Dynamic networks of physiologic interactions of brain waves and rhythms in muscle activity

Abstract

The brain plays a central role in facilitating vital body functions and in regulating physiological and organ systems, including the skeleto-muscular and locomotor system. While neural control is essential to synchronize and coordinate activation of various muscle groups and muscle fibers within muscle groups in relation to body movements and distinct physiologic states, the dynamic networks of brain-muscle interactions have not been explored and the complex regulatory mechanism of brain-muscle control remains unknown. Here we present a first study of network interactions between brain waves at different cortical locations and peripheral muscle activity across key physiologic states - wake, sleep and distinct sleep stages. Utilizing a novel approach based on the Network Physiology framework and the concept of time delay stability, we find that for each physiologic state the network of cortico-muscular interactions is characterized by a specific hierarchical organization of network topology and network links strength, where particular brain waves are main mediators of interaction and control of muscular activity. Further, we uncover that with transition from one physiological state to another, the brain-muscle interaction network undergoes marked reorganization in the profile of network links strength, indicating a direct association between network structure and physiological state and function. The pronounced stratification in brain-muscle network characteristics across sleep stages is consistent for chin and leg muscle groups and persists across subjects, indicating a remarkable universality and a previously unrecognized basic physiologic mechanism that regulates muscle activity even during rest and in the absence targeted direct movement. Our findings demonstrate previously unrecognized coordination between brain waves and activation of different muscle fiber types within muscle groups, laws of brain-muscle cross-communication and principles of network integration and control. These investigations demonstrate the potential of network-based biomarkers for classification of distinct physiological states and conditions, for the diagnosis and prognosis of neurodegenerative, movement and sleep disorders, and for developing efficient treatment strategies.