Adaptation and generalization to opposing perturbations in walking

Abstract

Little is known on how the CNS would select its movement options when a person faces a novel or recurring perturbation of two opposing types (slip or trip) while walking. The purposes of this study were (1) to determine whether young adults' adaptation to repeated slips would interfere with their recovery from a novel trip, and (2) to investigate the generalized strategies after they were exposed to a mixed training with both types of perturbation. Thirty-two young adults were assigned to either the training group, which first underwent repeated-slip training before encountering a novel, unannounced trip while walking, or to the control group, which only experienced the same novel, unannounced trip. The former group would then experience a mix of repeated trips and slips. The results indicated that prior adaptation to slips had only limited interference during the initial phase of trip recovery. In fact, the prior repeated-slip exposure had primed their reaction, which mitigated any error resulting from early interference. As a result, they did not have to take a longer compensatory step for trip recovery than did the controls. After the mixed training, subjects were able to converge effectively the motion state of their center of mass (in its position and velocity space) to a stable and generalized "middle ground" steady-state. Such movement strategies not only further strengthened their robust reactive control of stability, but also reduced the CNS' overall reliance on accurate context prediction and on feedback correction of perturbation-induced movement error.

Fig. 1

The diagrammatic representation of the experimental setup and video series for slip and trip. (a) A slip was induced by releasing a low-friction moveable platform free to slide 150-cm forward shortly after leading/slipping foot touchdown (i.e., right foot). The platform was mounted on a frame with two rows of linear bearings, and the frame was bolted onto two force plates to measure the ground reaction force. The movable platform was embedded in a 7-m walkway and made less noticeable to the subject by surrounding stationary decoy platforms. (b) A trip was induced by obstructing the subject’s left limb during mid-to-late swing phase using an obstacle device, which was triggered at right foot touchdown (RTD). The obstacle device consisted of an 11-cm tall plate, which was locked in a flat position by a pair of electromagnets during regular walking, and became upright to induce a trip when unlocked by powering off the electromagnets. A set of 28 light-reflective markers were placed on the subjects’ upper and lower extremities, torso, the movable platform, and the obstacle device. All subjects were required to wear a pair of modified glasses that blocked the lower half of the visual field, and a safety harness which was adjusted to prevent a fall to the ground. A load cell connected to the harness was used to measure the forces exerted on the harness. Video series were shown in typical (c) slip and (d) trip events.

Fig. 2

Shown were testing protocols for (a) training and control groups, and (b) the hypotheses and analyses for evaluation of interference and mixed (interference) training effects. The protocol for the training group consisted of eight regular walking trials followed by a block of eight slips [including the first novel slip (S1) and another seven consecutive slips (S2–S8)], a block of three unperturbed trials (N), a block of eight trips [including the first novel trip (T1) and another seven consecutive trips (T2–T8)], another block of three unperturbed trials, a second block of five slips (S9–S13) followed by a block of three unperturbed trials, a second block of five trips (T9–T13) followed by a block of three unperturbed trials, and then a mixed block of seven slips (S14–S20), seven trips (T14–T20), and four unperturbed trials interspersed. NS and NT represented the last regular walking trial prior to the first novel perturbation (S1), and respectively served as the baseline walking performance for comparison with data from slip and trip trials. The protocol for the control group consisted of eight regular walking trials followed by an unannounced, novel trip (TC).

Fig. 3

Demonstrations of the typical recordings of kinematic variables during slip and trip for (a) the hip height, pre-slip/trip step length, and the foot angle; (b) the recovery step length and the follow-up step length during trips with lowering strategy, and the trunk angle; and (c) the recovery step length and the follow-up step length during trips with elevating strategy, and the toe clearance.

