Information decomposition of multichannel EMG to map functional interactions in the distributed motor system

Tjeerd W Boonstra,Luca Faes,Jennifer N Kerkman,Daniele Marinazzo

doi:10.1016/j.neuroimage.2019.116093

Tjeerd W Boonstra, Luca Faes + Show 2 more

Open Access

https://doi.org/10.1016/j.neuroimage.2019.116093

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Abstract

The central nervous system needs to coordinate multiple muscles during postural control. Functional coordination is established through the neural circuitry that interconnects different muscles. Here we used multivariate information decomposition of multichannel EMG acquired from 14 healthy participants during postural tasks to investigate the neural interactions between muscles. A set of information measures were estimated from an instantaneous linear regression model and a time-lagged VAR model fitted to the EMG envelopes of 36 muscles. We used network analysis to quantify the structure of functional interactions between muscles and compared them across experimental conditions. Conditional mutual information and transfer entropy revealed sparse networks dominated by local connections between muscles. We observed significant changes in muscle networks across postural tasks localized to the muscles involved in performing those tasks. Information decomposition revealed distinct patterns in task-related changes: unimanual and bimanual pointing were associated with reduced transfer to the pectoralis major muscles, but an increase in total information compared to no pointing, while postural instability resulted in increased information, information transfer and information storage in the abductor longus muscles compared to normal stability. These findings show robust patterns of directed interactions between muscles that are task-dependent and can be assessed from surface EMG recorded during static postural tasks. We discuss directed muscle networks in terms of the neural circuitry involved in generating muscle activity and suggest that task-related effects may reflect gain modulations of spinal reflex pathways.

Highlights

Adaptive behavior emerges in the nervous system from the ongoing interactions among the body and the environment
These cognitive functions result from the dynamic interactions of distributed neural populations operating in large-scale networks that determine the flow of information through the central nervous system (Bressler and Menon, 2010; Sporns et al, 2004)
While the functional implications of large-scale networks have mainly been investigated within the brain (Petersen and Sporns, 2015), we expected that similar principles apply to the entire nervous system and encompass interactions between brain and body

Summary

Introduction

Adaptive behavior emerges in the nervous system from the ongoing interactions among the body and the environment. The brain and spinal cord are interwoven with the body and interact through the peripheral and autonomic nervous systems with other organ systems (Freund et al, 2016) Through these neuronal pathways, dynamic interactions among subsystems are mediated to support physiological function and establish system-wide integration (Bashan et al, 2012). The corticospinal tract originates from different cortical areas including primary motor cortex and terminates widely within the spinal gray matter, including direct monosynaptic projections to contralateral spinal motor neurons (Lemon, 2008) Other descending pathways such as the vestibulospinal and the reticulospinal tract originate from brainstem nuclei, project to bilateral regions of the spinal cord and are involved in controlling posture and locomotion (Kuypers, 1981). Gain modulation in sensorimotor pathways is difficult to assess during natural movements

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