Muscle Synergies in Cycling after Incomplete Spinal Cord Injury: Correlation with Clinical Measures of Motor Function and Spasticity

Abstract

Background: After incomplete spinal cord injury (iSCI), patients suffer important sensorimotor impairments, such as abnormal locomotion patterns and spasticity. Complementary to current clinical diagnostic procedures, the analysis of muscle synergies has emerged as a promising tool to study muscle coordination, which plays a major role in the control of multi-limb functional movements.

Objective: Based on recent findings suggesting that walking and cycling share similar synergistic control, the analysis of muscle synergies during cycling might be explored as an early descriptor of gait-related impaired control. This idea was split into the following two hypotheses: (a) iSCI patients present a synergistic control of muscles during cycling; (b) muscle synergies outcomes extracted during cycling correlate with clinical measurements of gait performance and/or spasticity.

Methods: Electromyographic (EMG) activity of 13 unilateral lower limb muscles was recorded in a group of 10 healthy individuals and 10 iSCI subjects during cycling at four different cadences. A non-negative matrix factorization (NNMF) algorithm was applied to identify synergistic components (i.e., activation coefficients and muscle synergy vectors). Reconstruction goodness scores (VAF and r (2)) were used to evaluate the ability of a given number of synergies to reconstruct the EMG signals. A set of metrics based on the similarity between pathologic and healthy synergies were correlated with clinical scales of gait performance and spasticity.

Results: iSCI patients preserved a synergistic control of muscles during cycling. The similarity with the healthy reference was consistent with the degree of the impairment, i.e., less impaired patients showed higher similarities with the healthy reference. There was a strong correlation between reconstruction goodness scores at 42 rpm and motor performance scales (TUG, 10-m test and WISCI II). On the other hand, the similarity between the healthy and affected synergies presented correlation with some spasticity symptoms measured by Penn, Modified Ashworth and SCATS scales.

Conclusion: Overall, the results of this study support the hypothesis that the analysis of muscle synergies during cycling can provide detailed quantitative assessment of functional motor impairments and symptoms of spasticity caused by abnormal spatiotemporal muscle co-activation following iSCI.

Keywords: cycling; motor function; muscle synergies; spasticity; spinal cord injury.

Figure 1

Group average electromyographic (EMG) envelopes of the 13 recorded muscles for each of the four speeds during cycling (30, 42, 50, and 60 rpm). For each group (healthy subjects, thin lines; iSCI patients, thick lines), a total of 100 cycling cycles (10 cycles by subject) were averaged and expressed as a function of the pedaling cycle. Pedaling cycle begins when the pedal corresponding to the dominant leg (in healthy subjects) or the most affected leg (in iSCI subjects) is at the lowest position and ends when the pedal reaches the lowest position again. EMGs from each subject and muscle were previously normalized by the average of its maximum values throughout the 10 cycles. a.u., arbitrary unit. ^*, muscles belonging to the eight muscles set used in parallel analysis. Number indicate lag times that maximized the cross-correlation function. A negative value indicates that the mean EMG envelopes of iSCI patients shifted earlier in the cycle relative to the mean EMG envelopes of healthy group.

Figure 2

Variability accounted for (VAF_total) (A) and coefficient of determination (r²) (B) according to the number of synergies, for each of the four speeds (30, 42, 50, and 60 rpm). Values are given in means ± SD. These reconstruction goodness indexes were calculated after running the NNMF algorithm to reconstruct a set of 8 EMG envelopes for the healthy group (I) and the iSCI group (II), as well as a set of 13 EMG envelopes (III and IV for the healthy group and iSCI group, respectively). A VAF_total value of 100% and a r² value of 1 mean perfect reconstruction of the EMG set. ^*Number of synergies sufficient to describe VAF_total values ≥ 85% for at least half of the healthy participants.

Figure 3

Reconstruction of EMG envelopes in four speeds (30, 42, 50, and 60 rpm) using concatenated data from the 10 healthy subjects (A), and individual data from a patient with spasticity—ID 04 (B) and a patient without spasticity—ID 09 (C), applying the NNMF algorithm with three synergies. I: muscle synergy vectors. Each muscle synergy vector has a time-invariant profile, representing the relative contribution of each synergy for each muscular pattern. Muscle synergy vectors were normalized by their maximum value. II: averaged activation coefficients, indicating time-variant profiles responsible to activate each synergy.

Figure 4

Correlation between walking tests scores in iSCI patients and reconstruction goodness indexes at 42 rpm, for the sets of 8 and 13 muscles. VAF_total scores correlated negatively with TUG (A) and 10-m (B) tests; VAF_total scores correlated positively with WISCI II (C). r² scores correlated negatively with TUG (D) and 10-m (E) tests; r² scores correlated positively with WISCI II (F).

Figure 5

Correlation between spasticity scales in iSCI patients and W · W₀, and H · H₀ scores. For the set of 8 muscles at 42 rpm, W3 · W₀3 correlated negatively with PENN (A) and W1 · W₀1 correlated negatively with clonus spasms assessed with SCATS (B). H2 · H₀2 correlated negatively with Ashworth for the sets of 8 muscles at 42 rpm (C) and 13 muscles at 30 rpm (D). ^*Correlation is significant at the 0.05 level (2-tailed). ^**Correlation is significant at the 0.01 level (2-tailed).