Dynamical network-based evaluation for neuromuscular dysfunction in stroke-induced hemiplegia during standing

Abstract

Background: A given movement requires precise coordination of multiple muscles under the control of center nervous system. However, detailed knowledge about the changing characteristics of neuromuscular control for multi-muscle coordination in post-stroke hemiplegic patients during standing is still lacking. This study aimed to investigate the hemiplegia-linked neuromuscular dysfunction during standing from the perspective of multi-muscle dynamical coordination by utilizing a novel network approach - weighted recurrence network (WRN).

Methods: Ten male hemiplegic patients with first-ever stroke and 10 age-matched healthy male adults were instructed to stand on a platform quietly for 30 s with eyes opened and eyes closed, respectively. The WRN was constructed based on the surface electromyography signals of 16 muscles from trunk, hips, thighs and calves. Relevant topological parameters, including clustering coefficient (C) and average shortest path length (L), were extracted to evaluate the dynamical coordination of multiple muscles. A measure of node centrality in network theory, degree of centrality (DC), was innovatively introduced to assess the contribution of single muscle in the multi-muscle dynamical coordination. The standing-related assessment metric, center of pressure (COP), was provided by the platform directly.

Results: Results showed that the post-stroke hemiplegic patients stood with remarkably higher similarity of muscle activation and more coupled intermuscular dynamics, characterized by higher C and lower L than the healthy subjects (p < 0.05). The DC values and rankings of back, hip and calf muscles on the affected side were significantly decreased, whereas those on the unaffected side were significantly increased in hemiplegia group compared with the healthy group (p < 0.05). Without visual feedback, subjects exhibited enhanced muscle coordination and increased muscle involvement (p < 0.05). A decrease in C and an increase in L of WRN were observed with decreased COP areas (p < 0.05).

Conclusions: These findings revealed that stroke-induced hemiplegia could significantly influence the neuromuscular control, which was manifested as more coupled intermuscular dynamics, abnormal deactivation of muscles on affected side and compensation of muscles on unaffected side from the perspective of multi-muscle coordination. Enhanced multi-muscle dynamical coordination was strongly associated with impaired postural control. This study provides a novel analytical tool for evaluation of neuromuscular dysfunction and specification of responsible muscles for impaired postural control in stroke-induced hemiplegic patients, and could be potentially applied in clinical practice.

Keywords: Hemiplegia; Muscle networks; Neuromuscular dysfunction; Postural control; Stroke; Surface electromyogram.

Fig. 1

Experimental set-up. (a) The positioning of sEMG electrodes; (b) The standing balance test

Fig. 2

Visualization of the WRN for representative subjects. (a) EO condition; (b) EC condition

Fig. 3

Statistical results of functional muscle networks WRN. (a) Statistical results of parameter C; (b) Statistical results of parameter L. ^† (p < 0.05) significant difference between hemiplegia and control groups. * (p < 0.05) and ** (p < 0.001) significant differences between EO and EC conditions

Fig. 4

The ranking of normalized DCs in descending order. (a) and (b) are the ranking of normalized DCs under EO and EC conditions, respectively. In hemiplegia group, A and UA represent the affected and unaffected sides, respectively; In control group, A and UA represent the matched-affected and matched-unaffected sides, respectively. The lines beside the bars represent the ranking differences of the same muscles between the affected (matched-affected) and unaffected (matched-unaffected) sides in one group. (c) and (d) are the ranking position changes of same muscles between hemiplegia and control group. Negative values represent a decrease in the DC ranking position of the muscle in hemiplegia group compared to the control group, while positive values represent an increase in the DC ranking position of the muscle in hemiplegia group compared to the control group

Fig. 5

The correlations between holistic topological parameters of WRN and area of COP. (a) Correlations between parameter C and area of COP; (b) Correlations between parameter L and area of COP