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Network Physiology of Cortico–Muscular Interactions

Skeletal muscle activity is continuously modulated across physiologic states to provide coordination, flexibility and responsiveness to body tasks and external inputs. Despite the central role the muscular system plays in facilitating vital body functions, the network of brain-muscle interactions re...

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Autores principales: Rizzo, Rossella, Zhang, Xiyun, Wang, Jilin W. J. L., Lombardi, Fabrizio, Ivanov, Plamen Ch.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7726198/
https://www.ncbi.nlm.nih.gov/pubmed/33324233
http://dx.doi.org/10.3389/fphys.2020.558070
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author Rizzo, Rossella
Zhang, Xiyun
Wang, Jilin W. J. L.
Lombardi, Fabrizio
Ivanov, Plamen Ch.
author_facet Rizzo, Rossella
Zhang, Xiyun
Wang, Jilin W. J. L.
Lombardi, Fabrizio
Ivanov, Plamen Ch.
author_sort Rizzo, Rossella
collection PubMed
description Skeletal muscle activity is continuously modulated across physiologic states to provide coordination, flexibility and responsiveness to body tasks and external inputs. Despite the central role the muscular system plays in facilitating vital body functions, the network of brain-muscle interactions required to control hundreds of muscles and synchronize their activation in relation to distinct physiologic states has not been investigated. Recent approaches have focused on general associations between individual brain rhythms and muscle activation during movement tasks. However, the specific forms of coupling, the functional network of cortico-muscular coordination, and how network structure and dynamics are modulated by autonomic regulation across physiologic states remains unknown. To identify and quantify the cortico-muscular interaction network and uncover basic features of neuro-autonomic control of muscle function, we investigate the coupling between synchronous bursts in cortical rhythms and peripheral muscle activation during sleep and wake. Utilizing the concept of time delay stability and a novel network physiology approach, we find that the brain-muscle network exhibits complex dynamic patterns of communication involving multiple brain rhythms across cortical locations and different electromyographic frequency bands. Moreover, our results show that during each physiologic state the cortico-muscular network is characterized by a specific profile of network links strength, where particular brain rhythms play role of main mediators of interaction and control. Further, we discover a hierarchical reorganization in network structure across physiologic states, with high connectivity and network link strength during wake, intermediate during REM and light sleep, and low during deep sleep, a sleep-stage stratification that demonstrates a unique association between physiologic states and cortico-muscular network structure. The reported empirical observations are consistent across individual subjects, indicating universal behavior in network structure and dynamics, and high sensitivity of cortico-muscular control to changes in autonomic regulation, even at low levels of physical activity and muscle tone during sleep. Our findings demonstrate previously unrecognized basic principles of brain-muscle network communication and control, and provide new perspectives on the regulatory mechanisms of brain dynamics and locomotor activation, with potential clinical implications for neurodegenerative, movement and sleep disorders, and for developing efficient treatment strategies.
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spelling pubmed-77261982020-12-14 Network Physiology of Cortico–Muscular Interactions Rizzo, Rossella Zhang, Xiyun Wang, Jilin W. J. L. Lombardi, Fabrizio Ivanov, Plamen Ch. Front Physiol Physiology Skeletal muscle activity is continuously modulated across physiologic states to provide coordination, flexibility and responsiveness to body tasks and external inputs. Despite the central role the muscular system plays in facilitating vital body functions, the network of brain-muscle interactions required to control hundreds of muscles and synchronize their activation in relation to distinct physiologic states has not been investigated. Recent approaches have focused on general associations between individual brain rhythms and muscle activation during movement tasks. However, the specific forms of coupling, the functional network of cortico-muscular coordination, and how network structure and dynamics are modulated by autonomic regulation across physiologic states remains unknown. To identify and quantify the cortico-muscular interaction network and uncover basic features of neuro-autonomic control of muscle function, we investigate the coupling between synchronous bursts in cortical rhythms and peripheral muscle activation during sleep and wake. Utilizing the concept of time delay stability and a novel network physiology approach, we find that the brain-muscle network exhibits complex dynamic patterns of communication involving multiple brain rhythms across cortical locations and different electromyographic frequency bands. Moreover, our results show that during each physiologic state the cortico-muscular network is characterized by a specific profile of network links strength, where particular brain rhythms play role of main mediators of interaction and control. Further, we discover a hierarchical reorganization in network structure across physiologic states, with high connectivity and network link strength during wake, intermediate during REM and light sleep, and low during deep sleep, a sleep-stage stratification that demonstrates a unique association between physiologic states and cortico-muscular network structure. The reported empirical observations are consistent across individual subjects, indicating universal behavior in network structure and dynamics, and high sensitivity of cortico-muscular control to changes in autonomic regulation, even at low levels of physical activity and muscle tone during sleep. Our findings demonstrate previously unrecognized basic principles of brain-muscle network communication and control, and provide new perspectives on the regulatory mechanisms of brain dynamics and locomotor activation, with potential clinical implications for neurodegenerative, movement and sleep disorders, and for developing efficient treatment strategies. Frontiers Media S.A. 2020-11-26 /pmc/articles/PMC7726198/ /pubmed/33324233 http://dx.doi.org/10.3389/fphys.2020.558070 Text en Copyright © 2020 Rizzo, Zhang, Wang, Lombardi and Ivanov. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Physiology
Rizzo, Rossella
Zhang, Xiyun
Wang, Jilin W. J. L.
Lombardi, Fabrizio
Ivanov, Plamen Ch.
Network Physiology of Cortico–Muscular Interactions
title Network Physiology of Cortico–Muscular Interactions
title_full Network Physiology of Cortico–Muscular Interactions
title_fullStr Network Physiology of Cortico–Muscular Interactions
title_full_unstemmed Network Physiology of Cortico–Muscular Interactions
title_short Network Physiology of Cortico–Muscular Interactions
title_sort network physiology of cortico–muscular interactions
topic Physiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7726198/
https://www.ncbi.nlm.nih.gov/pubmed/33324233
http://dx.doi.org/10.3389/fphys.2020.558070
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