Distinct cortico-muscular coupling between step and stance leg during reactive stepping responses

Abstract

Balance recovery often relies on successful stepping responses, which presumably require precise and rapid interactions between the cerebral cortex and the leg muscles. Yet, little is known about how cortico-muscular coupling (CMC) supports the execution of reactive stepping. We conducted an exploratory analysis investigating time-dependent CMC with specific leg muscles in a reactive stepping task. We analyzed high density EEG, EMG, and kinematics of 18 healthy young participants while exposing them to balance perturbations at different intensities, in the forward and backward directions. Participants were instructed to maintain their feet in place, unless stepping was unavoidable. Muscle-specific Granger causality analysis was conducted on single step- and stance-leg muscles over 13 EEG electrodes with a midfrontal scalp distribution. Time-frequency Granger causality analysis was used to identify CMC from cortex to muscles around perturbation onset, foot-off and foot strike events. We hypothesized that CMC would increase compared to baseline. In addition, we expected to observe different CMC between step and stance leg because of their functional role during the step response. In particular, we expected that CMC would be most evident for the agonist muscles while stepping, and that CMC would precede upregulation in EMG activity in these muscles. We observed distinct Granger gain dynamics over theta, alpha, beta, and low/high-gamma frequencies during the reactive balance response for all leg muscles in each step direction. Interestingly, between-leg differences in Granger gain were almost exclusively observed following the divergence of EMG activity. Our results demonstrate cortical involvement in the reactive balance response and provide insights into its temporal and spectral characteristics. Overall, our findings suggest that higher levels of CMC do not facilitate leg-specific EMG activity. Our work is relevant for clinical populations with impaired balance control, where CMC analysis may elucidate the underlying pathophysiological mechanisms.