Functional Corticospinal Projections from Human Supplementary Motor Area Revealed by Corticomuscular Coherence during Precise Grip Force Control

Abstract

The purpose of the present study was to investigate whether corticospinal projections from human supplementary motor area (SMA) are functional during precise force control with the precision grip (thumb-index opposition). Since beta band corticomuscular coherence (CMC) is well-accepted to reflect efferent corticospinal transmission, we analyzed the beta band CMC obtained with simultaneous recording of electroencephalographic (EEG) and electromyographic (EMG) signals. Subjects performed a bimanual precise visuomotor force tracking task by applying isometric low grip forces with their right hand precision grip on a custom device with strain gauges. Concurrently, they held the device with their left hand precision grip, producing similar grip forces but without any precision constraints, to relieve the right hand. Some subjects also participated in a unimanual control condition in which they performed the task with only the right hand precision grip while the device was held by a mechanical grip. We analyzed whole scalp topographies of beta band CMC between 64 EEG channels and 4 EMG intrinsic hand muscles, 2 for each hand. To compare the different topographies, we performed non-parametric statistical tests based on spatio-spectral clustering. For the right hand, we obtained significant beta band CMC over the contralateral M1 region as well as over the SMA region during static force contraction periods. For the left hand, however, beta band CMC was only found over the contralateral M1. By comparing unimanual and bimanual conditions for right hand muscles, no significant difference was found on beta band CMC over M1 and SMA. We conclude that the beta band CMC found over SMA for right hand muscles results from the precision constraints and not from the bimanual aspect of the task. The result of the present study strongly suggests that the corticospinal projections from human SMA become functional when high precision force control is required.

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

“…In line with previous studies (Babiloni et al, 2008; Meng et al, 2008; Witham et al, 2010; Chen et al, 2013), beta-band corticomuscular coherence (linear) is detected not only at the primary sensorimotor areas (S1-M1) but also association areas, including both motor association cortices, i.e., PFA and SMA and sensory association area, i.e., PPC. Although both descending motor and ascending sensory feedback tracts can contribute to the corticomuscular coupling (Meng et al, 2008; Witham et al, 2011), stronger linear coherence was detected at the S1-M1 and motor association cortices (PFA, SMA) compared to the sensory associated PPC.…”

“…Although linear coupling between SMA/PMA and muscles are smaller, this is still functionally significant. The linear corticomuscular coupling measured at SMA and PFA was suggested to be functionally related to the fine modulation of force control (Chen et al, 2013). …”

“…The descending corticospinal motor tract is an obvious pathway resulting in the corticomuscular coupling. Furthermore, neural oscillations coupled with muscle activity are found in the primary motor cortex as well as motor association cortices including the supplementary motor area (SMA) and the prefrontal cortex (Ohara et al, 2001; Babiloni et al, 2008; Meng et al, 2008; Chen et al, 2013). …”

The functional role of beta‐oscillations in the supplementary motor area during reaching and grasping after stroke: A question of structural damage to the corticospinal tract

“…Desynchronization of ongoing beta oscillatory activity occurs during active and passive movements, as well as motor imagery and movement anticipation (Brinkman, Stolk, Dijkerman, de Lange, & Toni, ; Pfurtscheller & Lopes da Silva, ). During weak to moderate muscle contraction, corticomuscular coherence is prominent specifically in the beta band (Mima & Hallett, ) and has been related to specific movement parameters such as precision and force constraints (Chen, Entakli, Bonnard, Berton, & De Graaf, ; Kilner, Baker, Salenius, Hari, & Lemon, ), which are distinctive features of the present task.…”

Beta Band Corticomuscular Drive Reflects Muscle Coordination Strategies

“…Similar low-force isometric precision task have been previously used in literature for CMC analysis (Baker et al, 1997; Kilner et al, 2000; Fisher et al, 2002; Riddle and Baker, 2006; Chen et al, 2013). Raw coherence values were first normalized by conversion to standard Z-scores using the following formula $Z=\frac{\text{arctanh}\left(\sqrt{\text{C}}\right)}{\sqrt{1/2N}}$…”