Neuromuscular constraints on muscle coordination during overground walking in persons with chronic incomplete spinal cord injury

Abstract

Objective: Incomplete spinal cord injury (iSCI) disrupts motor control and limits the ability to coordinate muscles for overground walking. Inappropriate muscle activity has been proposed as a source of clinically observed walking deficits after iSCI. We hypothesized that persons with iSCI exhibit lower locomotor complexity compared to able-body (AB) controls as reflected by fewer motor modules, as well as, altered module composition and activation.

Methods: Eight persons with iSCI and eight age-matched AB controls walked overground at prescribed cadences. Electromyograms of fourteen single leg muscles were recorded. Non-negative matrix factorization was used to identify the composition and activation of motor modules, which represent groups of consistently co-activated muscles that accounted for 90% of variability in muscle activity.

Results: Motor module number, composition, and activation were significantly altered in persons with iSCI as compared to AB controls during overground walking at self-selected cadences. However, there was no significant difference in module number between persons with iSCI and AB controls when cadence and assistive device were matched.

Conclusions: Muscle coordination during overground walking is impaired after chronic iSCI.

Significance: Our results are indicative of neuromuscular constraints on muscle coordination after iSCI. Altered muscle coordination contributes to person-specific gait deficits during overground walking.

Keywords: Modules; Motor control; Muscle coordination; Spinal cord injury; Walking.

Copyright © 2014 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved.

Figures

Figure 1. Schematic of experimental setup and motor module analyses

A) Schematic of surface EMG recordings from 14 right limb muscles and footswitch placement. B) Schematic of non-negative matrix factorization reconstruction of observed EMG. Each time-invariant motor module (wi), displayed as bar plots in which each bar represents the relative muscle contribution, is flexibly recruited at varying activation levels across time (Ci). The linear sum of the modules multiplied by their activations at each time point accounts for > 90% of the variability in the observed EMG across all time points and muscles. Metrics describing module activations also are illustrated. The dashed horizontal line on C1 indicates the 0.15 threshold. Cpeak is the maximum activation, Carea is the area under the curve in the region where C is above threshold, and Cduty is the percent of the gait cycle in the region where C is above threshold.

Figure 2. Persons with iSCI exhibit fewer motor modules than AB subjects during overground walking

A) Bar plots showing the number of modules (mean ± 1 standard error) required to explain muscle activity for SCI subjects (n=8) and AB subjects (n=8). Asterisk indicates significant difference based on a Mann-Whitney U test for independent samples. B) Bars showing number of modules (mean ± 1 standard error) for the subset of matched SCI (n=5) and AB (n=5) subjects. ABmatch indicates the number of modules exhibited when the AB (n=5) subjects were constrained to walk at the cadence and with the assistive device of their iSCI match. Asterisk indicates significant difference based on Wilcoxon Signed Rank test for related samples between AB and ABmatch.

Figure 3. Inter-subject reconstructions show that AB modules can be flexibly combined to reconstruct a wider range of muscle coordination patterns

The dashed gray line indicates 90% VAF, the level of reconstruction achieved when modules were extracted from the data. A) Bar plots showing the variance accounted for (VAF, mean ± 1 standard error) when using one subject’s modules to reconstruct muscle activity from other subjects. Each plot represents a mean across 8 subjects. From left to right: Mean VAF for each individual AB modules reconstructing remaining muscle activity of AB subjects, individual iSCI modules reconstructing remaining SCIs’ muscle activity, individual AB modules reconstructing SCIs’ muscle activity, and individual SCI modules reconstructing muscle activity of AB subjects. B–D) Bar plots showing the variance accounted for (VAF, mean ± 1 standard error) by reconstructions for the 5 subjects included in the cadence and assistive device matched subset. B) Mean VAF of each individual ABmatch modules reconstructing their matched iSCI subject’s muscle activity versus individual SCI modules reconstructing their matched ABmatch subject’s muscle activity in the cadence and assistive device condition. C) Individual ABmatch modules reconstructing the same AB subject’s muscle activity from the self-selected condition versus individual iSCI modules reconstructing their matched AB subject’s muscle activity. D) Individual ABmatch modules reconstructing remaining ABmatch muscle activity in the cadence and assistive device condition versus individual iSCI modules reconstructing the remaining iSCIs’ muscle activity. Asterisks indicate significant differences between groups at p < 0.05.

Figure 4. Motor modules exhibited by each AB subject and representative activations

Bar plots represent the relative muscle contributions to each module, with muscles ordered as indicated by the legend at the bottom. Standard deviation bars show the variation about the mean muscle contribution across 10 bootstrapped extractions. Each column represents modules from a single AB subject. Modules were considered similar and, thus, group in a row if r > 0.532 when compared to AB1 modules, the subject with the most modules. Functional labels to the left indicate the purported mechanical function of that module or group of modules (Neptune et al., 2001). On the far right, representative activations for each module are shown as line plots from one of 2 representative subjects that exhibited that module (AB8 unless indicated as AB2). The lines show the mean module activation across the gait cycle (5% bins) for self-selected walking trials.

Figure 5. Motor modules and activations exhibited during overground walking in a representative subject with iSCI

Modules and activations from a representative iSCI subject (SCI4) who exhibited 4 modules, the mean number for iSCI subjects. As in Figure 4, bar plots represent the muscle contributions to each module and line plots show the corresponding mean activations across the gait cycle. Modules were assigned the same color and functional label if they were statistically similar to those shown in Figure 4 (r

Figure 6. Modules differ between subject groups in number, composition, and activation

Comparison of modules and activations for a representative AB (AB6) and iSCI (SCI6) matched pair. SCI6 modules were considered similar and aligned to AB6 modules if r > 0.532. The r-values for each module and activation represent the similarity to AB#. Colors and functional labels indicate similarity to as described for Figure 4. The gray modules were dissimilar in the Figure 4 comparison but aligned when only compared to AB6’s hip flexion module.

Figure 7. AB subjects reduce their module number and activation when walking at matching iSCI cadence and assistive device

A) Modules extracted from muscle coordination patterns during walking at self-selected cadences (112 steps per minute) for a representative subject (AB6) compared to modules extracted from the ABmatch condition of walking for that same subject (38 steps per minute with loftstrand crutches). Module number was reduced. B) Modules (left) exhibited by a representative subject (AB8) walking at self-selected cadences. Module activations required to reconstruct muscle coordination during the self-selected condition (middle, 110 steps per minute) versus the cadence and assistive device match condition (right, 26 steps per minute with rolling walker). All activations were reduced, particularly during stance. Colors and functional labels again indicate similarity to those shown in Figure 4.

Figure 8. Motor module number versus overground self-selected cadence in subjects with iSCI and age-matched controls

Linear regression models were used to describe the relationship between self-selected cadence and module number for AB subjects walking at self-selected cadence, subjects with iSCI walking at self-selected cadence, and AB subjects walking at matched iSCI cadences and assistive devices (ABmatch). Data are pooled across all subjects. Data from AB subjects are represented with open circles, data from iSCI subjects are represented as black circles, and data from ABmatch subjects are represented with gray circles. Thin dashed lines above and below the regression line define 95% confidence intervals. The model was significant for describing a relationship between self-selected cadence and motor module number (r2 = 0.4; p < 0.003).