Scalp electroencephalograms over ipsilateral sensorimotor cortex reflect contraction patterns of unilateral finger muscles

Abstract

A variety of neural substrates are implicated in the initiation, coordination, and stabilization of voluntary movements underpinned by adaptive contraction and relaxation of agonist and antagonist muscles. To achieve such flexible and purposeful control of the human body, brain systems exhibit extensive modulation during the transition from resting state to motor execution and to maintain proper joint impedance. However, the neural structures contributing to such sensorimotor control under unconstrained and naturalistic conditions are not fully characterized. To elucidate which brain regions are implicated in generating and coordinating voluntary movements, we employed a physiologically inspired, two-stage method to decode relaxation and three patterns of contraction in unilateral finger muscles (i.e., extension, flexion, and co-contraction) from high-density scalp electroencephalograms (EEG). The decoder consisted of two parts employed in series. The first discriminated between relaxation and contraction. If the EEG data were discriminated as contraction, the second stage then discriminated among the three contraction patterns. Despite the difficulty in dissociating detailed contraction patterns of muscles within a limb from scalp EEG signals, the decoder performance was higher than chance-level by 2-fold in the four-class classification. Moreover, weighted features in the trained decoders revealed EEG features differentially contributing to decoding performance. During the first stage, consistent with previous reports, weighted features were localized around sensorimotor cortex (SM1) contralateral to the activated fingers, while those during the second stage were localized around ipsilateral SM1. The loci of these weighted features suggested that the coordination of unilateral finger muscles induced different signaling patterns in ipsilateral SM1 contributing to motor control. Weighted EEG features enabled a deeper understanding of human sensorimotor processing as well as of a more naturalistic control of brain-computer interfaces.