Postural dependence of human locomotion during gait initiation

Abstract

The initiation of human walking involves postural motor actions for body orientation and balance stabilization that must be effectively integrated with locomotion to allow safe and efficient transport. Our ability to coordinately adapt these functions to environmental or bodily changes through error-based motor learning is essential to effective performance. Predictive compensations for postural perturbations through anticipatory postural adjustments (APAs) that stabilize mediolateral (ML) standing balance normally precede and accompany stepping. The temporal sequencing between these events may involve neural processes that suppress stepping until the expected stability conditions are achieved. If so, then an unexpected perturbation that disrupts the ML APAs should delay locomotion. This study investigated how the central nervous system (CNS) adapts posture and locomotion to perturbations of ML standing balance. Healthy human adults initiated locomotion while a resistance force was applied at the pelvis to perturb posture. In experiment 1, using random perturbations, step onset timing was delayed relative to the APA onset indicating that locomotion was withheld until expected stability conditions occurred. Furthermore, stepping parameters were adapted with the APAs indicating that motor prediction of the consequences of the postural changes likely modified the step motor command. In experiment 2, repetitive postural perturbations induced sustained locomotor aftereffects in some parameters (i.e., step height), immediate but rapidly readapted aftereffects in others, or had no aftereffects. These results indicated both rapid but transient reactive adaptations in the posture and gait assembly and more durable practice-dependent changes suggesting feedforward adaptation of locomotion in response to the prevailing postural conditions.

Keywords: balance; coordination; locomotion; motor adaptation; posture.

Fig. 1.

Models for the posture and locomotion coupling. Two hypotheses for the sequencing of posture and locomotion during the initiation of walking tested by perturbing the postural weight transfer before stepping. OFF represents the normal unperturbed time course of the postural (green) and locomotor (blue) events occurring at the initiation of walking, and ON indicates the predicted time course of the same events when a passive frictional resistance is applied to the pelvis in the frontal plane to delay the time of occurrence of the mediolateral (ML) center of pressure (CoP) peak (red arrows). According to a 1st hypothesis (left), the postural and locomotor events could be sequenced by sending 2 independent motor commands to engage both systems with a fixed inherent delay (lag) in the release of locomotion to allow the ML weight transfer to occur before the onset of stepping. In this independent model of coordination, an unexpected perturbation of the postural system would not be taken into account by the locomotion system, such that the step command (gray bars) and step onset (gray arrows) would not be modified. Alternatively (right), these events could be sequenced in an interactive way such that locomotion onset might be triggered when anticipated postural state conditions have been reached. In this case, the same unexpected postural perturbation should delay the step command and onset since expected postural prerequisites would not be achieved. Bottom: schematic illustration of the postural ML CoP displacement (green) and the step ankle vertical displacement (blue). The usual normal profile observed during unperturbed step initiation is indicated by the dashed lines, and the solid lines represent the expected changes of these events according to both hypotheses.

Fig. 2.

Averaged time profiles during random postural perturbations. Averaged data from 1 representative subject during step initiation without (average of 10 baseline trials in blue) and with (average of 15 ON trials in red) a postural perturbation. All records were synchronized with the onset of the net CoP displacement (vertical dotted line) at time zero. The shaded regions represent ±1 SD. The lateral displacement of the body center of mass (CoM) shows a smaller displacement for the perturbation ON condition. The lateral displacement of the CoP under the stepping side is increased in amplitude and duration to overcome the resistance applied to the pelvis. The vertical displacement of the stepping ankle marker shows a delay in the 1st step timing and increased step height. The mean EMG activity of stepping leg muscles shows a delay of the step command [illustrated by the rectus femoris (RF) and the tensor fasciae latae (TFL) activity], a modification of the step motor command with the appearance of a phasic activation bursts in soleus (SOL) and gastrocnemius medialis (GAST) when a postural perturbation is randomly applied, whereas no modification in the onset of the tiabialis anterior (TA) activity was observed. The anteroposterior (AP) displacement of the CoM and the CoP were unmodified for the perturbation ON condition.

Fig. 3.

Effects of a random postural perturbation. Group averages (±1 SD) of the duration (A) and the amplitude (B) of the ML anticipatory postural adjustments (APAs) and the onset (C) of the TFL (light grey), RF: (dark grey), and the 1st step (white) relative to the onset of the APA. *Significant differences at P < 0.05 between the ON condition and the 2 other conditions, which were not different.

Fig. 4.

First step characteristics changes following the random postural perturbations. Group averages (±1 SD) of the step duration (A), step clearance (B), and length and width (C). The step was shorter in time, higher and placed more laterally, but did not change in length. *Significant differences at P < 0.05 between the ON condition (red) and the two other condition (BASE: blue; OFF: grey), which were not different.

Fig. 5.

Effects of a systematic postural perturbation on the timing of the events. Group averages (±1 SD) of the timing of postural and locomotor's events relative to the onset of the anticipatory postural adjustments are presented for experiment 2. *Significant difference at P < 0.05 between PRE adaptation trials and the 1st block of adaptation (A1). §Significant difference at P < 0.05 between PRE adaptation and the 1st POST adaptation trial (T1).

Fig. 6.

Effects of a systematic postural perturbation. Group averages (±1 SD) for ML displacement of the CoM (A), step width (B), and step clearance (C) are presented for experiment 2. *Significant difference at P < 0.05 between PRE adaptation trials and the 1st block of adaptation (A1). #Significant difference at P < 0.05 between PRE and POST adaptation trials. §Significant difference at P < 0.05 between PRE adaptation and the 1st POST adaptation trial (T1).