Context-Specificity of Locomotor Learning Is Developed during Childhood.

Humans can perform complex movements with speed and agility in the face of constantly changing task demands. To accomplish this, motor plans are adapted to account for errors in our movements because of changes in our body (e.g., growth or injury) or in the environment (e.g., walking on sand vs ice). It has been suggested that adaptation that occurs in response to changes in the state of our body will generalize across different movement contexts and environments, whereas adaptation that occurs with alterations in the external environment will be context-specific. Here, we asked whether the ability to form generalizable versus context-specific motor memories develops during childhood. We performed a cross-sectional study of context-specific locomotor adaptation in 35 children (3-18 years old) and 7 adults (19-31 years old). Subjects first adapted their gait and learned a new walking pattern on a split-belt treadmill, which has two belts that move each leg at a different speed. Then, subjects walked overground to assess the generalization of the adapted walking pattern across different environments. Our results show that the generalization of treadmill after-effects to overground walking decreases as subjects' age increases, indicating that age and experience are critical factors regulating the specificity of motor learning. Our results suggest that although basic locomotor patterns are established by two years of age, brain networks required for context-specific locomotor learning are still being developed throughout youth.

A Brake-Based Overground Gait Rehabilitation Device for Altering Propulsion Impulse Symmetry.

This paper introduces a new device for gait rehabilitation, the gait propulsion trainer (GPT). It consists of two main components (a stationary device and a wearable system) that work together to apply periodic stance-phase resistance as the user walks overground. The stationary device provides the resistance forces via a cable that tethers the user's pelvis to a magnetic-particle brake. The wearable system detects gait events via foot switches to control the timing of the resistance forces. A hardware verification test confirmed that the GPT functions as intended. We conducted a pilot study in which one healthy adult and one stroke survivor walked with the GPT with increasing resistance levels. As hypothesized, the periodic stance-phase resistance caused the healthy participant to walk asymmetrically, with greatly reduced propulsion impulse symmetry; as GPT resistance increased, the walking speed also decreased, and the propulsion impulse appeared to increase for both legs. In contrast, the stroke participant responded to GPT resistance by walking faster and more symmetrically in terms of both propulsion impulse and step length. Thus, this paper shows promising results of short-term training with the GPT, and more studies will follow to explore its long-term effects on hemiparetic gait.

Making Sense of Cerebellar Contributions to Perceptual and Motor Adaptation.

The cerebellum is thought to adapt movements to changes in the environment in order to update an implicit understanding of the association between our motor commands and their sensory consequences. This trial-by-trial motor recalibration in response to external perturbations is frequently impaired in people with cerebellar damage. In healthy people, adaptation to motor perturbations is also known to induce a form of sensory perceptual recalibration. For instance, hand-reaching adaptation tasks produce transient changes in the sense of hand position, and walking adaptation tasks can lead to changes in perceived leg speed. Though such motor adaptation tasks are heavily dependent on the cerebellum, it is not yet understood how the cerebellum is associated with these accompanying sensory recalibration processes. Here we asked if the cerebellum is required for the recalibration of leg-speed perception that normally occurs alongside locomotor adaptation, as well as how ataxia severity is related to sensorimotor recalibration deficits in patients with cerebellar damage. Cerebellar patients performed a speed-matching task to assess perception of leg speed before and after walking on a split-belt treadmill, which has two belts driving each leg at a different speed. Healthy participants update their perception of leg speed following split-belt walking such that the "fast" leg during adaptation feels slower afterwards, whereas cerebellar patients have significant deficits in this sensory perceptual recalibration. Furthermore, our analysis demonstrates that ataxia severity is a crucial factor for both the sensory and motor adaptation impairments that affect patients with cerebellar damage.

Using a Split-belt Treadmill to Evaluate Generalization of Human Locomotor Adaptation.

