Ryan T. Roemmich

Effects of dopaminergic therapy on locomotor adaptation and adaptive learning in persons with Parkinson's disease

Persons with Parkinsons disease (PD) are characterized by multifactorial gait deficits, though the factors which influence the abilities of persons with PD to adapt and store new gait patterns are unclear. The purpose of this study was to investigate the effects of dopaminergic therapy on the abilities of persons with PD to adapt and store gait parameters during split-belt treadmill (SBT) walking. Ten participants with idiopathic PD who were being treated with stable doses of orally-administered dopaminergic therapy participated. All participants performed two randomized testing sessions on separate days: once while optimally-medicated (ON meds) and once after 12-h withdrawal from dopaminergic medication (OFF meds). During each session, locomotor adaptation was investigated as the participants walked on a SBT for 10 min while the belts moved at a 2:1 speed ratio. We assessed locomotor adaptive learning by quantifying: (1) aftereffects during de-adaptation (once the belts returned to tied speeds immediately following SBT walking) and (2) savings during re-adaptation (as the participants repeated the same SBT walking task after washout of aftereffects following the initial SBT task). The withholding of dopaminergic medication diminished step length aftereffects significantly during de-adaptation. However, both locomotor adaptation and savings were unaffected by levodopa. These findings suggest that dopaminergic pathways influence aftereffect storage but do not influence locomotor adaptation or savings within a single session of SBT walking. It appears important that persons with PD should be optimally-medicated if walking on the SBT as gait rehabilitation.

Visuomotor Learning Generalizes Around the Intended Movement.

Abstract Human motor learning is useful if it generalizes beyond the trained task. Here, we introduce a new idea about how human visuomotor learning generalizes. We show that learned reaching movements generalize around where a person intends to move (i.e., aiming direction) as opposed to where they actually move. We used a visual rotation paradigm that allowed us to disentangle whether generalization is centered on where people aim to move, where they actually move, or where visual feedback indicates they moved. Participants reached to a visual target with their arm occluded from view. The cursor feedback was rotated relative to the position of their unseen hand to induce learning. Participants verbally reported their aiming direction, reached, and then were shown the outcome. We periodically introduced single catch trials with no feedback to measure learning. Results showed that learning was maximal at the participants’ aiming location, and not at the actual hand position or where the cursor was displayed. This demonstrates that visuomotor learning generalizes around where we intend to move rather than where we actually move, and thus introduces a new role for cognitive processes beyond simply reducing movement error.

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.

Execution of Activities of Daily Living in Persons with Parkinson Disease.

INTRODUCTION Muscular weakness and the motor difficulties associated with Parkinson disease (PD) often impair the performance of activities of daily living (ADL). However, little is known about the magnitude and distribution of relative muscular effort of persons with PD during ADL. The purpose of this investigation was to determine the relative magnitude of lower extremity moment production that persons with PD use to perform common ADL. METHODS Fifteen participants with mild-to-moderate PD and 14 age/sex-matched controls volunteered. Participants performed a series of ADL tasks, as follows: gait initiation (GI), gait, and stair ascending tasks. Participants were then asked to perform maximal-effort isokinetic tests of hip and knee extension and ankle plantarflexion at speeds of 90° per second and 120° per second. Relative effort was quantified as a percentage of the maximal isokinetic value produced by a joint during performance of the ADL. Relative effort and peak isokinetic joint moments were analyzed using a mixed-model ANOVA with repeated measures. All other comparisons were evaluated using independent t-tests. RESULTS Persons with PD produced smaller ankle plantarflexion moment at both 90° per second and 120° per second (P < 0.05). Relative effort during GI (271% vs 189%, P < 0.05) and gait (270% vs 161%, P < 0.05) was significantly greater at the ankle in persons with PD. Contribution of the ankle to the support moment was lower in PD during stair ascending (24% vs 34%) and GI (63% vs 57%) compared with that in controls. CONCLUSIONS The reduced ankle moments during ADL are indicative of deficits in muscular capabilities in those with PD. Moreover, PD caused a redistribution of joint torques, such that PD participants used their hip extensors more and ankle plantarflexors less.

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).

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.

Comparing Aftereffects after Split-Belt Treadmill Walking and Unilateral Stepping.

PURPOSE Asymmetric step length is a problem common to many orthopedic and neurologic populations. Herein, we compare step length aftereffects during overground gait after two rehabilitation intervention strategies to combat step length asymmetry: split-belt treadmill (SBT) walking and unilateral stepping. METHODS Eighteen healthy young adults (22 ± 3 yr) first performed 10 overground gait trials. Participants then walked for 10 min under three different treadmill conditions in a randomized order: SBT walking, slow unilateral stepping, and fast unilateral stepping. Immediately after each treadmill condition, participants performed ten overground gait trials. Mean step length asymmetry was calculated across the first five strides of the overground gait trials to assess the storage of aftereffects after each treadmill condition. We also explored the lower extremity kinematics during each treadmill condition to investigate movement patterns that lead to greatest aftereffects. RESULTS Significantly higher step length asymmetry was observed in overground gait trials after SBT walking compared to those after slow and fast unilateral stepping, indicating greater aftereffect/carryover of the SBT walking pattern to overground gait. During fast unilateral stepping, increased flexion in the hip, knee, and ankle of the stationary limb was significantly associated with increased step length aftereffects. CONCLUSIONS The aftereffects observed after acute SBT walking were significantly greater than those after unilateral stepping. Both exercises induce aftereffects of similar kinematic patterns, although likely through different mechanisms. In sum, SBT walking induces the greatest aftereffects, although unilateral stepping also induces a change in gait behavior. During unilateral stepping, the largest aftereffects occur when the walker does not simply fully extend the stationary limb and allow the treadmill to passively move the stepping limb during stance.

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.

Independent voluntary correction and savings in locomotor learning

ABSTRACT 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. Summary: Fast, voluntary changes to human walking patterns do not affect the motor memory formed through simultaneous adaptive learning.

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.