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Functional brain networks assessed with surface electroencephalography for predicting motor recovery in a neural guided intervention for chronic stroke

Predicting whether a chronic stroke patient is likely to benefit from a specific intervention can help patients establish reasonable expectations. It also provides the basis for candidates selecting for the intervention. Recent convergent evidence supports the value of network-based approach for und...

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Autores principales: Sun, Rui, Wong, Wan-Wa, Wang, Jing, Wang, Xin, Tong, Raymond K Y
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8936428/
https://www.ncbi.nlm.nih.gov/pubmed/35350709
http://dx.doi.org/10.1093/braincomms/fcab214
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author Sun, Rui
Wong, Wan-Wa
Wang, Jing
Wang, Xin
Tong, Raymond K Y
author_facet Sun, Rui
Wong, Wan-Wa
Wang, Jing
Wang, Xin
Tong, Raymond K Y
author_sort Sun, Rui
collection PubMed
description Predicting whether a chronic stroke patient is likely to benefit from a specific intervention can help patients establish reasonable expectations. It also provides the basis for candidates selecting for the intervention. Recent convergent evidence supports the value of network-based approach for understanding the relationship between dysfunctional neural activity and motor deficits after stroke. In this study, we applied resting-state brain connectivity networks to investigate intervention-specific predictive biomarkers of motor improvement in 22 chronic stroke participants who received either combined action observation with EEG-guided robot-hand training (Neural Guided-Action Observation Group, n = 12, age: 34–68 years) or robot-hand training without action observation and EEG guidance (non-Neural Guided-text group, n = 10, age: 42–57 years). The robot hand in Neural Guided-Action Observation training was activated only when significant mu suppression (8–12 Hz) was detected from participant’s EEG signals in ipsilesional hemisphere while it was randomly activated in non-Neural Guided-text training. Only the Neural Guided-Action Observation group showed a significant long-term improvement in their upper-limb motor functions (P < 0.5). In contrast, no significant training effect on the paretic motor functions was found in the non-Neural Guided-text group (P > 0.5). The results of brain connectivity estimated via EEG coherence showed that the pre-training interhemispheric connectivity of delta, theta, alpha and contralesional connectivity of beta were motor improvement related in the Neural Guided-Action Observation group. They can not only differentiate participants with good and poor recovery (interhemispheric delta: P = 0.047, Hedges’ g = 1.409; interhemispheric theta: P = 0.046, Hedges’ g = 1.333; interhemispheric alpha: P = 0.038, Hedges’ g = 1.536; contralesional beta: P = 0.027, Hedges’ g = 1.613) but also significantly correlated with post-training intervention gains (interhemispheric delta: r = −0.901, P < 0.05; interhemispheric theta: r = −0.702, P < 0.05; interhemispheric alpha: r = −0.641, P < 0.05; contralesional beta: r = −0.729, P < 0.05). In contrast, no EEG coherence was significantly correlated with intervention gains in the non-Neural Guided-text group (all [Formula: see text]). Partial least square regression showed that the combination of pre-training interhemispheric and contralesional local connectivity could precisely predict intervention gains in the Neural Guided-Action Observation group with a strong correlation between predicted and observed intervention gains (r = 0.82 [Formula: see text]) and between predicted and observed intervention outcomes (r = 0.90 [Formula: see text]). In summary, EEG-based resting-state brain connectivity networks may serve clinical decision-making by offering an approach to predicting Neural Guided-Action Observation training-induced motor improvement.
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spelling pubmed-89364282022-03-28 Functional brain networks assessed with surface electroencephalography for predicting motor recovery in a neural guided intervention for chronic stroke Sun, Rui Wong, Wan-Wa Wang, Jing Wang, Xin Tong, Raymond K Y Brain Commun Original Article Predicting whether a chronic stroke patient is likely to benefit from a specific intervention can help patients establish reasonable expectations. It also provides the basis for candidates selecting for the intervention. Recent convergent evidence supports the value of network-based approach for understanding the relationship between dysfunctional neural activity and motor deficits after stroke. In this study, we applied resting-state brain connectivity networks to investigate intervention-specific predictive biomarkers of motor improvement in 22 chronic stroke participants who received either combined action observation with EEG-guided robot-hand training (Neural Guided-Action Observation Group, n = 12, age: 34–68 years) or robot-hand training without action observation and EEG guidance (non-Neural Guided-text group, n = 10, age: 42–57 years). The robot hand in Neural Guided-Action Observation training was activated only when significant mu suppression (8–12 Hz) was detected from participant’s EEG signals in ipsilesional hemisphere while it was randomly activated in non-Neural Guided-text training. Only the Neural Guided-Action Observation group showed a significant long-term improvement in their upper-limb motor functions (P < 0.5). In contrast, no significant training effect on the paretic motor functions was found in the non-Neural Guided-text group (P > 0.5). The results of brain connectivity estimated via EEG coherence showed that the pre-training interhemispheric connectivity of delta, theta, alpha and contralesional connectivity of beta were motor improvement related in the Neural Guided-Action Observation group. They can not only differentiate participants with good and poor recovery (interhemispheric delta: P = 0.047, Hedges’ g = 1.409; interhemispheric theta: P = 0.046, Hedges’ g = 1.333; interhemispheric alpha: P = 0.038, Hedges’ g = 1.536; contralesional beta: P = 0.027, Hedges’ g = 1.613) but also significantly correlated with post-training intervention gains (interhemispheric delta: r = −0.901, P < 0.05; interhemispheric theta: r = −0.702, P < 0.05; interhemispheric alpha: r = −0.641, P < 0.05; contralesional beta: r = −0.729, P < 0.05). In contrast, no EEG coherence was significantly correlated with intervention gains in the non-Neural Guided-text group (all [Formula: see text]). Partial least square regression showed that the combination of pre-training interhemispheric and contralesional local connectivity could precisely predict intervention gains in the Neural Guided-Action Observation group with a strong correlation between predicted and observed intervention gains (r = 0.82 [Formula: see text]) and between predicted and observed intervention outcomes (r = 0.90 [Formula: see text]). In summary, EEG-based resting-state brain connectivity networks may serve clinical decision-making by offering an approach to predicting Neural Guided-Action Observation training-induced motor improvement. Oxford University Press 2021-09-25 /pmc/articles/PMC8936428/ /pubmed/35350709 http://dx.doi.org/10.1093/braincomms/fcab214 Text en © The Author(s) (2021). Published by Oxford University Press on behalf of the Guarantors of Brain. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Original Article
Sun, Rui
Wong, Wan-Wa
Wang, Jing
Wang, Xin
Tong, Raymond K Y
Functional brain networks assessed with surface electroencephalography for predicting motor recovery in a neural guided intervention for chronic stroke
title Functional brain networks assessed with surface electroencephalography for predicting motor recovery in a neural guided intervention for chronic stroke
title_full Functional brain networks assessed with surface electroencephalography for predicting motor recovery in a neural guided intervention for chronic stroke
title_fullStr Functional brain networks assessed with surface electroencephalography for predicting motor recovery in a neural guided intervention for chronic stroke
title_full_unstemmed Functional brain networks assessed with surface electroencephalography for predicting motor recovery in a neural guided intervention for chronic stroke
title_short Functional brain networks assessed with surface electroencephalography for predicting motor recovery in a neural guided intervention for chronic stroke
title_sort functional brain networks assessed with surface electroencephalography for predicting motor recovery in a neural guided intervention for chronic stroke
topic Original Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8936428/
https://www.ncbi.nlm.nih.gov/pubmed/35350709
http://dx.doi.org/10.1093/braincomms/fcab214
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