Automatic learning mechanisms for flexible human locomotion.

Movement flexibility and automaticity are necessary to successfully navigate different environments. When encountering difficult terrains such as a muddy trail, we can change how we step almost immediately so that we can continue walking. This flexibility comes at a cost since we initially must pay deliberate attention to how we are moving. Gradually, after a few minutes on the trail, stepping becomes automatic so that we do not need to think about our movements. Canonical theory indicates that different adaptive motor learning mechanisms confer these essential properties to movement: explicit control confers flexibility, while forward model recalibration confers automaticity. Here we uncover a distinct mechanism of treadmill walking adaptation - an automatic stimulus-response mapping - that confers both properties to movement. The mechanism is flexible as it learns stepping patterns that can be rapidly changed to suit a range of treadmill configurations. It is also automatic as it can operate without deliberate control or explicit awareness by the participants. Our findings reveal a tandem architecture of forward model recalibration and automatic stimulus-response mapping mechanisms for walking, reconciling different findings of motor adaptation and perceptual realignment.

Gait speed and individual characteristics are related to specific gait metrics in neurotypical adults.

Gait biofeedback is a well-studied strategy to reduce gait impairments such as propulsion deficits or asymmetric step lengths. With biofeedback, participants alter their walking to reach the desired magnitude of a specific parameter (the biofeedback target) with each step. Biofeedback of anterior ground reaction force and step length is commonly used in post-stroke gait training as these variables are associated with self-selected gait speed, fall risk, and the energy cost of walking. However, biofeedback targets are often set as a function of an individual's baseline walking pattern, which may not reflect the ideal magnitude of that gait parameter. Here we developed prediction models based on speed, leg length, mass, sex, and age to predict anterior ground reaction force and step length of neurotypical adults as a possible method for personalized biofeedback. Prediction of these values on an independent dataset demonstrated strong agreement with actual values, indicating that neurotypical anterior ground reaction forces can be estimated from an individual's leg length, mass, and gait speed, and step lengths can be estimated from individual's leg length, mass, age, sex, and gait speed. Unlike approaches that rely on an individual's baseline gait, this approach provides a standardized method to personalize gait biofeedback targets based on the walking patterns exhibited by neurotypical individuals with similar characteristics walking at similar speeds without the risk of over- or underestimating the ideal values that could limit feedback-mediated reductions in gait impairments.

Speed-dependent biomechanical changes vary across individual gait metrics post-stroke relative to neurotypical adults.

BACKGROUND: Gait training at fast speeds is recommended to reduce walking activity limitations post-stroke. Fast walking may also reduce gait kinematic impairments post-stroke. However, it is unknown if differences in gait kinematics between people post-stroke and neurotypical adults decrease when walking at faster speeds. OBJECTIVE: To determine the effect of faster walking speeds on gait kinematics post-stroke relative to neurotypical adults walking at similar speeds. METHODS: We performed a secondary analysis with data from 28 people post-stroke and 50 neurotypical adults treadmill walking at multiple speeds. We evaluated the effects of speed and group on individual spatiotemporal and kinematic metrics and performed k-means clustering with all metrics at self-selected and fast speeds. RESULTS: People post-stroke decreased step length asymmetry and trailing limb angle impairment, reducing between-group differences at fast speeds. Speed-dependent changes in peak swing knee flexion, hip hiking, and temporal asymmetries exaggerated between-group differences. Our clustering analyses revealed two clusters. One represented neurotypical gait behavior, composed of neurotypical and post-stroke participants. The other characterized stroke gait behavior-comprised entirely of participants post-stroke with smaller lower extremity Fugl-Meyer scores than the post-stroke participants in the neurotypical gait behavior cluster. Cluster composition was largely consistent at both speeds, and the distance between clusters increased at fast speeds. CONCLUSIONS: The biomechanical effect of fast walking post-stroke varied across individual gait metrics. For participants within the stroke gait behavior cluster, walking faster led to an overall gait pattern more different than neurotypical adults compared to the self-selected speed. This suggests that to potentiate the biomechanical benefits of walking at faster speeds and improve the overall gait pattern post-stroke, gait metrics with smaller speed-dependent changes may need to be specifically targeted within the context of fast walking.

