Direction-dependent control of balance during walking and standing

Abstract

Human walking has previously been described as "controlled falling." Some computational models, however, suggest that gait may also have self-stabilizing aspects requiring little CNS control. The fore-aft component of walking may even be passively stable from step to step, whereas lateral motion may be unstable and require motor control for balance, as through active foot placement. If this is the case, walking humans might rely less on integrative sensory feedback, such as vision, for anteroposterior (AP) than for mediolateral (ML) balance. We tested whether healthy humans (n=10) exhibit such direction-dependent control, by applying low-frequency perturbations to the visual field (a projected virtual hallway) and measuring foot placement during treadmill walking. We found step variability to be nearly 10 times more sensitive to ML than to AP perturbations, as quantified by the increase in root-mean-square step variability per unit change in perturbation amplitude. This is not simply due to poorer physiological sensitivity of vision in the AP direction: similar perturbations applied to quiet standing produced reversed direction dependence, with an AP sensitivity 2.3-fold greater than that of ML. Tandem (heel-to-toe) standing yielded ML sensitivity threefold greater than that of AP, suggesting that the base of support influences the stability of standing. Postural balance nevertheless appears to require continuous, integrative motor control for balance in all directions. In contrast, walking balance requires step-by-step, integrative control for balance, but mainly in the lateral direction. In the fore-aft direction, balance may be maintained through an "uncontrolled," yet passively stabilized, series of falls.

FIG. 1.

Predictions of sensitivity to visual perturbations, for walking, normal standing, and tandem standing. Previous computational models (Kuo 1999) predict that walking may have passive dynamic stability in the anteroposterior (AP) direction but instability in the mediolateral (ML) direction that is controlled with active foot placement. An indicator of active control is step variability, measured through the center of pressure (COP) under each foot. Models predict high sensitivity of ML (step width) variability to ML visual perturbations (“ML/ML sensitivity”). Ellipses denote covariance of step variability, computed from root-mean-square step deviations. The stability of standing is expected to depend on the base of support, with greater instability in the AP direction for normal standing and the ML direction for tandem (heel-to-toe) standing. Variability of continuous COP, as opposed to step-to-step COP in walking, quantifies posture control. High AP/AP sensitivity to visual perturbations is expected during normal standing and high ML/ML sensitivity during tandem standing.

FIG. 2.

Experimental setup. Subjects walked or stood on an instrumented treadmill displaying a virtual hallway moving at the same speed as the treadmill belt. Visual perturbations were superimposed on the hallway motion and their effect was measured using COP variability. Virtual reality display uses a single projector and curved rear projection screen to provide wide viewing angle and immersive feeling of moving within a tiled hallway. A split-belt treadmill recorded the instantaneous COP (dashed line).

FIG. 3.

Variability of walking as a function of AP and ML visual perturbations. Step variability data (filled circles), defined as root-mean-square (RMS) deviations of step width and length, are plotted against perturbation amplitude. Data were fit well by a linear relationship (solid lines for linear regression fits); we defined perturbation sensitivity as the change in step variability per unit change in perturbation amplitude (i.e., slope of linear fit). Step width generally exhibited greater variability than that of step length. Only ML perturbations produced significant changes in step variability. Error bars denote SD. Asterisks (*) denote significant sensitivity (P < 0.05).

FIG. 4.

Variability of normal and tandem standing as a function of AP and ML visual perturbations. COP variability data (filled circles), defined as RMS deviations in the AP and ML directions, are plotted against perturbation amplitude. Linear regression fits (solid lines) to data yield slopes quantifying sensitivity to perturbations. During normal standing (left), AP variability was generally greater than ML variability and more sensitive to visual perturbations in both directions. During tandem standing, there was greater variability than normal standing, but only the ML/ML sensitivity was significant. Error bars denote SD. Asterisks (*) denote significant sensitivity (P < 0.05).

FIG. 5.

Summary of mean perturbation sensitivities for walking, normal standing, and tandem standing. Two sensitivities are compared: ML/ML (i.e., sensitivity of ML variability to ML perturbations) and AP/AP (see Figs. 3 and 4). During walking and tandem standing, ML/ML sensitivity was significantly greater than AP/AP sensitivity (asterisks denote P < 0.05). The sensitivities were reversed for normal standing. The differential sensitivity remained in effect during walking with a nominally stationary visual field (“No Flow”), indicating that the contrast with normal standing is not due to differences in visual field motion. Walking sensitivities are consistent with model predictions of passive dynamic stability from step to step and standing results are consistent with static stability expected from the base of support.

FIG. 6.

Step width and length variability as a function of visual perturbation direction. Data points show mean and SD of RMS variability for perturbations with amplitude 0.25 m, along with ellipses fitted to these data (solid lines). Variabilities in the control conditions with no perturbations are shown for comparison (dashed circles). Step width variability was greatest for perturbations in the ML direction, whereas step length variability did not change significantly with perturbation direction.