Understanding the mechanisms underlying locomotor learning helps researchers and clinicians optimize gait retraining as part of motor rehabilitation. However, studying human locomotor learning can be challenging. During infancy and childhood, the neuromuscular system is quite immature, and it is unlikely that locomotor learning during early stages of development is governed by the same mechanisms as in adulthood. By the time humans reach maturity, they are so proficient at walking that it is difficult to come up with a sufficiently novel task to study de novo locomotor learning. The split-belt treadmill, which has two belts that can drive each leg at a different speed, enables the study of both short- (i.e., immediate) and long-term (i.e., over minutes-days; a form of motor learning) gait modifications in response to a novel change in the walking environment. Individuals can easily be screened for previous exposure to the split-belt treadmill, thus ensuring that all experimental participants have no (or equivalent) prior experience. This paper describes a typical split-belt treadmill adaptation protocol that incorporates testing methods to quantify locomotor learning and generalization of this learning to other walking contexts. A discussion of important considerations for designing split-belt treadmill experiments follows, including factors like treadmill belt speeds, rest breaks, and distractors. Additionally, potential but understudied confounding variables (e.g., arm movements, prior experience) are considered in the discussion.

Neuromechanical interactions between the limbs during human locomotion: an evolutionary perspective with translation to rehabilitation.

During bipedal locomotor activities, humans use elements of quadrupedal neuronal limb control. Evolutionary constraints can help inform the historical ancestry for preservation of these core control elements support transfer of the huge body of quadrupedal non-human animal literature to human rehabilitation. In particular, this has translational applications for neurological rehabilitation after neurotrauma where interlimb coordination is lost or compromised. The present state of the field supports including arm activity in addition to leg activity as a component of gait retraining after neurotrauma.

Gait Transitions in Human Infants: Coping with Extremes of Treadmill Speed.

Spinal pattern generators in quadrupedal animals can coordinate different forms of locomotion, like trotting or galloping, by altering coordination between the limbs (interlimb coordination). In the human system, infants have been used to study the subcortical control of gait, since the cerebral cortex and corticospinal tract are immature early in life. Like other animals, human infants can modify interlimb coordination to jump or step. Do human infants possess functional neuronal circuitry necessary to modify coordination within a limb (intralimb coordination) in order to generate distinct forms of alternating bipedal gait, such as walking and running? We monitored twenty-eight infants (7-12 months) stepping on a treadmill at speeds ranging between 0.06-2.36 m/s, and seventeen adults (22-47 years) walking or running at speeds spanning the walk-to-run transition. Six of the adults were tested with body weight support to mimic the conditions of infant stepping. We found that infants could accommodate a wide range of speeds by altering stride length and frequency, similar to adults. Moreover, as the treadmill speed increased, we observed periods of flight during which neither foot was in ground contact in infants and in adults. However, while adults modified other aspects of intralimb coordination and the mechanics of progression to transition to a running gait, infants did not make comparable changes. The lack of evidence for distinct walking and running patterns in infants suggests that the expression of different functional, alternating gait patterns in humans may require neuromuscular maturation and a period of learning post-independent walking.

Gait speed influences aftereffect size following locomotor adaptation, but only in certain environments.

Movements learned in one set of conditions may not generalize to other conditions. For example, practicing walking on a split-belt treadmill subsequently changes coordination between the legs during normal ("tied-belt") treadmill walking; however, there is limited generalization of these aftereffects to natural walking over the ground. We hypothesized that generalization of split-belt treadmill adaptation to over-ground walking would be improved by maintaining consistency in other task variables, specifically gait speed. This hypothesis was based on our previous finding that treadmill aftereffect size was sensitive to gait speed: Aftereffects were largest when tested on tied-belts running at the same speed as the slower belt during split-belt adaptation. In the present study, healthy adults were assigned to a "slow" or "fast" over-ground walking group. Both groups adapted to split-belts (0.7:1.4 m/s), and treadmill aftereffects were tested on tied-belts at the slow (0.7 m/s) and fast (1.4 m/s) speeds. All participants were subsequently transferred to the over-ground environment. The slow and fast groups walked over-ground at 0.7 and 1.4 m/s, respectively. As in previous work, we found that the size of aftereffects during treadmill walking was speed-dependent, with larger aftereffects occurring at 0.7 m/s compared with 1.4 m/s. However, over-ground walking aftereffects were less sensitive to changes in gait speed. We also found that aftereffects in spatial coordination generalized more to over-ground walking than aftereffects in temporal coordination across all speeds of walking. This suggests that different factors influence aftereffect size in different walking environments and for different measures of coordination.

