Closing the Loop: From Motor Neuroscience to Neurorehabilitation.

The fields of human motor control, motor learning, and neurorehabilitation have long been linked by the intuition that understanding how we move (and learn to move) leads to better rehabilitation. In reality, these fields have remained largely separate. Our knowledge of the neural control of movement has expanded, but principles that can directly impact rehabilitation efficacy remain somewhat sparse. This raises two important questions: What can basic studies of motor learning really tell us about rehabilitation, and are we asking the right questions to improve the lives of patients? This review aims to contextualize recent advances in computational and behavioral studies of human motor learning within the framework of neurorehabilitation. We also discuss our views of the current challenges facing rehabilitation and outline potential clinical applications from recent theoretical and basic studies of motor learning and control.

Joint-level coordination patterns for split-belt walking across different speed ratios.

Locomotion is a highly flexible process, requiring rapid changes to gait due to changes in the environment or goals. Here, we used a split-belt treadmill to examine how the central nervous system coordinates a novel gait pattern. Existing research has focused on summary measures, most often step lengths, when describing changes induced while walking on the split-belt treadmill and during subsequent aftereffects. Here, we asked how the nervous system adjusts individual joint motions and the coordination pattern of the legs when people walk with one leg moving at either 2×, 3×, or 4× the speed of the other leg. We found that relative to tied-belt walking, split-belt perturbations change the timing relationships between the legs while most joint angle peaks and range of motion change little. The kinematic changes over the course of adaptation (i.e., from the beginning to end of a single split-belt walking bout) were subtle, particularly when comparing individual joint motions. The magnitude of the belt speed differences impacted intralimb coordination but did not produce consistent differences in most other measures. Most significant changes in kinematics occurred in the fast leg. Overall, interlimb timing changes drove a large proportion of the differences observed between tied-belt and split-belt gaits. Thus, it appears that the central nervous system can produce novel gait patterns through changes in coordination between legs that lead to new configurations at significant time points. These patterns can use within-limb and within-joint patterns that closely resemble those of normal walking.NEW & NOTEWORTHY We studied how the nervous system coordinates limb movements during asymmetric gait. Using a split-belt treadmill, we found that most changes in motion occurred when comparing motions between limbs, rather than among joints within a limb. Individual joint patterns resembled speed-matched comparisons, but this meant that joint movements became asymmetric during split-belt walking. These findings demonstrate that the nervous system can use consistent joint motions that are reconfigured in time to achieve new gait patterns.

Two-dimensional video-based analysis of human gait using pose estimation.

Human gait analysis is often conducted in clinical and basic research, but many common approaches (e.g., three-dimensional motion capture, wearables) are expensive, immobile, data-limited, and require expertise. Recent advances in video-based pose estimation suggest potential for gait analysis using two-dimensional video collected from readily accessible devices (e.g., smartphones). To date, several studies have extracted features of human gait using markerless pose estimation. However, we currently lack evaluation of video-based approaches using a dataset of human gait for a wide range of gait parameters on a stride-by-stride basis and a workflow for performing gait analysis from video. Here, we compared spatiotemporal and sagittal kinematic gait parameters measured with OpenPose (open-source video-based human pose estimation) against simultaneously recorded three-dimensional motion capture from overground walking of healthy adults. When assessing all individual steps in the walking bouts, we observed mean absolute errors between motion capture and OpenPose of 0.02 s for temporal gait parameters (i.e., step time, stance time, swing time and double support time) and 0.049 m for step lengths. Accuracy improved when spatiotemporal gait parameters were calculated as individual participant mean values: mean absolute error was 0.01 s for temporal gait parameters and 0.018 m for step lengths. The greatest difference in gait speed between motion capture and OpenPose was less than 0.10 m s-1. Mean absolute error of sagittal plane hip, knee and ankle angles between motion capture and OpenPose were 4.0°, 5.6° and 7.4°. Our analysis workflow is freely available, involves minimal user input, and does not require prior gait analysis expertise. Finally, we offer suggestions and considerations for future applications of pose estimation for human gait analysis.

Precision Rehabilitation: Optimizing Function, Adding Value to Health Care.

