The Neuromuscular Origins of Kinematic Variability during Perturbed Walking

Abstract

We investigated the neuromuscular contributions to kinematic variability and thus step to step adjustments in posture and foot placement across a range of walking speeds in response to optical flow perturbations of different amplitudes using a custom virtual environment. We found that perturbations significantly increased step width, decreased step length, and elicited larger trunk sway compared to normal walking. However, perturbation-induced effects on the corresponding variabilities of these measurements were much more profound. Consistent with our hypotheses, we found that: (1) perturbations increased EMG activity of the gluteus medius and postural control muscles during leg swing, and increased antagonist leg muscle coactivation during limb loading in early stance, and (2) changes in the magnitude of step to step adjustments in postural sway and lateral foot placement positively correlated with those of postural control and gluteus medius muscle activities, respectively, in response to perturbations. However, (3) interactions between walking speed and susceptibility to perturbations, when present, were more complex than anticipated. Our study provides important mechanistic neuromuscular insight into walking balance control and important reference values for the emergence of balance impairment.

Conflict of interest statement

The authors declare that they have no competing interests.

Figures

Figure 1

(A) Subjects walked in an immersive virtual environment while watching a hallway with and without continuous mediolateral optical flow perturbations. Group average (±standard deviation) foot placement and trunk kinematic (B) magnitudes and (C) variabilities across the three walking speeds during normal and visually perturbed walking. Asterisks (*) indicate significantly different from normal, unperturbed walking in Tukey’s post-hoc pairwise comparisons (p < 0.05). SW: Step width; SL: Step length; SWV: Step width variability; SLV: Step length variability.

Figure 2

Perturbation-induced changes in lower leg muscle activities. Group average electromyographic (EMG) recordings from the lower leg muscles during normal (±standard error) and visually perturbed walking as a function of the gait cycle. Amplitudes are normalized to the mean values over a complete stride walking normally at 1.25 m/s. Solid horizontal lines with numerical indicators represent gait cycle phases with significant main effects of perturbation amplitude (p A) TA: Tibalis anterior; (B) MG: Medial gastrocnemius; (C) SOL: Soleus; (D) PL: Peroneus longus.

Figure 3

Perturbation-induced changes in upper leg muscle activities. Group average electromyographic (EMG) recordings from the thigh muscles during normal (±standard error) and visually perturbed walking as a function of the gait cycle. Amplitudes are normalized to the mean values over a complete stride walking normally at 1.25 m/s. Solid horizontal lines with numerical indicators represent gait cycle phases with significant main effects of perturbation amplitude (p A) GM: Gluteus medius; (B) MH: Medial hamstring; (C) VL: vastus lateralis.

Figure 4

Perturbation-induced changes in postural control muscle activities. Group average electromyographic (EMG) recordings from postural control muscles during normal (±standard error) and visually perturbed walking as a function of the gait cycle. Amplitudes are normalized to the mean values over a complete stride walking normally at 1.25 m/s. Solid horizontal lines with numerical indicators represent gait cycle phases with significant main effects of perturbation amplitude (p A) EO: External oblique; (B) ES: Erector spinae.

Figure 5

Correlations between changes in step width variability (SWV) and those in gluteus medius (GM) activity during (A) terminal swing, (B) midstance, and (C) early stance, pooled across walking speeds and perturbation amplitudes.

Figure 6

Correlations between changes in postural sway variability and those in (A) external oblique (EO) and (B) gluteus medius (GM) activity, both during terminal swing. (C) Correlations between concurrent changes in gluteus medius (GM) activity and those in external oblique (EO) activity during terminal swing. All correlations pooled across walking speeds and perturbation amplitudes.