Effects of traumatic brain injury on locomotor adaptation.

BACKGROUND AND PURPOSE: Locomotor adaptation is a form of short-term learning that enables gait modifications and reduces movement errors when the environment changes. This adaptation is critical for community ambulation for example, when walking on different surfaces. While many individuals with traumatic brain injury (TBI) recover basic ambulation, less is known about recovery of more complex locomotor skills, like adaptation. The purpose of this study was to investigate how TBI affects locomotor adaptation. METHODS: Fourteen adults with TBI and 11 nondisabled comparison participants walked for 15 minutes on a split-belt treadmill with 1 belt moving at 0.7 m/s, and the other at 1.4 m/s. Subsequently, aftereffects were assessed and de-adapted during 15 minutes of tied-belt walking (both belts at 0.7 m/s). RESULTS: Participants with TBI showed greater asymmetry in interlimb coordination on split-belts than the comparison group. Those with TBI did not adapt back to baseline symmetry, and some individuals did not store significant aftereffects. Greater asymmetry on split-belts and smaller aftereffects were associated with greater ataxia. DISCUSSION: Participants with TBI were more perturbed by walking on split-belts and showed some impairment in adaptation. This suggests a reduced ability to learn a new form of coordination to compensate for environmental changes. Multiple interacting factors, including cerebellar damage and impairments in higher-level cognitive processes, may influence adaptation post-TBI. CONCLUSIONS: Gait adaptation to novel environment demands is impaired in persons with chronic TBI and may be an important skill to target in rehabilitation. VIDEO ABSTRACT AVAILABLE: (See Video, Supplemental Digital Content 1, http://links.lww.com/JNPT/A74) for more insights from the authors.

Modulating locomotor adaptation with cerebellar stimulation.

Human locomotor adaptation is necessary to maintain flexibility of walking. Several lines of research suggest that the cerebellum plays a critical role in motor adaptation. In this study we investigated the effects of noninvasive stimulation of the cerebellum to enhance locomotor adaptation. We found that anodal cerebellar transcranial direct current stimulation (tDCS) applied during adaptation expedited the adaptive process while cathodal cerebellar tDCS slowed it down, without affecting the rate of de-adaptation of the new locomotor pattern. Interestingly, cerebellar tDCS affected the adaptation rate of spatial but not temporal elements of walking. It may be that spatial and temporal control mechanisms are accessible through different neural circuits. Our results suggest that tDCS could be used as a tool to modulate locomotor training in neurological patients with gait impairments.

Motor adaptation training for faster relearning.

Adaptation is an error-driven motor learning process that can account for predictable changes in the environment (e.g., walking on ice) or in ourselves (e.g., injury). Our ability to recall and build upon adapted motor patterns across days is essential to this learning process. We investigated how different training paradigms affect the day-to-day memory of an adapted walking pattern. Healthy human adults walked on a split-belt treadmill, and returned the following day to assess recall, relearning rate, and performance. In the first experiment, one group adapted and de-adapted (i.e., washed-out the learning) several times on day 1 to practice the initial stage of learning where errors are large; another group adapted only one time and then practiced in the adapted ("learned") state where errors were small. On day 2, they performed washout trials before readapting. The group that repeatedly practiced the initial portion of adaptation where errors are large showed the fastest relearning on the second day. In fact, the memory was nearly as strong as that of a third group that was left overnight in the adapted state and was not washed-out before reexposure on the second day. This demonstrates that alternating exposures to early adaptation and washout can enhance readaptation. In the second experiment, we tested whether the opposite split-belt pattern interferes with day 2 relearning. Surprisingly, it did not, and instead was similar to practicing in the adapted state. These results show that the structure of the initial phase of learning influences the ease of motor relearning.