Updates in Motor Learning: Implications for Physical Therapist Practice and Education.

Over the past 3 decades, the volume of human motor learning research has grown enormously. As such, the understanding of motor learning (ie, sustained change in motor behavior) has evolved. It has been learned that there are multiple mechanisms through which motor learning occurs, each with distinctive features. These mechanisms include use-dependent, instructive, reinforcement, and sensorimotor adaptation-based motor learning. It is now understood that these different motor learning mechanisms contribute in parallel or in isolation to drive desired changes in movement, and each mechanism is thought to be governed by distinct neural substrates. This expanded understanding of motor learning mechanisms has important implications for physical therapy. It has the potential to facilitate the development of new, more precise treatment approaches that physical therapists can leverage to improve human movement. This Perspective describes scientific advancements related to human motor learning mechanisms and discusses the practical implications of this work for physical therapist practice and education.

Younger and Late Middle-Aged Adults Exhibit Different Patterns of Cognitive-Motor Interference During Locomotor Adaptation, With No Disruption of Savings.

It has been proposed that motor adaptation and subsequent savings (or faster relearning) of an adapted movement pattern are mediated by cognitive processes. Here, we evaluated the pattern of cognitive-motor interference that emerges when young and late middle-aged adults perform an executive working memory task during locomotor adaptation. We also asked if this interferes with savings of a newly learned walking pattern, as has been suggested by a study of reaching adaptation. We studied split-belt treadmill adaptation and savings in young (21 ± 2 y/o) and late middle-aged (56 ± 6 y/o) adults with or without a secondary 2-back task during adaptation. We found that young adults showed similar performance on the 2-back task during baseline and adaptation, suggesting no effect of the dual-task on cognitive performance; however, dual-tasking interfered with adaptation over the first few steps. Conversely, dual-tasking caused a decrement in cognitive performance in late middle-aged adults with no effect on adaptation. To determine if this effect was specific to adaptation, we also evaluated dual-task interference in late middle-aged adults that dual-tasked while walking in a complex environment that did not induce motor adaptation. This group exhibited less cognitive-motor interference than late middle-aged adults who dual-tasked during adaptation. Savings was unaffected by dual-tasking in both young and late middle-aged adults, which may indicate different underlying mechanisms for savings of reaching and walking. Collectively, our findings reveal an age-dependent effect of cognitive-motor interference during dual-task locomotor adaptation and no effect of dual-tasking on savings, regardless of age. Young adults maintain cognitive performance and show a mild decrement in locomotor adaptation, while late middle-aged adults adapt locomotion at the expense of cognitive performance.

Feasibility and utility of transcutaneous spinal cord stimulation combined with walking-based therapy for people with motor incomplete spinal cord injury.

STUDY DESIGN: Prospective case series. OBJECTIVES: To evaluate the feasibility and preliminary efficacy of combining transcutaneous spinal cord stimulation (TSCS) with walking-based physical therapy. SETTING: Hospital-based outpatient center in Maryland, United States. METHODS: Ten individuals with chronic (>1 year) motor incomplete spinal cord injury (iSCI) completed 23 sessions of 2-h therapy over 8 weeks. TSCS was delivered for the first 30 min of each session using a clinically available device with adjustable current. To assess feasibility of the intervention, we tracked pain, adverse events, and participant retention. Preliminary efficacy was assessed by evaluating changes in walking speed, endurance, and quality following the intervention with select functional outcome measures (10-m walk test (10MWT), 6-min walk test (6MWT), timed up and go, and walking index for spinal cord injury II). RESULTS: We found that the combined intervention was feasible in an outpatient clinical setting. Participants tolerated the TSCS well, with no reports of significant adverse events or other issues (e.g., skin irritation or pain that disrupted training). None of the participants elected to discontinue the study. Participants also showed significant improvements in each measure of walking function following the intervention. Changes in walking speed, as measured by the 10MWT (0.56 ± 0.29 m/s to 0.72 ± 0.36 m/s), exceeded the minimal clinically important difference for individuals with iSCI. Changes in walking quality and endurance, as measured by the 6MWT (149.88 ± 99.87 m to 194.53 ± 106.56 m), exceeded the minimal detectable change for individuals with iSCI. CONCLUSIONS: These results indicate that TSCS is clinically feasible and may be useful as an adjunct to walking-based therapy for adults with iSCI.