Precision medicine efforts are underway in many medical disciplines; however, the power of precision rehabilitation has not yet been explored. Precision medicine aims to deliver the right intervention, at the right time, in the right setting, for the right person, ultimately bolstering the value of the care that we provide. To date, precision medicine efforts have rarely focused on function at the level of a person, but precision rehabilitation is poised to change this and bring the focus on function to the broader precision medicine enterprise. To do this, subgroups of individuals must be identified based on their level of function via precise measurement of their abilities in the physical, cognitive, and psychosocial domains. Adoption of electronic health records, advances in data storage and analytics, and improved measurement technology make this shift possible. Here we detail critical components of the precision rehabilitation framework, including (1) the synergistic use of various study designs, (2) the need for standardized functional measurements, (3) the importance of precise and longitudinal measures of function, (4) the utility of comprehensive databases, (5) the importance of predictive analyses, and (6) the need for system and team science. Precision rehabilitation has the potential to revolutionize clinical care, optimize function for all individuals, and magnify the value of rehabilitation in health care; however, to reap the benefits of precision rehabilitation, the rehabilitation community must actively pursue this shift.

The human preference for symmetric walking often disappears when one leg is constrained.

KEY POINTS: We hypothesized that minimization of metabolic power could drive people to walk asymmetrically when one leg is constrained We studied healthy young adults and independently constrained one or both step lengths to be markedly shorter or longer than preferred using visual feedback When one leg was constrained to take a shorter or longer step than preferred, asymmetric walking patterns were less metabolically costly than symmetric walking patterns When one leg was constrained to take a shorter or longer step than preferred and the other leg was allowed to move freely, most participants naturally adopted an asymmetric gait People may prefer to walk asymmetrically to minimize metabolic power when the function of one leg is constrained during fixed-speed treadmill walking ABSTRACT: The bilateral symmetry inherent in healthy human walking is often disrupted in clinical conditions that primarily affect one leg (e.g. stroke). This seems intuitive: with one leg constrained, gait becomes asymmetric. However, the emergence of asymmetry is not inevitable. Consider that symmetric walking could be preserved by matching the movement of the unconstrained leg to that of the constrained leg. While this is theoretically possible, it is rarely observed in clinical populations. Here, we hypothesized that minimization of metabolic power could drive people to walk asymmetrically when one leg is constrained, even when symmetric walking remains possible. We tested this hypothesis by performing two experiments in healthy adults. In Experiment 1, we constrained one step to be markedly shorter or longer than preferred. We observed that participants could significantly reduce metabolic power by adopting an asymmetric gait (one short/long step, one preferred step) rather than maintaining a symmetric gait (bilateral short/long steps). Indeed, when allowed to walk freely in this situation, participants naturally adopted a less effortful asymmetric gait. In Experiment 2, we applied a milder constraint that more closely approximated magnitudes of step length asymmetry that are observed in clinical populations. Responses in this experiment were more heterogeneous, though most participants adopted an asymmetric gait. These findings support two central conclusions: (1) symmetry is not necessarily energetically optimal in constrained human walking, and (2) people may prefer to walk asymmetrically to minimize metabolic power when one leg is constrained during fixed-speed treadmill walking, especially when the constraint is large.

Applications of Pose Estimation in Human Health and Performance across the Lifespan.

The emergence of pose estimation algorithms represents a potential paradigm shift in the study and assessment of human movement. Human pose estimation algorithms leverage advances in computer vision to track human movement automatically from simple videos recorded using common household devices with relatively low-cost cameras (e.g., smartphones, tablets, laptop computers). In our view, these technologies offer clear and exciting potential to make measurement of human movement substantially more accessible; for example, a clinician could perform a quantitative motor assessment directly in a patient's home, a researcher without access to expensive motion capture equipment could analyze movement kinematics using a smartphone video, and a coach could evaluate player performance with video recordings directly from the field. In this review, we combine expertise and perspectives from physical therapy, speech-language pathology, movement science, and engineering to provide insight into applications of pose estimation in human health and performance. We focus specifically on applications in areas of human development, performance optimization, injury prevention, and motor assessment of persons with neurologic damage or disease. We review relevant literature, share interdisciplinary viewpoints on future applications of these technologies to improve human health and performance, and discuss perceived limitations.

