Small directional treadmill perturbations induce differential gait stability adaptation

Abstract

Introducing unexpected perturbations to challenge gait stability is an effective approach to investigate balance control strategies. Little is known about the extent to which people can respond to small perturbations during walking. This study aimed to determine how subjects adapted gait stability to multidirectional perturbations with small magnitudes applied on a stride-by-stride basis. Ten healthy young subjects walked on a treadmill that either briefly decelerated belt speed ("stick"), accelerated belt speed ("slip"), or shifted the platform medial-laterally at right leg mid-stance. We quantified gait stability adaptation in both anterior-posterior and medial-lateral directions using margin of stability and its components, base of support, and extrapolated center of mass. Gait stability was disrupted upon initially experiencing the small perturbations as margin of stability decreased in the stick, slip, and medial shift perturbations and increased in the lateral shift perturbation. Gait stability metrics were generally disrupted more for perturbations in the coincident direction. Subjects employed both feedback and feedforward strategies in response to the small perturbations, but mostly used feedback strategies during adaptation. Subjects primarily used base of support (foot placement) control in the lateral shift perturbation and extrapolated center of mass control in the slip and medial shift perturbations. These findings provide new knowledge about the extent of gait stability adaptation to small magnitude perturbations applied on a stride-by-stride basis and reveal potential new approaches for balance training interventions to target foot placement and center of mass control.NEW & NOTEWORTHY Little is known about if and how humans can adapt to small magnitude perturbations experienced on a stride-by-stride basis during walking. Here, we show that even small perturbations disrupted gait stability and that subjects could still adapt their reactive balance control. Depending on the perturbation direction, subjects might prefer adjusting their foot placement over their center of mass and vice versa. These findings could help potentially tune balance training to target specific aspects of balance.

Keywords: adaptation; balance; gait; margin of stability; perturbation.

Graphical abstract

Figure 1.

Schematic of the perturbations and experimental protocol. A: perturbation onset occurred at right leg mid-stance (black leg in red outline). There were 4 perturbation directions, and 2 sizes for the anterior-posterior perturbations, for a total of six perturbation conditions. The red arrows are the initial relative surface displacements, and the faded red arrows are the displacements to return to the unperturbed state. B: the left belt speed was fixed at 1.0 m/s (blue). For the Stick0.2 and Stick0.4 perturbations, the right belt speed (red) decelerated to 0.8 m/s and 0.6 m/s, respectively, and then returned to the tied belt speed. For the Slip0.2 and Slip0.4 perturbations, the right belt speed accelerated to 1.2 m/s and 1.4 m/s, respectively, and then returned to the tied belt speed. For the lateral (L1) and medial (M1) perturbations, the treadmill shifted 1 cm laterally and medially, respectively, and then returned to neutral. The perturbations were ∼400 ms in duration. Gait events: right heel strike (rhs), left toe off (lto), left heel strike (lhs), and right toe off (rto). C: blocks of the experimental protocol. Each trial started with a 2-min unperturbed walking block (pre), followed by a 4-min perturbed walking block (perturbation), and completed with another 2-min unperturbed walking block (post). An unperturbed catch stride occurred randomly one out of every five strides during the perturbation block.

Figure 2.

Anterior-posterior and medial-lateral metrics of gait stability at left heel strike (lhs) and left toe off (lto). A: the anterior-posterior base of support (BOS_ap, orange arrow) was the anterior-posterior distance of the toe marker of the leading leg relative to the toe marker of the trailing leg. The anterior-posterior extrapolated center of mass (XCOM_ap, green arrow) was the anterior-posterior distance of XCOM relative to the toe marker of the trailing leg. The anterior-posterior margin of stability (MOS_ap, pink arrow) was the BOS_ap − XCOM_ap. B: the medial-lateral base of support (BOS_ml) was the medial-lateral distance of the ankle marker of the leading leg relative to the ankle marker of the trailing leg. The medial-lateral extrapolated center of mass (XCOM_ml) was the medial-lateral distance of XCOM relative to the ankle marker of the trailing leg. The medial-lateral margin of stability (MOS_ml) was the BOS_ml − XCOM_ml.

Figure 3.

Trajectories of the gait stability metrics [margin of stability (MOS), pink; base of support (BOS), orange, and extrapolated center of mass (XCOM), green] for specific strides of a representative subject for the Stick0.4, Slip0.4, L1, and M1 perturbations (black dotted line: the 2nd to last stride of pre; colored thick line: the 2nd stride of early perturbed; colored thin line: the 2nd to last stride of late perturbed; and black dashed line: the 2nd to last stride of post). The MOS_{ap, lhs}, BOS_{ap, lhs}, and XCOM_{ap, lhs} of the Stick0.4 and Slip0.4 perturbations, and MOS_{ml, lhs}, BOS_{ml, lhs}, and XCOM_{ml, lhs} of the lateral (L1) and medial (M1) perturbations deviated from pre at early perturbed, then MOS_lhs and BOS_lhs generally trended to the pre trajectory by late perturbed and returned to the pre trajectory by post, shown in the exploded view in the inset circles. The MOS_{ap, lto} of the Stick0.4 perturbation, BOS_{ap, lto} and XCOM_{ap, lto} of the Slip0.4 perturbation, and BOS_{ml, lto} and XCOM_{ml, lto} of the L1 perturbation deviated from pre at early perturbed, then BOS_lto and XCOM_lto trended to the pre trajectory by late perturbed and returned to the pre trajectory by post, shown in the exploded view in the inset circles. Gait events: right heel strike (rhs), left toe off (lto), left heel strike (lhs), and right toe off (rto). Dark gray area: double support phase. Light gray area: single support phase. The plots show the MOS and BOS during double support and XCOM for the entire gait cycle. ap, anterior-posterior; ml, medial-lateral.