Unilateral step training can drive faster learning of novel gait patterns.

Humans are capable of learning many new walking patterns. People have learned to snowshoe up mountains, racewalk marathons, and march in precise synchrony. But what is required to learn a new walking pattern? Here, we demonstrate that people can learn new walking patterns without actually walking. Through a series of experiments, we observe that stepping with only one leg can facilitate learning of an entirely new walking pattern (i.e., split-belt treadmill walking). We find that the nervous system learns from the relative speed difference between the legs-whether or not both legs are moving-and can transfer this learning to novel gaits. We also show that locomotor learning requires active movement: observing another person adapt their gait did not result in significantly faster learning. These findings reveal that people can learn new walking patterns without bilateral gait training, as stepping with one leg can facilitate adaptive learning that transfers to novel gait patterns.

Persons post-stroke improve step length symmetry by walking asymmetrically.

BACKGROUND AND PURPOSE: Restoration of step length symmetry is a common rehabilitation goal after stroke. Persons post-stroke often retain the ability to walk with symmetric step lengths ("symmetric steps"); however, the resulting walking pattern remains effortful. Two key questions with direct implications for rehabilitation have emerged: 1) how do persons post-stroke generate symmetric steps, and 2) why do symmetric steps remain so effortful? Here, we aimed to understand how persons post-stroke generate symmetric steps and explored how the resulting gait pattern may relate to the metabolic cost of transport. METHODS: We recorded kinematic, kinetic, and metabolic data as nine persons post-stroke walked on an instrumented treadmill under two conditions: preferred walking and symmetric stepping (using visual feedback). RESULTS: Gait kinematics and kinetics remained markedly asymmetric even when persons post-stroke improved step length symmetry. Impaired paretic propulsion and aberrant movement of the center of mass were evident during both preferred walking and symmetric stepping. These deficits contributed to diminished positive work performed by the paretic limb on the center of mass in both conditions. Within each condition, decreased positive paretic work correlated with increased metabolic cost of transport and decreased walking speed across participants. CONCLUSIONS: It is critical to consider the mechanics used to restore symmetric steps when designing interventions to improve walking after stroke. Future research should consider the many dimensions of asymmetry in post-stroke gait, and additional within-participant manipulations of gait parameters are needed to improve our understanding of the elevated metabolic cost of walking after stroke.

The capacity to learn new motor and perceptual calibrations develops concurrently in childhood.

Learning new movements through an error-based process called motor adaptation is thought to involve multiple mechanisms which are still largely not understood. Previous studies have shown that young children adapt movement more slowly than adults, perhaps supporting the involvement of distinct neural circuits that come online at different stages of development. Recent studies in adults have shown that in addition to recalibrating a movement, motor adaptation also leads to changes in the perception of that movement. However, we do not yet understand the relationship between the processes that underlie motor and perceptual recalibration. Here we studied motor and perceptual recalibration with split-belt walking adaptation in adults and children aged 6-8 years. Consistent with previous work, we found that this group of children adapted their walking patterns more slowly than adults, though individual children ranged from slow to adult-like in their adaptation rates. Perceptual recalibration was also reduced in the same group of children compared to adults, with individual children ranging from having no recalibration to having adult-like recalibration. In sum, faster motor adaptation and the ability to recalibrate movement perception both come online within a similar age-range, raising the possibility that the same sensorimotor mechanisms underlie these processes.

Trading Symmetry for Energy Cost During Walking in Healthy Adults and Persons Poststroke.

