows that mTBI impairs the dynamic coordination of neural network activity and proposes a potent new method for understanding mTBI. Elsevier 2021-10-01 /pmc/articles/PMC8517919/ /pubmed/34653838 http://dx.doi.org/10.1016/j.nicl.2021.102841 Text en © 2021 The Author(s) https://creativecommons.org/licenses/by/4.0/This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
spellingShingle Regular Article
Rier, Lukas
Zamyadi, Rouzbeh
Zhang, Jing
Emami, Zahra
Seedat, Zelekha A.
Mocanu, Sergiu
Gascoyne, Lauren E.
Allen, Christopher M.
Scadding, John W.
Furlong, Paul L.
Gooding-Williams, Gerard
Woolrich, Mark W.
Evangelou, Nikos
Brookes, Matthew J.
Dunkley, Benjamin T.
Mild traumatic brain injury impairs the coordination of intrinsic and motor-related neural dynamics
title Mild traumatic brain injury impairs the coordination of intrinsic and motor-related neural dynamics
title_full Mild traumatic brain injury impairs the coordination of intrinsic and motor-related neural dynamics
title_fullStr Mild traumatic brain injury impairs the coordination of intrinsic and motor-related neural dynamics
title_full_unstemmed Mild traumatic brain injury impairs the coordination of intrinsic and motor-related neural dynamics
title_short Mild traumatic brain injury impairs the coordination of intrinsic and motor-related neural dynamics
title_sort mild traumatic brain injury impairs the coordination of intrinsic and motor-related neural dynamics
topic Regular Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8517919/
https://www.ncbi.nlm.nih.gov/pubmed/34653838
http://dx.doi.org/10.1016/j.nicl.2021.102841
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