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.

Persons with essential tremor can adapt to new walking patterns.

Essential tremor (ET) is a common movement disorder that causes motor deficits similar to those seen in cerebellar disorders. These include kinetic tremor, gait ataxia, and impaired motor adaptation. Previous studies of motor adaptation in ET have focused on reaching while the effects of ET on gait adaptation are currently unknown. The purpose of this study was to contrast locomotor adaptation in persons with and without ET. We hypothesized that persons with ET would show impaired gait adaptation. In a cross-sectional study, persons with ET (n = 14) and healthy matched controls (n = 12) walked on a split-belt treadmill. Participants walked with the belts moving at a 2:1 ratio, followed by overground walking to test transfer, followed by a readaptation period and finally a deadaptation period. Step length asymmetry was measured to assess the rate of adaptation, amount of transfer, and rates of readaptation and deadaptation. Spatial, temporal, and velocity contributions to step length asymmetry were analyzed during adaptation. There were no group by condition interactions in step length asymmetry or contributions to step length asymmetry. Regardless of condition, persons with ET walked slower and exhibited lower temporal (P < 0.001) and velocity (P = 0.001) contributions to step length asymmetry than controls. Persons with ET demonstrated a preserved ability to adapt to, store, and transfer a new walking pattern. Despite probable cerebellar involvement in ET, locomotor adaptation is an available mechanism to teach persons with ET new gait patterns.NEW & NOTEWORTHY This study is the first to investigate walking adaptation abilities of people with essential tremor. Despite evidence of cerebellar impairment in this population, people with essential tremor can adapt their walking patterns. However, people with essential tremor do not modulate the timing of their footsteps to meet walking demands. Therefore, this study is the first to report impairments in the temporal aspects of walking in people with essential tremor during both typical and locomotor learning.

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.

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.

Motor learning in childhood reveals distinct mechanisms for memory retention and re-learning.

Adults can easily learn and access multiple versions of the same motor skill adapted for different conditions (e.g., walking in water, sand, snow). Following even a single session of adaptation, adults exhibit clear day-to-day retention and faster re-learning of the adapted pattern. Here, we studied the retention and re-learning of an adapted walking pattern in children aged 6-17 yr. We found that all children, regardless of age, showed adult-like patterns of retention of the adapted walking pattern. In contrast, children under 12 yr of age did not re-learn faster on the next day after washout had occurred-they behaved as if they had never adapted their walking before. Re-learning could be improved in younger children when the adaptation time on day 1 was increased to allow more practice at the plateau of the adapted pattern, but never to adult-like levels. These results show that the ability to store a separate, adapted version of the same general motor pattern does not fully develop until adolescence, and furthermore, that the mechanisms underlying the retention and rapid re-learning of adapted motor patterns are distinct.

Split-Belt Treadmill Walking Alters Lower Extremity Frontal Plane Mechanics.

Interventions that manipulate gait speed may also affect the control of frontal plane mechanics. Expanding the current knowledge of frontal plane adaptations during split-belt treadmill walking could advance our understanding of the influence of asymmetries in gait speed on frontal plane mechanics and provide insight into the breadth of adaptations required by split-belt walking (SBW). Thirteen young, healthy participants, free from lower extremity injury walked on a split-belt treadmill with belts moving simultaneously at different speeds. We examined frontal plane mechanics of the ankle, knee, and hip joints during SBW, as well as medio-lateral ground reaction forces (ML-GRF). We did not observe alterations in the frontal mechanics produced during early or late adaptation of SBW when compared to conditions where the belts moved together. We did observe that ML-GRF and hip moment impulse of the fast limb increased over time with adaptation to SBW. These results suggest this modality may provide a unique therapy for individuals with gait pathologies, impairments, or compensation(s).

Blocking trial-by-trial error correction does not interfere with motor learning in human walking.