Background. Humans typically walk in ways that minimize energy cost. Recent work has found that healthy adults will even adopt new ways of walking when a new pattern costs less energy. This suggests potential for rehabilitation to drive changes in walking by altering the energy costs of walking patterns so that the desired pattern becomes energetically optimal (ie, costs least energy of all available patterns). Objective. We aimed to change gait symmetry in healthy adults and persons poststroke by creating environments where changing symmetry allowed the participants to save energy. Methods. Across 3 experiments, we tested healthy adults (n = 12 in experiment 1, n = 20 in experiment 2) and persons poststroke (n = 7 in experiment 3) in a novel treadmill environment that linked asymmetric stepping and gait speed-2 factors that influence energy cost-to create situations where walking with one's preferred gait symmetry (or asymmetry, in the case of the persons poststroke) was no longer the least energetically costly way to walk. Results. Across the 3 experiments, we found that most participants changed their gait when experiencing the new energy landscape. Healthy adults often adopted an asymmetric gait if it saved energy, and persons poststroke often began to step more symmetrically than they prefer to walk in daily life. Conclusions. We used a novel treadmill environment to show that people with and without stroke change clinically relevant features of walking to save energy. These findings suggest that rehabilitation approaches aimed at making symmetric walking energetically "easier" may promote gait symmetry after stroke.

Movement and perception recalibrate differently across multiple days of locomotor learning.

Learning a new movement through error-based adaptation leads to recalibration of movement and altered perception of that movement. Although presumed to be closely related, the relationship between adaptation-based motor and perceptual changes is not well understood. Here we investigated the changes in motor behavior and leg speed perception over 5 days of split-belt treadmill adaptation. We specifically wanted to know if changes in the perceptual domain would demonstrate savings-like behavior (i.e., less recalibration with more practice) and if these changes would parallel the savings observed in the motor domain. We found that the recalibration of leg speed perception decreased across days of training, indicating savings-like behavior in this domain. However, we observed that the magnitude of savings across days was different between motor and perceptual domains. These findings suggest a degree of independence between the motor and perceptual processes that occur with locomotor adaptation. NEW & NOTEWORTHY Error-based adaptation learning drives changes in movement and perception of movement. Are these changes across domains linked or simply coincidental? Here, we studied changes in movement and perception across 5 days of repeated locomotor adaptation. Savings-like behavior in the motor and perceptual domains developed with different magnitudes and over different timescales, leading us to conclude that motor and perceptual processes operate at least somewhat independently during locomotor adaptation.

Independent voluntary correction and savings in locomotor learning.

Humans can acquire new walking patterns in many different ways. For example, we can change our gait voluntarily in response to instruction or adapt by sensing our movement errors. Here, we investigated how acquisition of a new walking pattern through simultaneous voluntary correction and adaptive learning affected the resulting motor memory of the learned pattern. We studied adaptation to split-belt treadmill walking with and without visual feedback of stepping patterns. As expected, visual feedback enabled faster acquisition of the new walking pattern. However, upon later re-exposure to the same split-belt perturbation, participants exhibited similar motor memories whether they had learned with or without visual feedback. Participants who received feedback did not re-engage the mechanism used to accelerate initial acquisition of the new walking pattern to similarly accelerate subsequent relearning. These findings reveal that voluntary correction neither benefits nor interferes with the ability to save a new walking pattern over time.

Accelerating locomotor savings in learning: compressing four training days to one.

Acquiring new movements requires the capacity of the nervous system to remember previously experienced motor patterns. The phenomenon of faster relearning after initial learning is termed "savings." Here we studied how savings of a novel walking pattern develops over several days of practice and how this process can be accelerated. We introduced participants to a split-belt treadmill adaptation paradigm for 30 min for 5 consecutive days. By training day 5, participants were able to produce near-perfect performance when switching between split and tied-belt environments. We found that this was due to their ability to shift specific elements of their stepping pattern to account for the split treadmill speeds from day to day. We also applied a state-space model to further characterize multiday locomotor savings. We then explored methods of achieving comparable savings with less total training time. We studied people training only on day 1, with either one extended split-belt exposure or alternating four times between split-belt and tied-belt conditions rapidly in succession. Both of these single-day training groups were tested again on day 5. Experiencing four abbreviated exposures on day 1 improved the performance on day 5 compared with one extended exposure on day 1. Moreover, this abbreviated group performed similarly to the group that trained for 4 consecutive days before testing on day 5, despite only having one-quarter of the total training time. These results demonstrate that we can leverage training structure to achieve a high degree of performance while minimizing training sessions. NEW & NOTEWORTHY Learning a new movement requires repetition. Here, we demonstrate how to more efficiently train an adapted walking pattern. By compressing split-belt treadmill training delivered over 4 days to four abbreviated bouts of training delivered on the first day of training, we were able to induce equivalent savings over a 5-day span. These results suggest that we can manipulate the delivery of training to most efficiently drive multiday learning of a novel walking pattern.

