Context-dependent reduction in corticomuscular coupling for balance control in chronic stroke survivors

Abstract

Balance control is an important indicator of mobility and independence in activities of daily living. How the functional coupling between the cortex and the muscle for balance control is affected following stroke remains to be known. We investigated the changes in coupling between the cortex and leg muscles during a challenging balance task over multiple frequency bands in chronic stroke survivors. Fourteen participants with stroke and ten healthy controls performed a challenging balance task. They stood on a computerized support surface that was either fixed (low difficulty condition) or sway-referenced with varying gain (medium and high difficulty conditions). We computed corticomuscular coherence between electrodes placed over the sensorimotor area (electroencephalography) and leg muscles (electromyography) and assessed balance performance using clinical and laboratory-based tests. We found significantly lower delta frequency band coherence in stroke participants when compared with healthy controls under medium difficulty condition, but not during low and high difficulty conditions. These differences were found for most of the distal but not for proximal leg muscle groups. No differences were found at other frequency bands. Participants with stroke showed poor balance clinical scores when compared with healthy controls, but no differences were found for laboratory-based tests. The observation of effects at distal but not at proximal muscle groups suggests differences in the (re)organization of the descending connections across two muscle groups for balance control. We argue that the observed group difference in delta band coherence indicates balance context-dependent alteration in mechanisms for the detection of somatosensory modulation resulting from sway-referencing of the support surface for balance maintenance following stroke.

Keywords: 2Stroke; Balance; Coupling; Descending tracts integrity; EEG; Perturbation.

Fig. 1

Experimental setup and the continuous balance task. (A) Experimental setup for the posture task. (B) Continuous balance task. (C) Representative EEG (Cz) and EMG traces for all five muscles for a single trial from one subject

Fig. 2

The medium difficulty balance task condition. A. Spectrograms of the EEG signal (Cz) and all five muscles (TA, GM, SOL, BF, RF) showing relative power magnitude across different frequency bands. B. Coherence spectra plots for Cz and each of the five muscles. Data have been averaged across all subjects within a group (Stroke participants and Healthy controls)

Fig. 3

Smaller cortico-muscular coherence for the TA muscle in stroke. Cortico-muscular coherence (CMC) magnitude between Cz (EEG) and tibialis anterior (TA-EMG) for all five frequency bands and all three task conditions for stroke participants and healthy controls. (A) CMC averaged across the entire 20 s trial. (B) CMC for seven trial bins. The dotted line represents coherence significance threshold Z. Data are means (± SEM) of all subjects. An asterisk indicates significant differences between groups

Fig. 4

Smaller cortico-muscular coherence for the GM muscle in stroke. Cortico-muscular coherence (CMC) magnitude between Cz (EEG) and gastrocnemius medialis (GM-EMG) for all five frequency bands and all three task conditions for stroke participants and healthy controls. (A) CMC averaged across the entire 20 s trial. (B) CMC for seven trial bins. The dotted line represents coherence significance threshold Z. Data are means (± SEM) of all subjects. An asterisk indicates significant differences between groups

Fig. 5

No group difference in cortico-muscular coherence for the SOL muscle. Cortico-muscular coherence (CMC) magnitude between Cz (EEG) and soleus (SOL-EMG) for all five frequency bands and all three task conditions for stroke participants and healthy controls. (A) CMC averaged across the entire 20 s trial. (B) CMC for seven trial bins. The dotted line represents coherence significance threshold Z. Data are means (± SEM) of all subjects

Fig. 6

No group difference in cortico-muscular coherence for the BF muscle. Cortico-muscular coherence (CMC) magnitude between Cz (EEG) and biceps femoris (BF-EMG) for all five frequency bands and all three task conditions for stroke participants and healthy controls. (A) CMC averaged across the entire 20 s trial. (B) CMC for seven trial bins. The dotted line represents coherence significance threshold Z. Data are means (± SEM) of all subjects

Fig. 7

No group difference in cortico-muscular coherence for the RF muscle. Cortico-muscular coherence (CMC) magnitude between Cz (EEG) and rectus femoris (RF-EMG) for all five frequency bands and all three task conditions for stroke participants and healthy controls. (A) CMC averaged across the entire 20 s trial. (B) CMC for seven trial bins. The dotted line represents coherence significance threshold Z. Data are means (± SEM) of all subjects

Fig. 8

Behavioral variables. A. Berg Balance Score (BBS) shown as median and quartiles. B. Timed Up and Go (TUG) shown as median and quartiles. C. RMS COP, D. RMS COPv, and E. COP Path length (PL) during the continuous balance task. COP data are means (± SEM) of all subjects. Asterisks indicate significant differences between groups