Fig. 4

Comparison of group means (±standard deviation [SD]) of the following variables between the first slip (S1) and the eighth slip (S8) for the training group: pre- and post-slip (a) COM position, (b) COM velocity, and (c) stability, pre-slip (d) step length and (e) foot angle, and (f) post-slip hip height. The COM position (X_COM/BOS) was defined as the absolute COM position in anteroposterior direction relative to the rear BOS and normalized by foot length. The COM velocity (V_COM/BOS) was calculated from differentiation of COM position and normalized to $\sqrt{g\times \mathit{\text{bh}}}$. Stability was defined as the shortest distance between the instantaneous COM state (i.e., position and velocity) and predicted FSR limits for backward balance loss under slip conditions. Stability value between 0 and 1 indicated that the COM state was within the FSR. Stability value of less than 0 indicated that the COM state fell outside of the FSR where backward balance loss was predicted. Pre-slip step length was calculated as the horizontal distance measured from the most posterior position of the left heel marker during the stance phase of the left foot to the most posterior position of the right heel marker during the stance phase of the right foot. Foot angle was defined as the angle between foot segment and the horizontal; a smaller angle indicates a more flat-footed landing. Trunk angle was defined as the angle between the trunk segment with the vertical line (+: extension; −: flexion). Hip height was calculated as the vertical distance from the ground to midpoint of bilateral hips and normalized by subjects’ height (/bh). *p < 0.05; **p < 0.01; ***p < 0.001.

Fig. 5

Shown are (a) the outcomes for selected trials of slips (S1, S9, and S20) and trips (T1, T9, and T20) for the training group, and the outcome of the first novel trip (TC) for the control group. A decrease in the percentage of falls (filled) and backward balance loss (BLOB) or compensatory stepping (CS) (hatched lines) was associated with an increase in the percentage of no loss of balance (NLOB) (unfilled) for the training group. All of the subjects in both the training and control groups had to take compensatory step to recover their balance on the first novel trip (T1 & TC). (b) Also shown were percentage changes in the strategy employed for recovery from selected trials of trips (T1, T9, and T20) for the training group and the first novel trip (TC) for the control group. Lowering-hit strategy (filled): the obstructed foot was rapidly lowered to the ground and the contralateral foot took the compensatory step after obstacle-hit. Elevating-hit strategy (unfilled): the obstructed foot took compensatory step after obstacle-hit. Elevating-cross strategy (cross lines): the subjects could cross over the obstacle without hitting. Overall, over 75% of the subjects in both training and control groups used lowering strategy to recover from a trip.

Fig. 6

Shown are (a) group means (±SD) of adaptive changes in post-slip/trip stability (reactive control) and (b) outcomes on selected trials which include the first block of slips (S1 through S8) and trips (T1 through T8) for the training group. Stability during a slip (backward stability) was measured as the shortest distance between the instantaneous COM state and predicted FSR limits for backward loss of balance under slip conditions. Also represented (a) are stability values on selected slip and trip trials from the mixed block (14, 16, 18 and 20) and (b) the percentage outcome on all trials of the mixed block. Stability during a trip (forward instability) was measured as the shortest distance between the instantaneous COM state and predicted FSR limits for forward loss of balance under non-slip conditions. Stability value of greater than 1 indicated less stability against forward balance loss; stability value between 0 and 1 indicated that the COM state was within the FSR. Stability value of less than 0 indicated that the COM state fell outside of the FSR where backward balance loss was predicted. Also shown are unperturbed trials after the slip and trip blocks (N1–N3 and N4–N6 trials) and the last unperturbed trial of the entire protocol (N16). NS represented the data for the regular walking trial prior to the first novel perturbation (i.e., S1). NT represented the data for the regular walking trial prior to S1. Both NS and NT were obtained at left foot touchdown. (b) **p < 0.05; **p < 0.01; **p < 0.001.

Fig. 7

Comparison of group means (±SD) of the following variables between the first novel trip from the training (T1) and control (TC) groups: pre-and post-trip (a) COM position, (b) COM velocity, and (c) forward instability, (d) toe clearance and compensatory step length, pre- and post-trip (e) trunk angle and (f) hip height. The COM position (X_COM/BOS) was defined as the absolute COM position in anteroposterior direction relative to the rear BOS and normalized by foot length. The COM velocity (V_COM/BOS) was calculated from differentiation of COM position and normalized to $\sqrt{g\times \mathit{\text{bh}}}$. Stability was measured as the shortest distance between the instantaneous COM state and predicted FSR limits for forward loss of balance under non-slip conditions. Stability value of greater than 1 indicated less stability against forward balance loss; stability value between 0 and 1 indicated that the COM state was within the FSR. The toe clearance was measured as the vertical distance from the ground to the left toe. Trunk angle was defined as the angle between the trunk segment with the vertical line (+: extension; −: flexion). Hip height was calculated as the vertical distance from the ground to midpoint of bilateral hips and normalized by subjects’ height (/bh). *p < 0.05; **p < 0.01.