Creating flexible motor memories in human walking.

The human nervous system has the ability to save newly learned movements (i.e. re-learn faster after initial learning) and generalize learning to new conditions. In the context of walking, we rely on savings and generalization of newly learned walking patterns to navigate changing environments and make progressive improvements with gait rehabilitation. Here, we used a split-belt treadmill to study how different perturbation parameters can influence savings and generalization of learning during walking. In Experiment 1, we investigated the effect of split perturbation size on savings of a newly learned walking pattern. We found that larger perturbations led to better savings than smaller perturbations. In Experiment 2, we studied how different features of the initial split perturbation influenced the generalization of learning. Interestingly, we found that practicing the same thing twice did not lead to fastest learning. Instead, initial exposure to larger perturbation ratios led to faster subsequent learning of smaller perturbation ratios as compared to repeated exposures to small perturbations. Collectively, our findings reveal that initial learning conditions can be leveraged to increase savings and shape flexible motor memories during walking.

Strategies to augment volitional and reflex function may improve locomotor capacity following incomplete spinal cord injury.

Many studies highlight the remarkable plasticity demonstrated by spinal circuits following an incomplete spinal cord injury (SCI). Such plasticity can contribute to improvements in volitional motor recovery, such as walking function, although similar mechanisms underlying this recovery may also contribute to the manifestation of exaggerated responses to afferent input, or spastic behaviors. Rehabilitation interventions directed toward augmenting spinal excitability have shown some initial success in improving locomotor function. However, the potential effects of these strategies on involuntary motor behaviors may be of concern. In this article, we provide a brief review of the mechanisms underlying recovery of volitional function and exaggerated reflexes, and the potential overlap between these changes. We then highlight findings from studies that explore changes in spinal excitability during volitional movement in controlled conditions, as well as altered kinematic and behavioral performance during functional tasks. The initial focus will be directed toward recovery of reflex and volitional behaviors following incomplete SCI, followed by recent work elucidating neurophysiological mechanisms underlying patterns of static and dynamic muscle activation following chronic incomplete SCI during primarily single-joint movements. We will then transition to studies of locomotor function and the role of altered spinal integration following incomplete SCI, including enhanced excitability of specific spinal circuits with physical and pharmacological interventions that can modulate locomotor output. The effects of previous and newly developed strategies will need to focus on changes in both volitional function and involuntary spastic reflexes for the successful translation of effective therapies to the clinical setting.

High-Intensity Locomotor Exercise Increases Brain-Derived Neurotrophic Factor in Individuals with Incomplete Spinal Cord Injury.

High-intensity locomotor exercise is suggested to contribute to improved recovery of locomotor function after neurological injury. This may be secondary to exercise-intensity-dependent increases in neurotrophin expression demonstrated previously in control subjects. However, rigorous examination of intensity-dependent changes in neurotrophin levels is lacking in individuals with motor incomplete spinal cord injury (SCI). Therefore, the primary aim of this study was to evaluate the effect of locomotor exercise intensity on peripheral levels of brain-derived neurotrophic factor (BDNF) in individuals with incomplete SCI. We also explored the impact of the Val66Met single-nucleotide polymorphism (SNP) on the BDNF gene on intensity-dependent changes. Serum concentrations of BDNF and insulin-like growth factor-1 (IGF-1), as well as measures of cardiorespiratory dynamics, were evaluated across different levels of exercise intensity achieved during a graded-intensity, locomotor exercise paradigm in 11 individuals with incomplete SCI. Our results demonstrate a significant increase in serum BDNF at high, as compared to moderate, exercise intensities (p = 0.01) and 15 and 30 min post-exercise (p < 0.01 for both), with comparison to changes at low intensity approaching significance (p = 0.05). Serum IGF-1 demonstrated no intensity-dependent changes. Significant correlations were observed between changes in BDNF and specific indicators of exercise intensity (e.g., rating of perceived exertion; R = 0.43; p = 0.02). Additionally, the data suggest that Val66Met SNP carriers may not exhibit intensity-dependent changes in serum BDNF concentration. Given the known role of BDNF in experience-dependent neuroplasticity, these preliminary results suggest that exercise intensity modulates serum BDNF concentrations and may be an important parameter of physical rehabilitation interventions after neurological injury.

