Erin V. L. Vasudevan

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.

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.

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. Summary: Neuronal interactions between arm and leg activity during rhythmic human movement assist in coordinating locomotion and may be usefully exploited in rehabilitation of walking.

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.

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.

Chapter 4 – Locomotor adaptation

Motor learning is an essential part of human behavior, but poorly understood in the context of walking control. Here, we discuss our recent work on locomotor adaptation, which is an error driven motor learning process used to alter spatiotemporal elements of walking. Locomotor adaptation can be induced using a split-belt treadmill that controls the speed of each leg independently. Practicing split-belt walking changes the coordination between the legs, resulting in storage of a new walking pattern. Here, we review findings from this experimental paradigm regarding the learning and generalization of locomotor adaptation. First, we discuss how split-belt walking adaptation develops slowly throughout childhood and adolescence. Second, we demonstrate that conscious effort to change the walking pattern during split-belt training can speed up adaptation but worsens retention. In contrast, distraction (i.e., performing a dual task) during training slows adaptation but improves retention. Finally, we show the walking pattern acquired on the split-belt treadmill generalizes to natural walking when vision is removed. This suggests that treadmill learning can be generalized to different contexts if visual cues specific to the treadmill are removed. These findings allow us to highlight the many future questions that will need to be answered in order to develop more rational methods of rehabilitation for walking deficits.

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.

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.

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 versions 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 wearers 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.

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 ineffcient 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 over-ground 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.