Figure 4.

Group-averaged (mean and standard deviation indicated by thick horizontal lines and one-sided error bar, n = 10) anterior-posterior and medial-lateral margin of stability (MOS, pink), base of support (BOS, orange), and extrapolated center of mass (XCOM, green) at left heel strike and left toe off for pre, early perturbed, late perturbed, early post, and late post during the anterior-posterior perturbations and the corresponding footprints with metrics at pre, early perturbed, and late perturbed. Thick arrows indicate significant changes from the previous phase. In the group-averaged plots, circles are individual subjects. A: subjects were destabilized at early perturbed then adapted by late perturbed during the Stick0.4 perturbation. B: subjects were destabilized and adapted during the Slip0.4 perturbation. *P < 0.05 and color-coded for the specific metrics with the significant differences between phases indicated by the brackets. ap, anterior-posterior; lhs, left heel strike; lto, left toe off; ml, medial-lateral.

Figure 5.

Group-averaged (mean and standard deviation indicated by thick horizontal lines and one-sided error bar, n = 10) anterior-posterior and medial-lateral margin of stability (MOS, pink), base of support (BOS, orange), and extrapolated center of mass (XCOM, green) at left heel strike and left toe off for pre, early perturbed, late perturbed, early post, and late post during the medial-lateral perturbations and the corresponding footprints with metrics at pre, early perturbed, and late perturbed. Thick arrows indicate significant changes from the previous phase. In the group-averaged plots, circles are individual subjects. A: subjects adapted to the lateral (L1) perturbation after initially being disrupted. B: subjects adapted to the medial (M1) perturbation after initially being disrupted. *P < 0.05 and color-coded for the specific metrics with the significant differences between phases indicated by the brackets. ap, anterior-posterior; lhs, left heel strike; lto, left toe off; ml, medial-lateral.

Figure 6.

Group-averaged (mean and standard deviation, n = 10) |Δ left heel strike base of support (BOS_lhs)| (orange) compared with |Δ left heel strike extrapolated center of mass (XCOM_lhs)| (green) during disruption (pre to early perturbed) and adaptation (early to late perturbed). Gray lines between bars are individual subjects. A: during disruption, BOS_lhs was disrupted more by the Stick0.4 perturbation, XCOM_lhs was disrupted more by the Slip0.4 and M1 perturbations. B: during adaptation, BOS_{ap, lhs} adapted more in the L1 perturbation, XCOM_{ap, lhs} adapted more in the Slip0.4 and M1 perturbations, BOS_{ml, lhs} adapted more in the L1 perturbation. *P < 0.05 and significant differences between |ΔBOS_lhs| and |ΔXCOM_lhs|. ap, anterior-posterior; ml, medial-lateral.

Figure 7.

Group-averaged (mean and standard deviation indicated by thick horizontal lines and one-sided error bar, n = 10) anterior-posterior and medial-lateral margin of stability (MOS, pink), base of support (BOS, orange), and extrapolated center of mass (XCOM, green) at left heel strike and left toe off for pre, early catch, late catch for the Stick0.4, Slip0.4, lateral (L1), and medial (M1) perturbations. Circles are individual subjects. Stick0.4 perturbation (A), Slip0.4 perturbation (B), L1 perturbation (C), and M1 perturbation (D) induced anticipatory responses at early catch, but subjects did not use more feedforward strategies by late catch. *P < 0.05 and color-coded for the specific metrics with the significant differences between phases indicated by the brackets. ap, anterior-posterior; lhs, left heel strike; lto, left toe off; ml, medial-lateral.

Figure 8.

Group-averaged (mean and standard deviation, n = 10) Δ left heel strike margin of stability (MOS_lhs, pink), Δ left heel strike base of support (BOS_lhs, orange), Δ left heel strike extrapolated center of mass (XCOM_lhs, green) during disruption (early perturbed minus pre) and adaptation (late minus early perturbed) for the Stick0.4 (black outline), Slip0.4 (gray outline), L1 (white fill), and M1 (gray fill) perturbations. Circles are individual subjects. A: anterior-posterior metrics at left heel strike were more sensitive to the anterior-posterior perturbations during disruption but not adaptation. B: MOS_{ml, lhs} and XCOM_{ml, lhs} were more sensitive to the medial-lateral perturbations during disruption but not adaptation. *With thick brackets: P < 0.05 and significant same signed differences between two perturbation conditions; *with thin brackets: P < 0.05 and significant opposite signed differences between two perturbation conditions. ap, anterior-posterior; ml, medial-lateral.

Figure 9.

Group-averaged (mean and standard deviation, n = 10) |Δ left heel strike margin of stability (MOS_lhs)| (pink), |Δ left heel strike base of support (BOS_lhs)| (orange), |Δ left heel strike extrapolated center of mass (XCOM_lhs)| (green) during disruption (pre to early perturbed) and adaptation (early to late perturbed) for the anterior-posterior perturbations. Dark bars indicate the regular size perturbations (Stick0.4 and Slip0.4) and light bars indicate the half-size perturbations (Stick0.2 and Slip0.2). Colored lines between bars are individual subjects. A: anterior-posterior metrics at left heel strike scaled with perturbation size during disruption but not adaptation. B: medial-lateral metrics at left heel strike did not scale with perturbation size during disruption and adaptation. +P < 0.05, perturbation size effect (perturbation condition effect was not reported). #P < 0.05, interaction effect between perturbation size (regular, 0.4; half-size, 0.2) and perturbation condition (stick, slip). *P < 0.025, significant differences between the regular and half-size perturbations of same condition. ap, anterior-posterior; ml, medial-lateral.