Learning from the Physical Consequences of Our Actions Improves Motor Memory.

Actions have consequences. Motor learning involves correcting actions that lead to movement errors and remembering these actions for future behavior. In most laboratory situations, movement errors have no physical consequences and simply indicate the progress of learning. Here, we asked how experiencing a physical consequence when making a movement error affects motor learning. Two groups of participants adapted to a new, prism-induced mapping between visual input and motor output while performing a precision walking task. Importantly, one group experienced an unexpected slip perturbation when making foot-placement errors during adaptation. Because of our innate drive for safety, and the fact that balance is fundamental to movement, we hypothesized that this experience would enhance motor memory. Learning generalized to different walking tasks to a greater extent in the group who experienced the adverse physical consequence. This group also showed faster relearning one week later despite exposure to a competing mapping during initial learning, evidence of greater memory consolidation. The group differences in generalization and consolidation occurred although they both experienced similar magnitude foot-placement errors and adapted at similar rates. Our results suggest the brain considers the potential physical consequences of movement error when learning and that balance-threatening consequences serve to enhance this process.

Savings in sensorimotor learning during balance-challenged walking but not reaching.

Safe and successful motor performance relies on the ability to adapt to physiological and environmental change and retain what is learned. An open question is what factors maximize this retention? One overlooked factor is the degree to which balance is challenged during learning. We propose that the greater need for control and/or perceived threat of falling or injury associated with balance-challenging tasks increases the value assigned to maintaining a learned visuomotor mapping (i.e., the new relationship between visual input and motor output). And we propose that a greater-valued mapping is a more retainable mapping, as it serves to benefit future motor performance. Thus, we tested the hypothesis that challenging balance enhances motor memory, reflected by greater recall and faster relearning (i.e., savings). Four groups of participants adapted to a novel visuomotor mapping induced by prism lenses while performing a reaching or walking task, with and without an additional balance challenge. We found that challenging balance did not disrupt visuomotor adaptation during reaching or walking. We then probed recall and savings by having participants repeat the adaptation protocol 1 wk later. For reaching, we found evidence of initial recall, though neither group demonstrated savings upon reexposure to the prisms. In contrast, both walking groups demonstrated significant initial recall and savings. In addition, we found that challenging balance significantly enhanced savings during walking. Taken together, our results demonstrate the robustness of motor memories formed during walking and highlight the potential influence of balance control on sensorimotor learning.NEW & NOTEWORTHY Most everyday tasks challenge our balance. Yet, this aspect of daily motor behavior is often overlooked in adaptation paradigms. Here, we show that challenging balance does not impair sensorimotor adaptation during precision reaching and walking tasks. Furthermore, we show that challenging balance enhances savings of a learned visuomotor mapping during walking. These results provide evidence for the potential performance benefits associated with learning during unconstrained, naturalistic behaviors.

How aging affects visuomotor adaptation and retention in a precision walking paradigm.

Motor learning is a lifelong process. However, age-related changes to musculoskeletal and sensory systems alter the relationship (or mapping) between sensory input and motor output, and thus potentially affect motor learning. Here we asked whether age affects the ability to adapt to and retain a novel visuomotor mapping learned during overground walking. We divided participants into one of three groups (n = 12 each) based on chronological age: a younger-aged group (20-39 years old); a middle-aged group (40-59 years old); and an older-aged group (60-80 years old). Participants learned a new visuomotor mapping, induced by prism lenses, during a precision walking task. We assessed retention one-week later. We did not detect significant effects of age on measures of adaptation or savings (defined as faster relearning). However, we found that older adults demonstrated reduced initial recall of the mapping, reflected by greater foot-placement error during the first adaptation trial one-week later. Additionally, we found that increased age significantly associated with reduced initial recall. Overall, our results suggest that aging does not impair adaptation and that older adults can demonstrate visuomotor savings. However, older adults require some initial context during relearning to recall the appropriate mapping.

Subthreshold stochastic vestibular stimulation affects balance-challenged standing and walking.

Subthreshold stochastic vestibular stimulation (SVS) is thought to enhance vestibular sensitivity and improve balance. However, it is unclear how SVS affects standing and walking when balance is challenged, particularly when the eyes are open. It is also unclear how different methods to determine stimulation intensity influence the effects. We aimed to determine (1) whether SVS affects stability when balance is challenged during eyes-open standing and overground walking tasks, and (2) how the effects differ based on whether optimal stimulation amplitude is derived from sinusoidal or cutaneous threshold techniques. Thirteen healthy adults performed balance-unchallenged and balance-challenged standing and walking tasks with SVS (0-30 Hz zero-mean, white noise electrical stimulus) or sham stimulation. For the balance-challenged condition, participants had inflatable rubber hemispheres attached to the bottom of their shoes to reduce the control provided by moving the center of pressure under their base of support. In different blocks of trials, we set SVS intensity to either 50% of participants' sinusoidal (motion) threshold or 80% of participants' cutaneous threshold. SVS reduced medial-lateral trunk velocity root mean square in the balance-challenged (p < 0.05) but not in the balance-unchallenged condition during standing. Regardless of condition, SVS decreased step-width variability and marginally increased gait speed when walking with the eyes open (p < 0.05). SVS intensity had minimal effect on the standing and walking measures. Taken together, our results provide insight into the effectiveness of SVS at improving balance-challenged, eyes-open standing and walking performance in healthy adults.

Challenging balance during sensorimotor adaptation increases generalization.

From reaching to walking, real-life experience suggests that people can generalize between motor behaviors. One possible explanation for this generalization is that real-life behaviors often challenge our balance. We propose that the exacerbated body motions associated with balance-challenged whole body movements increase the value to the nervous system of using a comprehensive internal model to control the task. Because it is less customized to a specific task, a more comprehensive model is also a more generalizable model. Here we tested the hypothesis that challenging balance during adaptation would increase generalization of a newly learned internal model. We encouraged participants to learn a new internal model using prism lenses that created a new visuomotor mapping. Four groups of participants adapted to prisms while performing either a standing-based reaching or precision walking task, with or without a manipulation that challenged balance. To assess generalization after the adaptation phase, participants performed a single trial of each of the other groups' tasks without prisms. We found that both the reaching and walking balance-challenged groups showed significantly greater generalization to the equivalent, nonadapted task than the balance-unchallenged groups. Additionally, we found some evidence that all groups generalized across tasks, for example, from walking to reaching and vice versa, regardless of balance manipulation. Overall, our results demonstrate that challenging balance increases the degree to which a newly learned internal model generalizes to untrained movements.NEW & NOTEWORTHY Real-life experience indicates that people can generalize between motor behaviors. Here we show that challenging balance during the learning of a new internal model increases the degree of generalization to untrained movements for both reaching and walking tasks. These results suggest that the effects of challenging balance are not specific to the task but instead apply to motor learning more broadly.