Evidence of synergy coordination patterns of upper-limb motor control in stroke patients with mild and moderate impairment

Abstract

Objectives: Previous studies showed that the central nervous system (CNS) controls movements by recruiting a low-dimensional set of modules, usually referred to as muscle synergies. Stroke alters the structure and recruitment patterns of muscle synergies, leading to abnormal motor performances. Some studies have shown that muscle synergies can be used as biomarkers for assessing motor function. However, coordination patterns of muscle synergies in post-stroke patients need more investigation to characterize how they are modified in functional movements. Methods: Thirteen mild-to-moderate stroke patients and twenty age-matched healthy subjects were recruited to perform two upper-limb movements, hand-to-mouth movement and reaching movement. Muscle synergies were extracted with nonnegative matrix factorization. We identified a set of reference synergies (i.e., averaged across healthy subjects) and typical synergies (i.e., averaged across stroke subjects) from the healthy group and stroke group respectively, and extracted affected synergies from each patient. Synergy similarity between groups was computed and analyzed. Synergy reconstruction analysis was performed to verify synergy coordination patterns in post-stroke patients. Results: On average, three synergies were extracted from both the healthy and stroke groups, while the mild impairment group had a significantly higher number of synergies than the healthy group. The similarity analysis showed that synergy structure was more consistent in the healthy group, and stroke instead altered synergy structure and induced more variability. Synergy reconstruction analysis at group and individual levels showed that muscle synergies of patients often showed a combination of healthy reference synergies in the analyzed movements. Finally, this study associated four synergy coordination patterns with patients: merging (equilibrium and disequilibrium), sharing (equilibrium and disequilibrium), losing, and preservation. The preservation was mainly represented in the mild impairment group, and the moderate impairment group showed more merging and sharing. Conclusion: This study concludes that stroke shows more synergy variability compared to the healthy group and the alterations of muscle synergies can be described as a combination of reference synergies by four synergy coordination patterns. These findings deepen the understanding of the underlying neurophysiological mechanisms and possible motor control strategies adopted by the CNS in post-stroke patients.

Keywords: electromyography (EMG); muscle synergies; rehabilitation; stroke; synergic patterns; upper-limb.

FIGURE 1

Schematic diagram of hand-to-mouth movement (A) and reaching movement (B) and the position of EMG electrodes (C). TRO and TRA, triceps brachii long and lateral head; LAT, latissimus dorsi; PEC, pectoralis major; DEA, DEM, and DEP, deltoid anterior, medial, and posterior; TRU, trapezius upper; BIC, biceps brachii; BRA, brachioradialis.

FIGURE 2

Schematic of four synergy coordination patterns, preservation, merging, sharing, and losing. Blue circles represent the reference synergies and green circles are the affected synergies. For preservation, merging, and sharing, all reference synergies are involved in the generation of affected synergies, and they are summarized as one-to-one, many-to-one, and one-to-many, respectively.

FIGURE 3

Number of synergies (A) and synergy similarity (B). HG, healthy group; SG, stroke group; MIG, mild impairment group (FM ≥ 50); MOG, moderate impairment group (FM < 50). Asterisks (*, ***) indicate significance level (0.05, 0.001).

FIGURE 4

Reference synergies and typical synergies (A). The number is the synergy vector similarity between reference synergies and typical synergies of each group is shown. (B) Shows the inter-group synergy similarity.

FIGURE 5

Synergy reconstruction at the group level. Three thresholds (0.2, 0.3, and 0.4) were set for synergy reconstruction analysis. The first row shows the results with a threshold of 0.4. The second row shows reference synergies. When the threshold is 0.2 or 0.3, the reconstruction results are very similar (the third row). Red, green, and blue bars represent reference synergies, typical synergies, and reconstructed synergies, respectively. We showed the procedure (arrow) with a reconstruction coefficient above the threshold and reconstruction similarity.

FIGURE 6

Synergy matching between synergies of each patient and reference synergies. The HG column represents reference synergies. MIG and MOG columns are the synergies of each patient. We paired the reference synergies and patients’ synergies by scalar product. Similarity values are shown in each subplot.

FIGURE 7

Synergy reconstruction analysis at individual level. (A) Synergies of patients (affected synergies). (B, C) show the reconstructed synergies by merging and fractionation analyses. (D, E) is the reconstruction similarity and coefficients. In (E, G), three squares in each column indicate the reconstruction coefficient when three reference synergies were used to reconstruct each affected synergy. Yellow squares represent the reconstruction coefficient above 0.3, and purple squares are below 0.3. The bars in (D, F) indicate the reconstructed similarity corresponding to each affected synergy. Blue bars represent the reconstruction similarity above 0.7 and gray bars below 0.7.

FIGURE 8

Representative subjects of each muscle synergy coordination pattern.

FIGURE 9

The similarity between affected synergies of each synergy coordination pattern and reference synergies. PRE, Preservation; LOS, Losing; MER_EQ, Equilibrium mode of merging; MER_DEQ, Disequilibrium mode of merging; SHA_EQ, Equilibrium mode of sharing; SHA_EQ, Disequilibrium mode of sharing.