Effects of Locomotor Exercise Intensity on Gait Performance in Individuals With Incomplete Spinal Cord Injury.

BACKGROUND: High-intensity stepping practice may be a critical component to improve gait following motor incomplete spinal cord injury (iSCI). However, such practice is discouraged by traditional theories of rehabilitation that suggest high-intensity locomotor exercise degrades gait performance. Accordingly, such training is thought to reinforce abnormal movement patterns, although evidence to support this notion is limited. OBJECTIVE: The purposes of this study were: (1) to evaluate the effects of short-term manipulations in locomotor intensity on gait performance in people with iSCI and (2) to evaluate potential detrimental effects of high-intensity locomotor training on walking performance. DESIGN: A single-day, repeated-measures, pretraining-posttraining study design was used. METHODS: Nineteen individuals with chronic iSCI performed a graded-intensity locomotor exercise task with simultaneous collection of lower extremity kinematic and electromyographic data. Measures of interest were compared across intensity levels of 33%, 67%, and 100% of peak gait speed. A subset of 9 individuals participated in 12 weeks of high-intensity locomotor training. Similar measurements were collected and compared between pretraining and posttraining evaluations. RESULTS: The results indicate that short-term increases in intensity led to significant improvements in muscle activity, spatiotemporal metrics, and joint excursions, with selected improvements in measures of locomotor coordination. High-intensity locomotor training led to significant increases in peak gait speed (0.64-0.80 m/s), and spatiotemporal and kinematic metrics indicate a trend for improved coordination. LIMITATIONS: Measures of gait performance were assessed during treadmill ambulation and not compared with a control group. Generalizability of these results to overground ambulation is unknown. CONCLUSIONS: High-intensity locomotor exercise and training does not degrade, but rather improves, locomotor function and quality in individuals with iSCI, which contrasts with traditional theories of motor dysfunction following neurologic injury.

Potential contributions of training intensity on locomotor performance in individuals with chronic stroke.

BACKGROUND AND PURPOSE: Many interventions can improve walking ability of individuals with stroke, although the training parameters that maximize recovery are not clear. For example, the contribution of training intensity has not been well established and may contribute to the efficacy of many locomotor interventions. The purpose of this preliminary study was to evaluate the effects of locomotor training intensity on walking outcomes in individuals with gait deficits poststroke. METHODS: Using a randomized cross-over design, 12 participants with chronic stroke (>6-month duration) performed either high-intensity (70%-80% of heart rate reserve; n = 6) or low-intensity (30%-40% heart rate reserve; n = 6) locomotor training for 12 or fewer sessions over 4 to 5 weeks. Four weeks following completion, the alternate training intervention was performed. Training intensity was manipulated by adding loads or applying resistance during walking, with similar speeds, durations, and amount of stepping practice between conditions. RESULTS: Greater increases in 6-Minute Walk Test performance were observed following high-intensity training compared with low-intensity training. A significant interaction of intensity and order was also observed for 6-Minute Walk Test and peak treadmill speed, with the largest changes in those who performed high-intensity training first. Moderate correlations were observed between locomotor outcomes and measures of training intensity. CONCLUSION: This study provides the first evidence that the intensity of locomotor practice may be an important independent determinant of walking outcomes poststroke. In the clinical setting, the intensity of locomotor training can be manipulated in many ways, although this represents only 1 parameter to consider.Video Abstract available for more insights from the authors (see Supplemental Digital Content 1, http://links.lww.com/JNPT/A90).