Movements can be learned implicitly in response to new environmental demands or explicitly through instruction and strategy. The former is often studied in an environment that perturbs movement so that people learn to correct the errors and store a new motor pattern. Here, we demonstrate in human walking that implicit learning of foot placement occurs even when an explicit strategy is used to block changes in foot placement during the learning process. We studied people learning a new walking pattern on a split-belt treadmill with and without an explicit strategy through instruction on where to step. When there is no instruction, subjects implicitly learn to place one foot in front of the other to minimize step-length asymmetry during split-belt walking, and the learned pattern is maintained when the belts are returned to the same speed, i.e., postlearning. When instruction is provided, we block expression of the new foot-placement pattern that would otherwise naturally develop from adaptation. Despite this appearance of no learning in foot placement, subjects show similar postlearning effects as those who were not given any instruction. Thus locomotor adaptation is not dependent on a change in action during learning but instead can be driven entirely by an unexpressed internal recalibration of the desired movement.

Two ways to save a newly learned motor pattern.

Savings, or faster relearning after initial learning, demonstrates humans' remarkable ability to retain learned movements amid changing environments. This is important within the context of locomotion, as the ability of the nervous system to "remember" how to walk in specific environments enables us to navigate changing terrains and progressively improve gait patterns with rehabilitation. Here, we used a split-belt treadmill to study precisely how people save newly learned walking patterns. In Experiment 1, we investigated savings by systematically varying the learning and unlearning environments. Savings was predominantly influenced by 1) previous exposure to similar abrupt changes in the environment and 2) the amount of exposure to the new environment. Relearning was fastest when these two factors coincided, and we did not observe savings after the environment was introduced gradually during initial learning. In Experiment 2, we then studied whether people store explicit information about different walking environments that mirrors savings of a new walking pattern. Like savings, we found that previous exposure to abrupt changes in the environment also drove the ability to recall a previously experienced walking environment accurately. Crucially, the information recalled was extrinsic information about the learning environment (i.e., treadmill speeds) and not intrinsic information about the walking pattern itself. We conclude that simply learning a new walking pattern is not enough for long-term savings; rather, savings of a learned walking pattern involves recall of the environment or extended training at the learned state.

Understanding mechanisms of generalization following locomotor adaptation.

Our nervous system has the remarkable ability to adapt our gait to accommodate changes in our body or surroundings. However, our adapted walking patterns often generalize only partially (or not at all) between different contexts. Here, we sought to understand how the nervous system generalizes adapted gait patterns from one context to another. Through a series of split-belt treadmill walking experiments, we evaluated different mechanistic hypotheses to explain the partial generalization of adapted gait patterns from split-belt treadmill to overground walking. In support of the credit assignment hypothesis, our experiments revealed the central finding that adaptation involves recalibration of two distinct forward models. Recalibration of the first model generalizes to overground walking, suggesting that the model represents the general movement dynamics of our body. On the other hand, recalibration of the second model does not generalize to overground walking, suggesting the model represents dynamics specific to treadmill walking. These findings reveal that there is a predefined portion of forward model recalibration that generalizes across context, leading to overall partial generalization of walking adaptation.

Clinical gait analysis using video-based pose estimation: Multiple perspectives, clinical populations, and measuring change.

Gait dysfunction is common in many clinical populations and often has a profound and deleterious impact on independence and quality of life. Gait analysis is a foundational component of rehabilitation because it is critical to identify and understand the specific deficits that should be targeted prior to the initiation of treatment. Unfortunately, current state-of-the-art approaches to gait analysis (e.g., marker-based motion capture systems, instrumented gait mats) are largely inaccessible due to prohibitive costs of time, money, and effort required to perform the assessments. Here, we demonstrate the ability to perform quantitative gait analyses in multiple clinical populations using only simple videos recorded using low-cost devices (tablets). We report four primary advances: 1) a novel, versatile workflow that leverages an open-source human pose estimation algorithm (OpenPose) to perform gait analyses using videos recorded from multiple different perspectives (e.g., frontal, sagittal), 2) validation of this workflow in three different populations of participants (adults without gait impairment, persons post-stroke, and persons with Parkinson's disease) via comparison to ground-truth three-dimensional motion capture, 3) demonstration of the ability to capture clinically relevant, condition-specific gait parameters, and 4) tracking of within-participant changes in gait, as is required to measure progress in rehabilitation and recovery. Importantly, our workflow has been made freely available and does not require prior gait analysis expertise. The ability to perform quantitative gait analyses in nearly any setting using only low-cost devices and computer vision offers significant potential for dramatic improvement in the accessibility of clinical gait analysis across different patient populations.

