Forearm and Hand Muscles Exhibit High Coactivation and Overlapping of Cortical Motor Representations

Gabriela P Tardelli,Maria A Nazarova,Victor H Souza,Marco A C Garcia,Pavel A Novikov,Oswaldo Baffa,Renan H Matsuda

doi:10.1007/s10548-022-00893-1

Abstract

Most of the motor mapping procedures using navigated transcranial magnetic stimulation (nTMS) follow the conventional somatotopic organization of the primary motor cortex (M1) by assessing the representation of a particular target muscle, disregarding the possible coactivation of synergistic muscles. In turn, multiple reports describe a functional organization of the M1 with an overlapping among motor representations acting together to execute movements. In this context, the overlap degree among cortical representations of synergistic hand and forearm muscles remains an open question. This study aimed to evaluate the muscle coactivation and representation overlapping common to the grasping movement and its dependence on the stimulation parameters. The nTMS motor maps were obtained from one carpal muscle and two intrinsic hand muscles during rest. We quantified the overlapping motor maps in size (area and volume overlap degree) and topography (similarity and centroid Euclidean distance) parameters. We demonstrated that these muscle representations are highly overlapped and similar in shape. The overlap degrees involving the forearm muscle were significantly higher than only among the intrinsic hand muscles. Moreover, the stimulation intensity had a stronger effect on the size compared to the topography parameters. Our study contributes to a more detailed cortical motor representation towards a synergistic, functional arrangement of M1. Understanding the muscle group coactivation may provide more accurate motor maps when delineating the eloquent brain tissue during pre-surgical planning.

Highlights

A fundamental debate on primary motor cortex (M1) organization is whether different body parts rely on a discrete somatotopic or functionally-specific representation on theBrain Topography (2022) 35:322–336 cortical surface (Schieber 2001)
In the M1, the somatotopic organization associates a cortical site to the control of a specific muscle (Penfield and Rasmussen 1950), whereas the functional organization suggests the cortical representation of limb movements (Gentner et al 2010; Strother et al 2012)
We demonstrate that the motor map parameters vary significantly between the pairs of muscles in size but not in topography (EMD and centroid Euclidean distance)

Summary

Introduction

A fundamental debate on primary motor cortex (M1) organization is whether different body parts rely on a discrete somatotopic or functionally-specific representation on theBrain Topography (2022) 35:322–336 cortical surface (Schieber 2001). Several studies have demonstrated that the high complexity of central movement generation can be derived from an extensive overlap and redundancy between adjacent cortical areas representations (Schieber 2001; Devanne et al 2006; Gentner and Classen 2006; Melgari et al 2008). The overlapping areas can be related to specific movements involving more than one adjacent single joint and, a complex synergy among different muscles (Strother et al 2012; Leo et al 2016), which corroborates the hypothesis of the functional organization of M1. In this context, the overlap degree (OD) in the cortical representation of synergistic hand and forearm muscles remains an open question. An approach that accounts for the functional overlap in cortical motor representations can lead to more selective cortical maps with the potential to improve patient prognostics (Frey et al 2014; Picht et al 2016)

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