Nonlinear Coupling between Cortical Oscillations and Muscle Activity during Isotonic Wrist Flexion.

Yuan Yang,Alfred C Schouten,Teodoro Solis-Escalante,Mark Van De Ruit,Frans C T Van Der Helm

doi:10.3389/fncom.2016.00126

Yuan Yang, Alfred C Schouten + Show 3 more

Open Access

https://doi.org/10.3389/fncom.2016.00126

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Abstract

Coupling between cortical oscillations and muscle activity facilitates neuronal communication during motor control. The linear part of this coupling, known as corticomuscular coherence, has received substantial attention, even though neuronal communication underlying motor control has been demonstrated to be highly nonlinear. A full assessment of corticomuscular coupling, including the nonlinear part, is essential to understand the neuronal communication within the sensorimotor system. In this study, we applied the recently developed n:m coherence method to assess nonlinear corticomuscular coupling during isotonic wrist flexion. The n:m coherence is a generalized metric for quantifying nonlinear cross-frequency coupling as well as linear iso-frequency coupling. By using independent component analysis (ICA) and equivalent current dipole source localization, we identify four sensorimotor related brain areas based on the locations of the dipoles, i.e., the contralateral primary sensorimotor areas, supplementary motor area (SMA), prefrontal area (PFA) and posterior parietal cortex (PPC). For all these areas, linear coupling between electroencephalogram (EEG) and electromyogram (EMG) is present with peaks in the beta band (15–35 Hz), while nonlinear coupling is detected with both integer (1:2, 1:3, 1:4) and non-integer (2:3) harmonics. Significant differences between brain areas is shown in linear coupling with stronger coherence for the primary sensorimotor areas and motor association cortices (SMA, PFA) compared to the sensory association area (PPC); but not for the nonlinear coupling. Moreover, the detected nonlinear coupling is similar to previously reported nonlinear coupling of cortical activity to somatosensory stimuli. We suggest that the descending motor pathways mainly contribute to linear corticomuscular coupling, while nonlinear coupling likely originates from sensory feedback.

Highlights

Coupling between neuronal populations facilitates their communication in the nervous system and may shorten reaction times (Varela et al, 2001; Schoffelen et al, 2005)
The independent component (IC) cluster in the left primary sensorimotor areas (S1-M1) contains components from 11 subjects with the mean dipole located in Brodmann area (BA) 4: [−33, −14, 47] (Talairach coordinates, unit: mm)
This study revealed for the first time nonlinear corticomuscular coupling in the sensorimotor network involving the primary sensorimotor areas and association areas

Summary

Introduction

Coupling between neuronal populations facilitates their communication in the nervous system and may shorten reaction times (Varela et al, 2001; Schoffelen et al, 2005). Nonlinear Corticomuscular Coupling plays an important role for neuronal communication between central and peripheral sensorimotor systems (Salenius and Hari, 2003; van Wijk et al, 2012). The linear part of corticomuscular coupling, known as corticomuscular coherence, has received much attention for decades (Mima and Hallett, 1999; Schoffelen et al, 2005; Witham et al, 2011; Raethjen and Muthuraman, 2012), neuronal communication underlying motor control have been demonstrated to be highly nonlinear (Darvas et al, 2009; Chen et al, 2010; Vlaar et al, 2016; Yang et al, 2016c). Using an established experimental paradigm completed by healthy subjects, our motivation is to establish a reference for future clinical studies

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