Multi-frequency arm cycling reveals bilateral locomotor coupling to increase movement symmetry.

Upright stance has allowed for substantial flexibility in how the upper limbs interact with each other: the arms can be coordinated in alternating, synchronous, or asymmetric patterns. While synchronization is thought to be the default mode of coordination during bimanual movement, there is little evidence for any bilateral coupling during locomotor-like arm cycling movements. Multi-frequency tasks have been used to reveal bilateral coupling during bimanual movements, thus here we used a multi-frequency task to determine whether the arms are coupled during arm cycling. It was hypothesized that bilateral coupling would be revealed as changes in background EMG and cutaneous reflexes when temporal coordination was altered. Twelve subjects performed arm cycling at 1 and 2 Hz with one arm while the contralateral arm was either at rest, cycling at the same frequency, or cycling at a different frequency (i.e., multi-frequency cycling with one arm at 1 Hz and the other at 2 Hz). To evoke reflexes, the superficial radial nerve was stimulated at the wrist. EMG was collected continuously from muscles of both arms. Results showed that background EMG in the lower frequency arm was amplified while reflex amplitudes were unaltered during multi-frequency cycling. We propose that neural coupling between the arms aids in equalizing muscle activity during asymmetric tasks to permit stable movement. Conversely, such interactions between the arms would likely be unnecessary in determining a reflexive response to a perturbation of one arm. Therefore, bilateral coupling was expressed when it was relevant to symmetry.

Unique characteristics of motor adaptation during walking in young children.

Children show precocious ability in the learning of languages; is this the case with motor learning? We used split-belt walking to probe motor adaptation (a form of motor learning) in children. Data from 27 children (ages 8-36 mo) were compared with those from 10 adults. Children walked with the treadmill belts at the same speed (tied belt), followed by walking with the belts moving at different speeds (split belt) for 8-10 min, followed again by tied-belt walking (postsplit). Initial asymmetries in temporal coordination (i.e., double support time) induced by split-belt walking were slowly reduced, with most children showing an aftereffect (i.e., asymmetry in the opposite direction to the initial) in the early postsplit period, indicative of learning. In contrast, asymmetries in spatial coordination (i.e., center of oscillation) persisted during split-belt walking and no aftereffect was seen. Step length, a measure of both spatial and temporal coordination, showed intermediate effects. The time course of learning in double support and step length was slower in children than in adults. Moreover, there was a significant negative correlation between the size of the initial asymmetry during early split-belt walking (called error) and the aftereffect for step length. Hence, children may have more difficulty learning when the errors are large. The findings further suggest that the mechanisms controlling temporal and spatial adaptation are different and mature at different times.

Younger is not always better: development of locomotor adaptation from childhood to adulthood.

New walking patterns can be learned over short timescales (i.e., adapted in minutes) using a split-belt treadmill that controls the speed of each leg independently. This leads to storage of a modified spatial and temporal motor pattern that is expressed as an aftereffect in regular walking conditions. Because split-belt walking is a novel task for adults and children alike, we used it to investigate how motor adaptation matures during human development. We also asked whether the immature pattern resembles that of people with cerebellar dysfunction, because we know that this adaptation depends on cerebellar integrity. Healthy children (3-18 years old) and adults, and individuals with cerebellar damage were adapted while walking on split belts (1:2 speed ratio). Adaptation and de-adaptation rates were quantified separately for temporal and spatial parameters. All healthy children and adults tested could learn the new timing at the same rate and showed significant aftereffects. However, children younger than 6 years old were unable to learn the new spatial coordination. Furthermore, children as old as age 11 years old showed slower rates of adaptation and de-adaptation of spatial parameters of walking. Young children showed patterns similar to cerebellar patients, with greater deficits in spatial versus temporal adaptation. Thus, although walking is a well-practiced, refined motor skill by late childhood (i.e., 11 years of age), the processes underlying learning new spatial relationships between the legs are still developing. The maturation of locomotor adaptation follows at least two time courses, which we propose is determined by the developmental state of the cerebellum.

