Pathway-specific modulatory effects of neuromuscular electrical stimulation during pedaling in chronic stroke survivors

Abstract

Background: Neuromuscular electrical stimulation (NMES) is extensively used in stroke motor rehabilitation. How it promotes motor recovery remains only partially understood. NMES could change muscular properties, produce altered sensory inputs, and modulate fluctuations of cortical activities; but the potential contribution from cortico-muscular couplings during NMES synchronized with dynamic movement has rarely been discussed.

Method: We investigated cortico-muscular interactions during passive, active, and NMES rhythmic pedaling in healthy subjects and chronic stroke survivors. EEG (128 channels), EMG (4 unilateral lower limb muscles) and movement parameters were measured during 3 sessions of constant-speed pedaling. Sensory-level NMES (20 mA) was applied to the muscles, and cyclic stimulation patterns were synchronized with the EMG during pedaling cycles. Adaptive mixture independent component analysis was utilized to determine the movement-related electro-cortical sources and the source dipole clusters. A directed cortico-muscular coupling analysis was conducted between representative source clusters and the EMGs using generalized partial directed coherence (GPDC). The bidirectional GPDC was compared across muscles and pedaling sessions for post-stroke and healthy subjects.

Results: Directed cortico-muscular coupling of NMES cycling was more similar to that of active pedaling than to that of passive pedaling for the tested muscles. For healthy subjects, sensory-level NMES could modulate GPDC of both ascending and descending pathways. Whereas for stroke survivors, NMES could modulate GPDC of only the ascending pathways.

Conclusions: By clarifying how NMES influences neuromuscular control during pedaling in healthy and post-stroke subjects, our results indicate the potential limitation of sensory-level NMES in promoting sensorimotor recovery in chronic stroke survivors.

Keywords: Cortico-muscular coupling; EEG/EMG; Generalized partial directed coherence; NMES; Pedaling; Stroke.

Fig. 1

EEG and NMES-pedaling system. a, The general structure of the systems involved, including stationary NMES-pedaling system, control system and EEG/sEMG measurement system. b, The placement of NMES electrodes and surface EMG electrodes.

Fig. 2

General signal processing flow charts. All the pre-processing, cleaning up and analysis techniques were included

Fig. 3

Crank torque values in three pedaling protocols for stroke and healthy subjects, average across subjects, half error-bar= ± 1 SEM., **, p<0.01, *, p<0.05

Fig. 4

EEG source localization results for twelve healthy subjects during three pedaling protocols. Five independent component clusters were demonstrated with different colors. The top row gives the dipole locations and the bottom row gives the corresponding cluster centroids, the transverse, sagittal and coronal views (from left to right), A-E, different source clusters centroids

Fig. 5

Grand pooled ERSP charts for three pedaling protocols of Cluster A, BA 6 for healthy subjects. Pedal phase dependent cortical responses were observed throughout the pedal cycle (x-axis) and in the selected frequency bands (y-axis, log scaled), warm and cold color indicates increased or decreased cortical activity relative to the mean spectrogram respectively

Fig. 6

EEG source localization results for sixteen stroke subjects during three pedaling protocols. Five independent component clusters were demonstrated with different colors. The top row gives the dipole locations and the bottom row demonstrated the corresponding cluster centroids, the transverse, sagittal and coronal views (from left to right), A-E, different source clusters centroids in sequence

Fig. 7

Descending and ascending pathways of GPDC between BA6 cluster and left leg muscles for different pedaling protocols in healthy subjects, average across ICs in the selected pedaling protocol in Table 2, half error-bar= ± 1SEM. Different color represents different muscle. Upper: brain to muscle connectivity, descending pathway, lower: muscle to brain connectivity, ascending pathway. **, p<0.01, *, p<0.05 for group level (all muscles) comparison between pedaling protocols, ##, p<0.01, #, p<0.05 for individual muscle comparison with passive pedaling

Fig. 8

Descending and ascending pathways of GPDC between BA24 cluster and affected leg muscles for different pedaling protocols in chronic stroke subjects, average across ICs in the selected pedaling protocol in Table 3, half error-bar= ± 1 SEM. Different color represents different muscle. Upper: brain to muscle connectivity, descending pathway, lower: muscle to brain connectivity, ascending pathway. *, p<0.05 for group level (all muscles) comparison between pedaling protocols, ##, p<0.01, #, p<0.05 for individual muscle comparison with passive pedaling