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. 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.

Motor module generalization across balance and walking is reduced after stroke

“…Indeed, we recently observed greater motor module consistency and distinctness during a balance-challenging walking behavior among expert professional ballet dancers compared with novice nondancers (Sawers et al 2015). Similarly, we found that improved gait and balance performance after rehabilitation in individuals with Parkinson's disease was associated not with increased module complexity but increased consistency and distinctness (Allen et al 2017). Although it is well-established that stroke survivors walk with increased step-to-step variability (e.g., spatiotemporal variability, Balasubramanian et al 2009), whether reduced motor performance is stroke survivors is accompanied by reduction in motor module consistency and distinctness is unknown.…”

“…To date, motor module analysis for lower limb muscle coordination post-stroke has primarily focused on the number of motor modules recruited during gait behaviors. We recently utilized novel metrics of motor module consistency, distinctness, and generalization to examine other features of muscle coordination and identified differences related to gait and balance performance in both healthy adults (Sawers et al 2015) and individuals with Parkinson's disease (Allen et al 2017). However, it remains unclear how these modular features of muscle coordination are affected after stroke.…”

“…Similarly, improved walking performance after post-stroke rehabilitation can occur without increasing motor module complexity (Routson et al 2013;Hashiguchi et al 2016). To aid in distinguishing important and clinically relevant impairments in motor performance, we recently introduced novel motor module metrics of consistency and distinctness (Sawers et al 2015;Allen et al 2017). These novel metrics reflect variations in muscle coordination across different repetitions of the same behavior (e.g., from gait cycle to gait cycle for walking).…”

“…Long-term training over many years in professional ballet dancers leads to better motor performance on a balance-challenging beam-walking behavior compared to nondancers, which is associated with recruiting more common motor modules across gait and balance movement behaviors (Sawers et al 2015). On the other end of the motor expertise-impairment spectrum, individuals with Parkinson's disease exhibit lower levels of motor module generalization across gait and balance behaviors compared to healthy adults, and improvements in motor performance after rehabilitation are associated with increases in motor module generalization (Allen et al 2017). Whether motor module generalization is reduced in stroke survivors whose ability to selectively recruit appropriate patterns of muscle coordination is impaired (e.g., Clark et al 2010;Knutsson and Richards 1979;Shiavi, Bugle, and Limbird 198) remains unknown.…”

Abnormal center of mass control during balance: a new biomarker of falls in people with Parkinson’s disease

“…We were somewhat surprised that we did not find that antagonist activity in MG was abnormal in PD at the group level in this sample, given that we have previously reported excessive MG antagonist activity during balance tasks using a similar paradigm in PD patients in the ON medication state. 80 However, in a subsequent extensive examination of the activation of 6 muscles throughout the leg performed on a subset of these data, we found that the presence of PD was associated with elevated antagonist activity across generally all muscles examined, but that when muscles were considered in isolation, the effect was statistically significant only in TA. Here, although some patients exhibited strong antagonist activity in MG (see Figure S2, upper panel), others exhibited very little antagonist activity (see Figure S2, lower panel).…”