Common muscle synergies for balance and walking

Abstract

Little is known about the integration of neural mechanisms for balance and locomotion. Muscle synergies have been studied independently in standing balance and walking, but not compared. Here, we hypothesized that reactive balance and walking are mediated by a common set of lower-limb muscle synergies. In humans, we examined muscle activity during multidirectional support-surface perturbations during standing and walking, as well as unperturbed walking at two speeds. We show that most muscle synergies used in perturbations responses during standing were also used in perturbation responses during walking, suggesting common neural mechanisms for reactive balance across different contexts. We also show that most muscle synergies using in reactive balance were also used during unperturbed walking, suggesting that neural circuits mediating locomotion and reactive balance recruit a common set of muscle synergies to achieve task-level goals. Differences in muscle synergies across conditions reflected differences in the biomechanical demands of the tasks. For example, muscle synergies specific to walking perturbations may reflect biomechanical challenges associated with single limb stance, and muscle synergies used during sagittal balance recovery in standing but not walking were consistent with maintaining the different desired center of mass motions in standing vs. walking. Thus, muscle synergies specifying spatial organization of muscle activation patterns may define a repertoire of biomechanical subtasks available to different neural circuits governing walking and reactive balance and may be recruited based on task-level goals. Muscle synergy analysis may aid in dissociating deficits in spatial vs. temporal organization of muscle activity in motor deficits. Muscle synergy analysis may also provide a more generalizable assessment of motor function by identifying whether common modular mechanisms are impaired across the performance of multiple motor tasks.

Keywords: electromyography; locomotion; motor control; muscle synergy; posture.

Figure 1

Examples of EMG activity in perturbation responses during (A) standing, (B) slow walking, and (C) self-selected speed walking. Responses to a forward and leftward perturbation of the support surface during each condition are shown. Balance perturbations were induced by ramp-and-hold displacement perturbations in 12 evenly spaced directions in the horizontal plane. EMG responses occur 100-ms after the onset of platform motion (vertical dashed line). Shown here are erector spinae (ERSP), gluteus medius (GMED), tensor fascia lata (TFL), rectus femoris (RFEM), vastus medialis (VMED), biceps femoris (BFLH), medial gastrocnemius (MGAS), soleus (SOL), peroneus (PERO), and tibialis anterior (TA) responses. Mean EMG activity was calculated for 3 time bins during the automatic postural response (PR), indicated by the red shaded region, beginning 100 ms (PR1), 175 ms (PR2), and 250 ms (PR3) following perturbation. One complete gait cycle is shown for each walking speed, and the horizontal bar indicates stance (gray) and swing (white) phase. Perturbations during walking were administered in early stance.

Figure 2

Lateral gastrocnemius (LGAS), medial gastrocnemius (MGAS), peroneus (PERO), and tibialis anterior (TA) activity during perturbation responses during standing (black), slow walking (green), and self-selected walking (blue), for (A) a rightward perturbation, (B) a forward perturbation, (C) a leftward perturbation, and (D) a backward perturbation. Vertical dashed line indicates perturbation onset and the red shaded box indicates the perturbation response time window used here for analysis: 100–325 ms after perturbation onset. For walking trials, the horizontal bar indicates stance (gray) and swing (white) phases. Muscle activity was averaged across each of 3 time bins during the postural response time window and plotted against perturbation direction to generate tuning curves shown in Figure 3.

Figure 3

Muscle tuning curves from perturbation responses during standing, slow walking, and self-selected walking speeds for a representative subject. Shown are the mean tuning curves ± standard deviations in PR1 across trials in each perturbation direction. Some muscles have consistent tuning across perturbation conditions (standing, slow walking, self-selected walking), while other muscles have different tuning across conditions.

Figure 4

Muscles synergies extracted from each experimental condition. (A) Muscle synergies extracted from perturbation responses during standing, slow walking, and self-selected walking. All but one of the muscle synergies used in slow walking perturbation responses was similar to those used in standing balance postural responses. All but one of the muscle synergies used in self-selected walking perturbation responses was similar to those used in standing and/or slow walking postural responses. Correlations between each muscle synergy vector and the corresponding muscle synergy from standing balance are shown. (B) Muscle synergies extracted from unperturbed walking. Muscle synergies extracted from standing balance perturbation responses were similar to those extracted from the entire timecourse of many trials of unperturbed walking. In this subject, one additional muscle synergy was identified from unperturbed walking that was not identified in standing postural responses.

Figure 5

Recruitment of muscle synergies common to perturbation responses during standing and walking. W₁, W₂, and W₃ were used in (A) standing perturbation responses as well as perturbation responses during (B) slow and (C) self-selected walking. W₂ was recruited for backward perturbations in all conditions, whereas W₃ was recruited for medial/lateral perturbations. W₁ was recruited for anterior/posterior perturbations in standing perturbation responses, and for anterior and lateral perturbations in walking perturbation responses.

Figure 6

Recruitment of muscle synergies identified in perturbation responses during standing but not walking. Muscle synergies used in standing perturbation responses that were not used in walking perturbation responses were recruited for (A) backward or (B) forward perturbation directions, shown for two different subjects.

Figure 7

Recruitment of muscle synergies identified in perturbation responses during walking but not standing. Muscle synergies used in walking perturbation responses that were not used in standing perturbation responses were recruited for (A) leftward or (B) rightward perturbation directions, shown for two different subjects.

Figure 8

Recruitment of muscle synergies identified in unperturbed walking. Ww₆ was identified from unperturbed walking but not during perturbation responses in any condition. Shown are the recruitment coefficients for a single trial of unperturbed walking at the self-selected speed. The gray boxes indicate stance phase.