Split-belt walking adaptation recalibrates sensorimotor estimates of leg speed but not position or force

Abstract

Motor learning during reaching not only recalibrates movement but can also lead to small but consistent changes in the sense of arm position. Studies have suggested that this sensory effect may be the result of recalibration of a forward model that associates motor commands with their sensory consequences. Here we investigated whether similar perceptual changes occur in the lower limbs after learning a new walking pattern on a split-belt treadmill--a task that critically involves proprioception. Specifically, we studied how this motor learning task affects perception of leg speed during walking, perception of leg position during standing or walking, and perception of contact force during stepping. Our results show that split-belt adaptation leads to robust motor aftereffects and alters the perception of leg speed during walking. This is specific to the direction of walking that was trained during adaptation (i.e., backward or forward). The change in leg speed perception accounts for roughly half of the observed motor aftereffect. In contrast, split-belt adaptation does not alter the perception of leg position during standing or walking and does not change the perception of stepping force. Our results demonstrate that there is a recalibration of a sensory percept specific to the domain of the perturbation that was applied during walking (i.e., speed but not position or force). Furthermore, the motor and sensory consequences of locomotor adaptation may be linked, suggesting overlapping mechanisms driving changes in the motor and sensory domains.

Two biomechanical strategies for locomotor adaptation to split-belt treadmill walking in subjects with and without transtibial amputation

“…Changes in step length symmetry were consistent with previous studies (Reisman et al 2005; Malone, Bastian, 2010; Vazquez et al, 2015). Both controls and amputees initially responded to split-belt walking by taking longer steps with the slow leg leading, but returned to baseline step length symmetry by late adaptation.…”

Split-Belt walking induces changes in active, but not passive, perception of step length

“…Our results show that the perception of limb position is altered following motor adaptation in locomotion, which supports prior findings that the perception of limb position is susceptible to motor adaptation (e.g., 5,6,15,7–14 ). However, we only observed perceptual after-effects when subjects actively generated motor commands and not when their legs were passively moved, which is consistent with prior work indicating that afferent signals encoding position remain intact following split-belt walking 16 . These findings contrast multiple reports of shifts in the estimation of hand position following motor adaptation when the arms are moved by the experimenter (e.g., 5–12 ).…”

“…We believe that this discrepancy between reaching and locomotion suggests that sensory changes post-adaptation arise from mismatched position estimates from different sensory sources (i.e., proprioception and vision), which is less prominent in walking. We also found that active perceptual effects were not observed in the leading leg’s position, as previously reported 16 , but they were clearly observed in the trailing leg’s position, which had not been assessed before. We posit two potential explanations for the altered estimation of the trailing leg’s position.…”

“…Interestingly, the effects of motor adaptation on the estimation of limb position in walking remains elusive. Namely, a recent study probing the perception of one leg position with respect to the body did not find passive or active perceptual after-effects despite robust motor after-effects 16 . This might be due to how perceptual after-effects were tested given evidence that passive and active perceptual changes post-adaptation are sensitive to the condition in which they are evaluated 17–19 .…”

Seeing the Errors You Feel Enhances Locomotor Performance but Not Learning

“…Unlike adaptation, energy optimization has not been shown to be cerebellum-dependent [25] or driven by prediction error, but instead results in a remapping between a movement pattern and its expected energetic consequences. It is unclear whether this remapping changes perception (as has been observed in split-belt walking [26,27]) or generalizes to other contexts.…”