Motor module generalization across balance and walking is impaired after stroke

Abstract

Muscle coordination is often impaired after stroke, leading to deficits in the control of walking and balance. In this study, we examined features of muscle coordination associated with reduced walking performance in chronic stroke survivors using motor module (a.k.a. muscle synergy) analysis. We identified differences between stroke survivors and age-similar neurotypical controls in the modular control of both overground walking and standing reactive balance. In contrast to previous studies that demonstrated reduced motor module number poststroke, our cohort of stroke survivors did not exhibit a reduction in motor module number compared with controls during either walking or reactive balance. Instead, the pool of motor modules common to walking and reactive balance was smaller, suggesting reduced generalizability of motor module function across behaviors. The motor modules common to walking and reactive balance tended to be less variable and more distinct, suggesting more reliable output compared with motor modules specific to either behavior. Greater motor module generalization in stroke survivors was associated with faster walking speed, more normal step length asymmetry, and narrower step widths. Our work is the first to show that motor module generalization across walking and balance may help to distinguish important and clinically relevant differences in walking performance across stroke survivors that would have been overlooked by examining only a single behavior. Finally, because similar relationships between motor module generalization and walking performance have been demonstrated in healthy young adults and individuals with Parkinson's disease, this suggests that motor module generalization across walking and balance may be important for well-coordinated walking. NEW & NOTEWORTHY This is the first work to simultaneously examine neuromuscular control of walking and standing reactive balance in stroke survivors. We show that motor module generalization across these behaviors (i.e., recruiting common motor modules) is reduced compared with controls and is associated with slower walking speeds, asymmetric step lengths, and larger step widths. This is true despite no between-group differences in module number, suggesting that motor module generalization across walking and balance is important for well-coordinated walking.

Keywords: electromyography; gait; muscle coordination; muscle synergy; postural control.

Fig. 1.

Example processed electromyography (EMG) from select muscles during overground walking and reactive balance. A: muscle activity for walking was recorded while participants walked overground at their self-selected speed for at least 3 trials over a 25-ft walkway. Dashed lines represent right heel strikes. For each trial, only data from the middle 20 ft of the 25-ft walkway were analyzed (represented by shaded region) to avoid the effects of gait initiation and termination. 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 is 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 ~150 ms after perturbation onset (denoted by vertical 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 (3 trials × 12 directions × 4 time bins = 144). TFL-R, tensor fascia lata; LGAS-R, lateral gastrocnemius; TA-R, tibialis anterior.

Fig. 2.

Motor module number and generalization across walking and reactive balance. A: representative motor modules from a control subject during walking (left) and reactive balance (right). Motor modules were extracted from each behavior independently and identified as shared across behaviors if r > 0.708. B: the number of motor modules recruited during overground walking (top) and reactive balance (bottom) did not differ between control (C; n = 16), nonparetic (N; n = 9), and paretic legs (P; n = 9). C: the percentage of shared motor modules was decreased in both the nonparetic and paretic legs compared with control legs. Sharing across behaviors was quantified as a percentage of total number of unique motor modules (i.e., 40% of the motor modules, or 2 of 5, were shared across behaviors in the representative subject in A). #P < 0.1. GMAX, gluteus maximus; GMED, gluteus medius; TFL, tensor fascia lata; ADMG, adductor magnus; BFLH, biceps femoris long head; RFEM, rectus femoris; VLAT, vastus lateralis; MGAS, medial gastrocnemius; LGAS, lateral gastrocnemius; SOL, soleus; PERO, peroneus longus; TA, tibialis anterior.

Fig. 3.

Motor module variability and distinctness. A: a 2-dimensional (i.e., 2 muscles) example of motor module variability and distinctness calculation. Left: colored bars for each muscle weighting represent the contribution of each 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 represents 1 of the 100 resampled motor modules as depicted on left. Motor module variability (W_var) is defined as the radius encompassing 95% of the resampled points (dashed circle), and motor module distinctness (W_dis) is the average distance between each cluster (solid line). B and C: motor module variability and distinctness did not differ between control (C; n = 16), nonparetic (N; n = 9), and paretic legs (P; n = 9) in either walking (top) or reactive balance (middle). However, in all legs, the motor modules that were shared across the two behaviors exhibited less variability and were more distinct than those that were recruited in only one of the behaviors (bottom). *P < 0.05; #P < 0.1. Musc., muscle.

Fig. 4.

Motor module timing variability. A: example motor module recruitment timing and calculation of module timing variability (C_var). For walking (left), C_var was calculated as the root mean square error (RMSE) of the timing curve across gait cycles. For reactive balance (right), C_var was calculated as the RMSE of the timing curve across perturbation directions (12 directions) and time bins [4 time bins: background and automatic postural response (APR) 1, APR2, and APR3]. Gray lines represent individual gait cycles for walking or trials for reactive balance. B: C_var during walking (left) was increased in the nonparetic leg (N; n = 8) compared with both the paretic (P; n = 8) and control legs (C; n = 16). No differences were identified between legs during reactive balance (middle). No differences were identified between modules that were shared across the two behaviors compared with those that were recruited in only one of the behaviors (right). *P < 0.05.

Fig. 5.

Structure of motor modules shared across walking and reactive balance. Three unique motor modules were identified across all legs as shared across behaviors. The numbers at right indicate in how many legs per group (control, nonparetic, paretic) each of these motor modules were present. GMAX, gluteus maximus; GMED, gluteus medius; TFL, tensor fascia lata; ADMG, adductor magnus; BFLH, biceps femoris long head; RFEM, rectus femoris; VLAT, vastus lateralis; MGAS, medial gastrocnemius; LGAS, lateral gastrocnemius; SOL, soleus; PERO, peroneus longus; TA, tibialis anterior.

Fig. 6.

Association between measures of walking performance and overall motor module generalization and recruitment of shared modules 1–3 in the paretic leg of individuals poststroke (S1–S9). Module numbers correspond to the shared modules identified across all subjects illustrated in Fig. 5. A: motor module generalization was positively correlated with walking speed and negatively correlated with step width and step length asymmetry. B: recruitment of a module that resembled shared module 1 was associated with increased walking speed, reduced step width, and reduced step length asymmetry (e.g., values becoming closer to 0.5, which represents perfect symmetry of step lengths). C: recruitment of a module that resembled shared module 2 was associated with reduced step width, step length asymmetry, and stride time variability. D: recruitment of a module that resembled shared module 3 was associated with decreased walking speed, increased step length asymmetry, and increased stride time variability. Symmetric step lengths occur at values of 0.5, and values above symmetry occur due to longer paretic than nonparetic steps.

Fig. 7.

Example stroke survivor data illustrating merged plantarflexor module during walking but independent recruitment of the plantarflexors during reactive balance. GMAX, gluteus maximus; GMED, gluteus medius; TFL, tensor fascia lata; ADMG, adductor magnus; BFLH, biceps femoris long head; RFEM, rectus femoris; VLAT, vastus lateralis; MGAS, medial gastrocnemius; LGAS, lateral gastrocnemius; SOL, soleus; PERO, peroneus longus; TA, tibialis anterior.