The effect of post-acute rehabilitation setting on 90-day mobility after stroke: A difference-in-difference analysis.

Background: After discharged from the hospital for acute stroke, individuals typically receive rehabilitation in one of three settings: inpatient rehabilitation facilities (IRFs), skilled nursing facilities (SNFs), or home with community services (i.e., home health or outpatient clinics). The initial setting of post-acute care (i.e., discharge location) is related to mortality and hospital readmission; however, the impact of this setting on the change in functional mobility at 90-days after discharge is still poorly understood. The purpose of this work was to examine the impact of discharge location on the change in functional mobility between hospital discharge and 90-days post-discharge. Methods: In this retrospective cohort study, we used the electronic health record to identify individuals admitted to Johns Hopkins Medicine with an acute stroke and who had measurements of mobility [Activity Measure for Post Acute Care Basic Mobility (AM-PAC BM)] at discharge from the acute hospital and 90-days post-discharge. Individuals were grouped by discharge location (IRF=190 [40%], SNF=103 [22%], Home with community services=182 [(38%]). We compared the change in mobility from time of discharge to 90-days post-discharge in each group using a difference-in-differences analysis and controlling for demographics, clinical characteristics, and social determinants of health. Results: We included 475 individuals (age 64.4 [14.8] years; female: 248 [52.2%]). After adjusting for covariates, individuals who were discharged to an IRF had a significantly greater improvement in AM-PAC BM from time of discharge to 90-days post-discharge compared to individuals discharged to a SNF or home with community services (ß=-3.5 (1.4), p=0.01 and ß=-8.2 (1.3), p=<0.001, respectively). Conclusions: These findings suggest that the initial post-acute rehabilitation setting impacts the magnitude of functional recovery at 90-days after discharge from the acute hospital. These findings support the need for high-intensity rehabilitation and for policies that facilitate the delivery of high-intensity rehabilitation after stroke.

Accuracy of Video-Based Gait Analysis Using Pose Estimation During Treadmill Walking Versus Overground Walking in Persons After Stroke.

OBJECTIVE: Video-based pose estimation is an emerging technology that shows significant promise for improving clinical gait analysis by enabling quantitative movement analysis with little costs of money, time, or effort. The objective of this study is to determine the accuracy of pose estimation-based gait analysis when video recordings are constrained to 3 common clinical or in-home settings (ie, frontal and sagittal views of overground walking and sagittal views of treadmill walking). METHODS: Simultaneous video and motion capture recordings were collected from 30 persons after stroke during overground and treadmill walking. Spatiotemporal and kinematic gait parameters were calculated from videos using an open-source human pose estimation algorithm and from motion capture data using traditional gait analysis. Repeated-measures analyses of variance were then used to assess the accuracy of the pose estimation-based gait analysis across the different settings, and the authors examined Pearson and intraclass correlations with ground-truth motion capture data. RESULTS: Sagittal videos of overground and treadmill walking led to more accurate measurements of spatiotemporal gait parameters versus frontal videos of overground walking. Sagittal videos of overground walking resulted in the strongest correlations between video-based and motion capture measurements of lower extremity joint kinematics. Video-based measurements of hip and knee kinematics showed stronger correlations with motion capture versus ankle kinematics for both overground and treadmill walking. CONCLUSION: Video-based gait analysis using pose estimation provides accurate measurements of step length, step time, and hip and knee kinematics during overground and treadmill walking in persons after stroke. Generally, sagittal videos of overground gait provide the most accurate results. IMPACT: Many clinicians lack access to expensive gait analysis tools that can help identify patient-specific gait deviations and guide therapy decisions. These findings show that video-based methods that require only common household devices provide accurate measurements of a variety of gait parameters in persons after stroke and could make quantitative gait analysis significantly more accessible.