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

Sophie Chen,Jonathan Entakli,Eric Berton,Mireille Bonnard,Jozina B De Graaf

doi:10.1371/journal.pone.0060291

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.

Highlights

The highly developed ability of some primates, including humans, to perform a precision grip is generally accepted to require direct spinal projections from the primary motor cortex (M1), a connection termed the corticospinal (CS) pathway [1,2,3,4]
The corticomuscular coherence (CMC) values and their topographies were similar for the unimanual and bimanual conditions. The aim of this experiment was to study the implication of the corticospinal (CS) projections originating from the supplementary motor area (SMA) in precise grip force control
This is clear in the result for a typical subject (Fig. 3) for the 2–4 s period where for left hand First Dorsal Interosseus (FDI), we found CMC over M1R with values comparable to those found over M1L for right hand FDI during the periods of interest but without CMC over the medial frontal region

Summary

Introduction

The highly developed ability of some primates, including humans, to perform a precision grip (thumb-index opposition) is generally accepted to require direct spinal projections from the primary motor cortex (M1), a connection termed the corticospinal (CS) pathway [1,2,3,4]. The medial wall of each hemisphere, where the supplementary motor area (SMA) is located, is one of the frontal areas with a large number of corticospinally projecting neurons [6,7] Until now, their existence has been mainly revealed by anatomical approaches [8,9,10,11,12,13] and very few studies on their functional role have been reported [14]. Non-invasive transcranial magnetic stimulation (TMS) studies in humans have shown motor evoked potentials in hand muscles following SMA stimulation with a latency comparable to that found for M1 stimulation [15,16], strongly suggesting the existence of fast CS projections from SMA. The purpose of the present study was to investigate whether the CS projections from human SMA are functional during force control with a precision grip

Objectives

Results

Discussion

Conclusion