Design and Pilot Study of a Gait Enhancing Mobile Shoe.

Hemiparesis is a frequent and disabling consequence of stroke and can lead to asymmetric and inefficient walking patterns. Training on a split-belt treadmill, which has two separate treads driving each leg at a different speed, can correct such asymmetries post-stroke. However, the effects of split-belt treadmill training only partially transfer to everyday walking over ground and extended training sessions are required to achieve long-lasting effects. Our aim is to develop an alternative device, the Gait Enhancing Mobile Shoe (GEMS), that mimics the actions of the split-belt treadmill, but can be used during overground walking and in one's own home, thus enabling long-term training. The GEMS does not require any external power and is completely passive; all necessary forces are redirected from the natural forces present during walking. Three healthy subjects walked on the shoes for twenty minutes during which one GEMS generated a backward motion and the other GEMS generated a forward motion. Our preliminary experiments suggest that wearing the GEMS did cause subjects to modify coordination between the legs and these changes persisted when subjects returned to normal over-ground walking. The largest effects were observed in measures of temporal coordination (e.g., duration of double-support). These results suggest that the GEMS is capable of altering overground walking coordination in healthy controls and could potentially be used to correct gait asymmetries post-stroke.

Motion controlled gait enhancing mobile shoe for rehabilitation.

Walking on a split-belt treadmill, which has two belts that can be run at different speeds, has been shown to improve walking patterns post-stroke. However, these improvements are only temporarily retained once individuals transition to walking over ground. We hypothesize that longer-lasting effects would be observed if the training occurred during natural walking over ground, as opposed to on a treadmill. In order to study such long-term effects, we have developed a mobile and portable device which can simulate the same gait altering movements experienced on a split-belt treadmill. The new motion controlled gait enhancing mobile shoe improves upon the previous version's drawbacks. This version of the GEMS has motion that is continuous, smooth, and regulated with on-board electronics. A vital component of this new design is the Archimedean spiral wheel shape that redirects the wearer's downward force into a horizontal backward motion. The design is passive and does not utilize any motors. Its motion is regulated only by a small magnetic particle brake. Further experimentation is needed to evaluate the long-term after-effects.

Split-belt treadmill adaptation shows different functional networks for fast and slow human walking.

New walking patterns can be learned over short time scales (i.e., adapted in minutes) using a split-belt treadmill that controls the speed of each leg independently. This leads to storage of a modified motor pattern that is expressed as an aftereffect in regular walking conditions and must be de-adapted to return to normal. Here we asked whether the nervous system adapts a general walking pattern that is used across many speeds or a specific pattern affecting only the two speeds experienced during split-belt training. In experiment 1, we tested three groups of healthy adult subjects walking at different split-belt speed combinations and then assessed aftereffects at a range of speeds. We found that aftereffects were largest at the slower speed that was used in split-belt training in all three groups, and it decayed gradually for all other speeds. Thus adaptation appeared to be more strongly linked to the slow walking speed. This result suggests a separation in the functional networks used for fast and slow walking. We tested this in experiment 2 by adapting walking to split belts and then determining how much fast regular walking washed out the slow aftereffect and vice versa. We found that 23-38% of the aftereffect remained regardless of which speed was washed out first. This demonstrates that there is only partial overlap in the functional networks coordinating different walking speeds. Taken together, our results suggest that there are some neural networks for controlling locomotion that are recruited specifically for fast versus slow walking in humans, similar to recent findings in other vertebrates.

The quadrupedal nature of human bipedal locomotion.

During rhythmic movement, arm activity contributes to the neural excitation of leg muscles. These observations are consistent with the emergence of human bipedalism and nonhuman primate arboreal quadrupedal walking. These neural and biomechanical linkages could be exploited in rehabilitation after neurotrauma to allow the arms to give the legs a helping hand during gait rehabilitation.