Rizzo Rossella, Wang Jilin W J L, DePold Hohler Anna, Holsapple James W, Vaou Okeanis E, Ivanov Plamen Ch
Keck Laboratory for Network Physiology, Department of Physics, Boston University, Boston, MA, United States.
Department of Engineering, University of Palermo, Palermo, Italy.
Front Netw Physiol. 2023 Sep 5;3:1168677. doi: 10.3389/fnetp.2023.1168677. eCollection 2023.
The brain plays central role in regulating physiological systems, including the skeleto-muscular and locomotor system. Studies of cortico-muscular coordination have primarily focused on associations between movement tasks and dynamics of specific brain waves. However, the brain-muscle functional networks of synchronous coordination among brain waves and muscle activity rhythms that underlie locomotor control remain unknown. Here we address the following fundamental questions: what are the structure and dynamics of cortico-muscular networks; whether specific brain waves are main network mediators in locomotor control; how the hierarchical network organization relates to distinct physiological states under autonomic regulation such as wake, sleep, sleep stages; and how network dynamics are altered with neurodegenerative disorders. We study the interactions between all physiologically relevant brain waves across cortical locations with distinct rhythms in leg and chin muscle activity in healthy and Parkinson's disease (PD) subjects. Utilizing Network Physiology framework and time delay stability approach, we find that 1) each physiological state is characterized by a unique network of cortico-muscular interactions with specific hierarchical organization and profile of links strength; 2) particular brain waves play role as main mediators in cortico-muscular interactions during each state; 3) PD leads to muscle-specific breakdown of cortico-muscular networks, altering the sleep-stage stratification pattern in network connectivity and links strength. In healthy subjects cortico-muscular networks exhibit a pronounced stratification with stronger links during wake and light sleep, and weaker links during REM and deep sleep. In contrast, network interactions reorganize in PD with decline in connectivity and links strength during wake and non-REM sleep, and increase during REM, leading to markedly different stratification with gradual decline in network links strength from wake to REM, light and deep sleep. Further, we find that wake and sleep stages are characterized by specific links strength profiles, which are altered with PD, indicating disruption in the synchronous activity and network communication among brain waves and muscle rhythms. Our findings demonstrate the presence of previously unrecognized functional networks and basic principles of brain control of locomotion, with potential clinical implications for novel network-based biomarkers for early detection of Parkinson's and neurodegenerative disorders, movement, and sleep disorders.
大脑在调节生理系统，包括骨骼肌肉和运动系统中起着核心作用。皮质-肌肉协调的研究主要集中在运动任务与特定脑电波动态之间的关联。然而，运动控制背后的脑电波与肌肉活动节律同步协调的脑-肌肉功能网络仍不清楚。在这里，我们解决以下基本问题：皮质-肌肉网络的结构和动态是什么；特定脑电波是否是运动控制中的主要网络调节因子；分层网络组织如何与自主调节下的不同生理状态（如清醒、睡眠、睡眠阶段）相关；以及网络动态如何因神经退行性疾病而改变。我们研究了健康和帕金森病（PD）受试者中，不同节律的腿部和下巴肌肉活动与皮质区域所有生理相关脑电波之间的相互作用。利用网络生理学框架和时间延迟稳定性方法，我们发现：1）每种生理状态都由一个独特的皮质-肌肉相互作用网络表征，具有特定的分层组织和连接强度分布；2）特定脑电波在每种状态下的皮质-肌肉相互作用中起主要调节因子的作用；3）PD导致皮质-肌肉网络的肌肉特异性破坏，改变了网络连通性和连接强度中的睡眠阶段分层模式。在健康受试者中，皮质-肌肉网络表现出明显的分层，在清醒和浅睡眠期间连接更强，在快速眼动（REM）和深睡眠期间连接较弱。相比之下，PD患者的网络相互作用发生重组，在清醒和非快速眼动睡眠期间连通性和连接强度下降，在快速眼动睡眠期间增加，导致明显不同的分层，网络连接强度从清醒到快速眼动、浅睡眠和深睡眠逐渐下降。此外，我们发现清醒和睡眠阶段由特定的连接强度分布表征，这些分布因PD而改变，表明脑电波和肌肉节律之间的同步活动和网络通信受到破坏。我们的研究结果证明了存在以前未被认识的功能网络以及大脑运动控制的基本原理，对基于网络的新型生物标志物在帕金森病和神经退行性疾病、运动和睡眠障碍的早期检测方面具有潜在的临床意义。
