Increased neuromuscular consistency in gait and balance after partnered, dance-based rehabilitation in Parkinson's disease

Abstract

Here we examined changes in muscle coordination associated with improved motor performance after partnered, dance-based rehabilitation in individuals with mild to moderate idiopathic Parkinson's disease. Using motor module (a.k.a. muscle synergy) analysis, we identified changes in the modular control of overground walking and standing reactive balance that accompanied clinically meaningful improvements in behavioral measures of balance, gait, and disease symptoms after 3 wk of daily Adapted Tango classes. In contrast to previous studies that revealed a positive association between motor module number and motor performance, none of the six participants in this pilot study increased motor module number despite improvements in behavioral measures of balance and gait performance. Instead, motor modules were more consistently recruited and distinctly organized immediately after rehabilitation, suggesting more reliable motor output. Furthermore, the pool of motor modules shared between walking and reactive balance increased after rehabilitation, suggesting greater generalizability of motor module function across tasks. Our work is the first to show that motor module distinctness, consistency, and generalizability are more sensitive to improvements in gait and balance function after short-term rehabilitation than motor module number. Moreover, as similar differences in motor module distinctness, consistency, and generalizability have been demonstrated previously in healthy young adults with and without long-term motor training, our work suggests commonalities in the structure of muscle coordination associated with differences in motor performance across the spectrum from motor impairment to expertise.NEW & NOTEWORTHY We demonstrate changes in neuromuscular control of gait and balance in individuals with Parkinson's disease after short-term, dance-based rehabilitation. Our work is the first to show that motor module distinctness, consistency, and generalizability across gait and balance are more sensitive than motor module number to improvements in motor performance following short-term rehabilitation. Our results indicate commonalities in muscle coordination improvements associated with motor skill reacquisition due to rehabilitation and motor skill acquisition in healthy individuals.

Keywords: dance; electromyography; exercise; muscle coordination; muscle synergy.

Fig. 1.

Example processed EMG from select muscles during overground walking (A) and reactive balance (B). A: muscle activity for walking was recorded while participants walked overground at their self-selected speed for at least 3 trials of 7.5 m each. For each trial, the first and last gait cycles were removed to avoid gait initiation and termination. Dashed lines represent right heel strikes, and the shaded region represents the gait cycles analyzed for 1 trial. Data from all trials for a subject were concatenated before motor module extraction to form an m × t data matrix, where m is the number of muscles and t the number of time points across all trials. B: muscle activity for reactive balance was assessed through ramp-and-hold perturbations in 12 evenly spaced directions. Left: responses to backward, forward, and leftward perturbations are illustrated. EMG responses occurred ~120–150 ms after perturbation onset (denoted by vertical dashed lines). Mean EMG activity was calculated during a background period before the perturbation and during three 75-ms time bins during the automatic postural response (APR, shaded regions). Right: tuning curves of mean muscle activity from perturbation responses as a function of perturbation directions for the first APR bin. Before motor module extraction, the tuning curves were assembled to form an m × t data matrix, where m is the number of muscles and t the number of data points (3 trials × 12 directions × 4 time bins = 144).

Fig. 2.

Number of motor modules and goodness of fit in overground walking (A) and reactive balance (B). Left: the number of motor modules (mean ± SD) recruited during overground walking and reactive balance either decreased or remained the same after Adapted Tango (AT) rehabilitation. Connected circles denote the numbers of motor modules for each subject before and after AT rehabilitation. Center: the number of motor modules selected accounted for ≥90% of the overall variability accounted for (VAF) as depicted by plots from an example subject. Right: EMG signals were well reconstructed with the extracted motor modules in both walking and reactive balance as depicted in the example original vs. reconstructed EMG plots from a representative subject (light solid lines, original EMG; dark dashed lines, reconstructed EMG).

Fig. 3.

Motor module sharing and coactivity in overground walking and reactive balance. A: representative motor modules during walking (left) and reactive balance (right). Motor modules were extracted from each behavior independently. Motor modules that were identified as similar between tasks are represented with the same color across tasks. B: % of motor modules shared between walking and reactive balance increased from before (Pre) to after (Post) AT rehabilitation in 5 of the 6 participants. Connected circles denote the value for each participant. Shared motor modules are those pairs of motor modules across behaviors in which r ≥ 0.684. Amount of sharing was quantified as % of total number of unique motor modules (i.e., 42.9% of the motor modules, or 3 of 7, were shared across behaviors in the representative subject in A). C: motor module coactivity increase from before (Pre) to after (Post) AT rehabilitation in both walking and reactive balance in most participants. Motor module coactivity was quantified as the average number of significantly active muscles per module (W_mus). Significantly active muscles represent those whose activation was consistently >0, despite variations over movement repetitions, and muscles were classified as significantly active if their 95% CI did not include 0, whereas nonsignificantly active muscle had 95% CIs that included 0 (i.e., filled bars with solid borders vs. open bars with dashed borders in the representative motor modules in A).

Fig. 4.

Spatial motor module variability and distinctness. Example motor modules and cluster plots for walking before rehabilitation (A) and after rehabilitation (B) depicting motor module consistency (R95) and distinctness (d). Left: colored bars for each muscle weighting represent the contribution of a muscle within a module over each of the 100 different resampled module extractions. Black bars indicate the mean across all resampled extractions. Right: each point in a cluster is a 2-dimensional representation of 1 of the 100 resampled motor modules as depicted on left. C: motor module variability decreased from before (Pre) to after (Post) AT rehabilitation in most participants for both walking and reactive balance. D: motor module distinctness increased in most participants after AT rehabilitation in both walking and reactive balance. Connected circles denote the value for each participant.

Fig. 5.

Increased motor module coactivity was associated with a reduction in motor module number after AT rehabilitation. Motor module coactivity increased in those participants who decreased motor module number, whereas those participants who had no change in motor module number had only minor changes in motor module coactivity. Values for each participant for walking are represented by circles.

Fig. 6.

Examples of associations between clinical scores vs. changes in motor module metrics. The change in walking endurance (6MWT, y-axis) is illustrated for each subject vs. the change in motor module number for walking (left), motor module distinctness for walking (center), and % of motor modules shared between walking and reactive balance (right). In general, changes in motor module number did not appear related to improvements in motor performance (e.g., 6MWT). In contrast, other motor module metrics (e.g., distinctness and % shared across tasks) demonstrated trends such that increases in these metrics were in general accompanied by increases in motor performance. Values for each participant are represented by closed circles. Shaded regions denote where there is an increase in both the clinical score and the motor module metric.