Fig. 8

Shown are group means (±SD) of adaptive changes in (a) pre-slip/trip COM position and (b) post-slip/trip COM position on selected trials of slips (S1, S9, S20) and trips (T1, T9, T20) for the training group. The COM position (X_COM/BOS) was defined as the absolute COM position in anteroposterior direction relative to the rear BOS and normalized by foot length. NS represented the data for the regular walking trial prior to the first novel perturbation (i.e., S1), and its pre- and post-slip data were obtained respectively at leading/ slipping foot (i.e., right foot) and left foot touchdown. NT represented the data for the regular walking trial prior to S1, and its pre- and post-trip data were obtained respectively at 30 ms prior to the time when the left toe marker was right above the erect plate and left foot touchdown. *p < 0.05; **p < 0.01; ***p < 0.001.

Fig. 9

Shown are group means (±SD) of adaptive changes in (a) pre-slip/trip COM velocity and (b) post-slip/trip COM velocity on selected trials of slips (S1, S9, S20) and trips (T1, T9, T20) for the training group. The COM velocity (V_COM/BOS) was calculated from differentiation of the COM position and normalized to $\sqrt{g\times \mathit{\text{bh}}}$. NS represented the data for the regular walking trial prior to the first novel perturbation (i.e., S1), and its pre- and post-slip data were obtained respectively at leading/slipping foot (i.e., right foot) and left foot touchdown. NT represented the data for the regular walking trial prior to S1, and its pre- and post-trip data were obtained respectively at 30 ms prior to the time when the left toe marker was right above the erect plate and left foot touchdown. *p < 0.05; **p < 0.01; ***p < 0.001.

Fig. 10

Shown are group means (±SD) of adaptive changes in (a) pre-slip/trip stability and (b) post-slip/trip stability on selected trials of slips (S1, S9, S20) and trips (T1, T9, T20) for the training group. Stability during a slip (backward stability) was measured as the shortest distance between the instantaneous COM state and predicted FSR limits for backward loss of balance under slip conditions. Stability during a trip (forward instability) was measured as the shortest distance between the instantaneous COM state and predicted FSR limits for forward loss of balance under non-slip conditions. Stability value of greater than 1 indicated less stability against forward balance loss; stability value between 0 and 1 indicated that the COM state was within the FSR. Stability value of less than 0 indicated that the COM state fell outside of the FSR where backward balance loss was predicted. NS represented the data for the regular walking trial prior to the first novel perturbation (i.e., S1), and its pre- and post-slip data were obtained respectively at leading/ slipping foot (i.e., right foot) and left foot touchdown. NT represented the data for the regular walking trial prior to S1, and its pre- and post-trip data were obtained respectively at 30 ms prior to the time when the left toe marker was right above the erect plate and left foot touchdown. *p < 0.05; **p < 0.01; ***p < 0.001.

Fig. 11

Shown are group means (±SD) of adaptive changes in (a) pre-slip/trip step length, (b) pre-slip/trip toe clearance, (c) post-slip/trip trunk angle, and (d) post-slip/trip hip height on selected trials of slips (S1, S9, and S20) and trips (T1, T9, and T20) for the training group. Pre-slip/trip step length was calculated as the horizontal distance measured from the most posterior position of the left heel marker during the stance phase of the left foot to the most posterior position of the right heel marker during the stance phase of the right foot prior to a slip/trip. Toe clearance was measured as the vertical distance from the ground to the left toe. Trunk angle was defined as the angle between the trunk segment with the vertical line (+: extension; −: flexion). Hip height was calculated as the vertical distance from the ground to midpoint of bilateral hips and normalized by subjects’ height (/bh). NS represented the data for the regular walking trial prior to the first novel perturbation (i.e., S1), and its pre- and post-slip data were obtained respectively at leading/slipping foot (i.e., right foot) and left foot touchdown. NT represented the data for the regular walking trial prior to S1, and its pre- and post-trip data were obtained respectively at 30 ms prior to the time when the left toe marker was right above the erect plate and left foot touchdown. *p < 0.05; **p < 0.01; ***p < 0.001.