The adaptation of muscle activity during split-belt walking reveals age-dependent decline of motor learning

Abstract

Recent studies suggest that planned and corrective actions are recalibrated during some forms of motor adaptation. However, corrective (a.k.a., reactive) movements in human locomotion are thought to simply reflect sudden environmental changes independently from sensorimotor recalibration. Thus, we asked if corrective responses can indicate the motor systems adapted state following prolonged exposure to a novel walking situation inducing sensorimotor adaptation. We recorded electromyographic signals bilaterally on 15 leg muscles before, during, and after split-belts walking (i.e., novel walking situation), in which the legs move at different speeds. We exploited the rapid temporal dynamics of corrective responses upon introduction or removal of an unexpected speed transition to isolate them from the overall motor output. We found that corrective muscle activity was structurally different following short vs. long exposures to split-belts walking. Only after a long exposure, removal of the novel environment elicited corrective muscle patterns that matched those expected in response to a perturbation opposite to the one originally experienced. This indicated that individuals who recalibrated their motor system adopted split-belts environment as their new "normal" and transitioning back to the original walking environment causes subjects to react as if it was novel to them. Interestingly, this learning declined with age, but steady state modulation of muscle activity during split-belts walking did not, suggesting potentially different neural mechanisms underlying these motor patterns. Taken together, our results show that corrective motor commands reflect the adapted state of the motor system, which is less flexible as we age. Significance statementWe showed that corrective muscle activity elicited by sudden environmental transitions is revealing of the underlying recalibration process during sensorimotor adaptation. This allowed us to identify age-related decline in motor learning that was not discernible from kinematic measures conventionally used in motor adaptation studies. These findings suggest that older populations may have limited potential to correct their movements through error-based protocols simply given their age. Moreover, we describe the distinct motor patterns recruited during and after the split condition, informing our understanding of the therapeutic effect of this task. Therefore, our detailed EMG characterization provides valuable normative data of muscle activity that could be reinforced with repeated exposure of split-belts walking.