A neuromechanical strategy for mediolateral foot placement in walking humans

Abstract

Stability is an important concern during human walking and can limit mobility in clinical populations. Mediolateral stability can be efficiently controlled through appropriate foot placement, although the underlying neuromechanical strategy is unclear. We hypothesized that humans control mediolateral foot placement through swing leg muscle activity, basing this control on the mechanical state of the contralateral stance leg. Participants walked under Unperturbed and Perturbed conditions, in which foot placement was intermittently perturbed by moving the right leg medially or laterally during the swing phase (by ∼50-100 mm). We quantified mediolateral foot placement, electromyographic activity of frontal-plane hip muscles, and stance leg mechanical state. During Unperturbed walking, greater swing-phase gluteus medius (GM) activity was associated with more lateral foot placement. Increases in GM activity were most strongly predicted by increased mediolateral displacement between the center of mass (CoM) and the contralateral stance foot. The Perturbed walking results indicated a causal relationship between stance leg mechanics and swing-phase GM activity. Perturbations that reduced the mediolateral CoM displacement from the stance foot caused reductions in swing-phase GM activity and more medial foot placement. Conversely, increases in mediolateral CoM displacement caused increased swing-phase GM activity and more lateral foot placement. Under both Unperturbed and Perturbed conditions, humans controlled their mediolateral foot placement by modulating swing-phase muscle activity in response to the mechanical state of the contralateral leg. This strategy may be disrupted in clinical populations with a reduced ability to modulate muscle activity or sense their body's mechanical state.

Keywords: biomechanics; locomotion; muscle activity; stability.

Fig. 1.

Spatiotemporal gait characteristics and patterns of muscle activity were quantified during Unperturbed and Perturbed walking. A: mediolateral swing foot displacement (x_swf) was measured as the mediolateral distance from the sacrum to the swing heel. Center of mass displacement (x_CoM) was measured as the mediolateral distance from the stance heel to the sacrum. For all steps, the positive direction was defined as the direction toward the swing foot. B: the gluteus medius (GM) activity pattern during Unperturbed walking is illustrated for a typical participant. The GM was most strongly active during stance but also exhibited a burst of activity during the first half of swing in some strides (boxed area). Individual strides (n = 250) are shown as thin lines, and the average stride is shown as a thick dark line. C: Unperturbed adductor magnus (AM) activity is illustrated for a typical participant. The AM was consistently active in the second half of swing (boxed area) and typically also exhibited smaller bursts of activity during early and late stance. Again, the thick dark line indicates the average of the illustrated 250 strides. D: during Perturbed walking, periods of gait were classified on the basis of their timing relative to the perturbation, as illustrated in a simple schematic. Steps were defined using heel-strike events from both legs (i.e., a right step was defined as the period from left heel strike to the next right heel strike). Strides were defined using heel-strike events from a single leg (i.e., from left heel strike to the next left heel strike) and were divided into stance and swing phases depending on whether this leg was on the ground. Perturbations were applied to the right leg during a right step (R₀ step), while the left leg was in stance (L₀ stance) and the right leg was in swing (R₀ swing). Negatively labeled strides (e.g., L₋₁) occur before the perturbation, while positively labeled strides (e.g., R₁) occur after the perturbation.

Fig. 2.

Several measures of gait kinematics and muscle activity were associated with the subsequent foot placement. A: mediolateral foot placement was significantly associated with swing-phase GM activity (GM_sw), swing-phase AM activity (AM_sw), and the initial mechanical state of the swing leg [x_swf, swing foot velocity (v_swf), swing foot acceleration (a_swf)]. Error bars represent SE. *Significant effect (P < 0.05). B: active strides were defined by early swing GM activity (boxed area) exceeding 2 SDs above the minimal EMG level during a stride. Inactive strides were defined by early swing GM activity remaining within 1 SD of this minimal value. C: Active and Inactive strides were paired on the basis of the initial mechanical state of the swing leg (at ∼60% gait cycle). The mediolateral (ML) location of the swing foot is plotted with respect to the final position of the CoM. During Active strides, the swing foot landed more laterally. For B and C, the lines represent averages and the shaded area represents 2 SDs around the average Inactive stride.

Fig. 3.

Characteristics of the stance leg and torso were associated with swing-phase GM activity in the contralateral leg. A: swing-phase GM activity was significantly associated with mediolateral CoM displacement (x_CoM), velocity (v_CoM), and acceleration (a_CoM), as well as by the simultaneous stance-phase GM activity in the contralateral leg (GM_st). Error bars represent SE. *Significant effect (P < 0.05). B: for a single participant, GM activity is illustrated for Active and Inactive strides. C: the CoM is farther from the stance foot throughout the Active strides. D: GM activity of the contralateral stance leg is higher during the Active strides than during the Inactive strides. For B–D, the lines represent averages and the shaded area represents 2 SDs around the average Inactive stride.

Fig. 4.

Perturbations influenced subsequent spatiotemporal gait characteristics. A: for a single participant, the effects of medial (top) and lateral (bottom) perturbations on the mediolateral locations of the left foot, CoM, and right foot are illustrated over 6 consecutive steps. Each trace illustrates the average response to the (∼20) perturbations delivered during a trial. Exclamation marks (!) indicate the approximate time when perturbations were applied. Right steps are shaded, and the vertical arrows indicate the measured mediolateral foot placements, defined as the mediolateral distance from the CoM to the foot at the time of heel strike. For simplicity, each step is illustrated as having the same duration. B: mediolateral foot placement was predictably influenced by both medial and lateral perturbations. The plotted values correspond to the average lengths of the vertical arrows illustrated in A across all participants. For clarity, left foot placement is plotted as positive while right foot placement is plotted as negative. C: step period was affected by medial and lateral perturbations, as the perturbed step consistently had a longer step period. For B and C, the vertical dashed line indicates the perturbed right step (R₀), in which the foot is moved either medially or laterally during swing. For each participant, we calculated the average values for these gait spatiotemporal metrics preceding and following the applied perturbations. Here, the dot locations indicate mean values and the error bars represent SDs of these values across all 10 participants. *Magnitude significantly greater than steady state, #magnitude significantly less than steady state (P < 0.05; post hoc t-tests).

Fig. 5.

Perturbations also influenced bilateral GM activity. A: for a single participant, the muscle activity during 3 consecutive right strides is illustrated for both legs, corresponding to the same time period illustrated in Fig. 4. Again, each trace illustrates the average response to the applied perturbations. For each leg, stance phases are indicated by shaded areas. Perturbations (indicated by exclamation marks) were delivered to the right leg when this leg was in swing (R₀ swing) and the left leg was in stance (L₀ stance). B: across participants, perturbations influenced right GM activity during both the perturbed stride and the subsequent stride. Generally, lateral and medial perturbations had opposite effects. C: perturbations also influenced the left GM activity. Most notably, after perturbations of the right leg the next swing phase with the left leg demonstrated substantial changes in GM activity. B and C: *significant increase in muscle activity relative to strides without a perturbation, ^#significant decrease (P < 0.05; post hoc t-tests).