Abstract

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.

Highlights

  • The human body is composed of diverse organ systems, each with its own regulatory mechanisms and complex dynamical behavior

  • By probing the coupling through the time delay in the bursting dynamics in the brain represented by physiological relevant cortical rhythms and peripheral muscle output signals, we establish the first detailed brain-muscles interaction networks characterizing basic physiologic states, and we show that the default brain-muscle network comprises state-specific patterns of communication involving several frequency bands— beta or gamma as shown by cortico-muscular coherence (CMC) during motor contraction

  • Each location can be represented by seven network nodes, which may dynamically interact among them and with nodes in different locations

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Summary

Introduction

The human body is composed of diverse organ systems, each with its own regulatory mechanisms and complex dynamical behavior. Organ-to-organ interactions occur at multiple levels and spatio-temporal scales to produce distinct physiologic states, e.g., wake and sleep. Mapping the network of organ interactions is of primary importance to fully understand basic physiologic states and functions, rigorously discriminate between healthy and pathological behaviors, and understand complex diseases associated with alterations and breakdown of networked interactions across levels in the human organism. A new field, Network Physiology, has been established to address the fundamental question of how distinct physiologic states and functions emerge out of organ network interactions (Bashan et al, 2012; Ivanov and Bartsch, 2014; Ivanov et al, 2016, 2017). Novel methodologies and approaches have been recently developed within the framework of Network Physiology to investigate brain-organ and organ-organ interactions and their association to different physiologic states (Faes et al, 2014, 2015; Bartsch et al, 2015; Liu et al, 2015b; Porta and Faes, 2015; Lin et al, 2016; Moorman et al, 2016)

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