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3 – Article: Movement error is not the best predictor of adaptive plasticity during human walking

Résumé

INTRODUCTION : Des études portant sur la planification motrice ont montré qu’il était possible d’induire une modification de la commande motrice en induisant une erreur de mouvement dans la trajectoire planifiée du membre. Patton et Mussa-Ivaldi (2004) ont suggéré que des champs de force standardisés pourraient être induits à l’aide d’outils robotisés afin de mettre à profit cette aptitude et d’aider les participants à apprendre un nouveau patron locomoteur. Il demeure toutefois nécessaire de valider si cette approche peut être appliquée directement en réadaptation locomotrice. Le but de cette étude est de valider l’effet d’une variation dans la force et la direction de l’erreur de mouvement sur la capacité adaptative à la marche.

MÉTHODE : Seize participants ont été exposés à quatre types de perturbations appliquées à la cheville par une orthèse robotisée alors qu’il marchait sur un tapis roulant. Les deux premiers furent exposés à des perturbations sporadiques afin de valider la faisabilité du protocol expérimental. Les 14 autres participant furent exposés au protocole complet comprenant une séquence randomisée de 4 conditions expérimentales, chacune séparée de 5 minutes de marche non perturbée. Chaque condition expérimentale (C1 à C4) impliquait une 1 perturbation survenant en moyenne à chaque 5 cycles de marche complétés, suivant une séquence pseudorandomisée. Chaque perturbation durait 150 ms et était appliqué durant la phase d’oscillation (72% du cycle de marche). C1 comprenait des étirements en plantiflexion de 6° à 120°/s. C2 et C3 appliquaient une force résistive et assistive de ±5Nm respectivement. C4 consistait à immobiliser transitoirement le mouvement à la cheville. Chaque participant recevait la consigne de marche le plus normalement possible, à leur vitesse de confort (3,6-4km/h) sans utiliser leurs mains pour s’appuyer. Les données cinématiques de la cheville et électromyographique du tibial antérieur et du soléaire furent enregistrées.

RÉSULTATS : Un minimum de 12/14 participants ont montré des signes d’adaptation en réponse aux conditions C1, C2 et C4. L’exposition à C3 par contre n’induisit pas d’adaptation malgré une erreur de mouvement significative. De même, l’analyse EMG identifia des réponses réflexes dans toutes les conditions sauf C3. Les études de régression montrèrent une corrélation plus puissante entre la réponse réflexe à courte latence et la force de l’adaptation.

CONCLUSION : Seules les perturbations opposant le mouvement planifié ont induit une adaptation. L’étude des réponses réflexes causée par les perturbations suggère une corrélation plus forte de l’adaptation avec la boucle réflexe à courte latence (M1). Cela suggère que l’impact fonctionnel de la perturbation, plutôt que la taille de l’erreur de mouvement, prédit le mieux l’adaptation.

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Abstract

INTRODUCTION: Classical reaching studies have shown that when exposed to a movement error caused by a force field, subjects adapt their muscle activation pattern to return their movement trajectory to baseline. Patton and Mussa-Ivaldi (2004) have proposed that this approach could be used for neuro-rehabilitation, where custom force fields could be created using robotic devices to teach specific movement patterns to patients. Can this approach be directly applied to locomotor rehabilitation? The aim of the present study was to look at the effects of movement error direction and velocity on adaptive capacity during walking.

METHODS: Sixteen subjects wore a robotized ankle-foot orthosis (rAFO) on their right ankle and walked on a treadmill. The first 2 of them were exposed to sporadic perturbation in order to validate the viability of our protocol. Thereafter, the other fourteen subjects were exposed in a randomized sequence to 4 types of perturbations, separated by five minutes of washout period. Each condition (C1 to C4) consisted in applying an average of 1 perturbation every 5 strides, according to an unpredictable pseudorandom sequence. All perturbations lasted 150 ms, and were applied during swing (72% of gait cycle). C1 consisted in a 6° plantarflexion stretch at 120°/s. C2 and C3 consisted in adding ±5Nm force resisting or assisting dorsiflexion, respectively. C4 simply stopped the ankle movement temporarily. Participants were asked to walk normally, hands free, at their comfortable walking speed (3.6 -4 km/h). Ankle kinematics and surface EMG of Tibialis Anterior (TA) and Soleus (SOL) were recorded.

RESULTS: At least 12/14 subjects showed an adaptation pattern, increasing their ankle dorsiflexion in conditions C1, C2, and C4. C3 did not induce any clear adaptation despite the presence of large ankle movement errors, however. EMG analysis demonstrated the presence of reflex responses in all condition except C3. Regression curves shows that short latency response (M1) best correlate with adaptation.

CONCLUSION: These results suggest that a “movement error approach” for locomotor rehabilitation induces adaptation only when resisting ongoing movement. The functional consequence of the error rather than its size could therefore be the trigger for adaptation. Potential underlying mechanisms are discussed.

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3.1 - Introduction

The neural control of walking results from the interaction of spinal, supraspinal and peripheral mechanisms. After lesions to the CNS, gait disorders are present and current rehabilitation methods are not optimal. While several models exist to trigger motor learning needed for motor rehabilitation, several of them are based on the notion of “movement error”, i.e. the difference between expected and actual movement kinematics is used to trigger anticipatory (feedforward) modifications in the next movement. This approach is based on a large literature in the field of reaching, has been proposed as an approach to design motor rehabilitation interventions (Patton and Mussa-Ivaldi) and is more and more used in gait rehabilitation (split-belt, FF training, etc). During walking however, other important factors besides or in combination with movement error need to be considered, such as foot clearance, dynamic balance, and limited degrees of freedom during single limb stance (representing 80% of the gait cycle). Moreover, gait initiation is triggered after the integration of various nervous structures, some of which are unrelated with the corticospinal pathways involved in reaching movements. The central pattern generator (CPG) is one of the main nervous structure involve in gait and is known for his automatic activity. Therefore, it may not be modulated by anticipatory mechanisms in the same way than reaching with the upper limb. Thus, knowledge gained from reaching studies must first be validated during walking in order to optimize motor learning and gait rehabilitation.

Force field (FF) training protocols have been studied during walking for a few years and has shown promising results so far. They were able to induce adapted responses that persist for some time, even after stimulus withdrawal. This adaptive process has been also shown to be partially involuntary. These changes to the drive control were therefore called adaptive plasticity since “structural or biochemical” changes may be involve to allow involuntary and sustained response after stimuli withdrawal. The adaptive plasticity process has also shown to be able to induce different results when exposed to changing force field characteristics (Emken and Reinkensmeyer 2004). The scope of the potential adaptations and the limits of this kind of plasticity are however unknown, as well as underlying mechanisms and neural networks. Therefore, force field related research should be pursued to better understand how and where (in the CNS) adaptive plasticity could be induced and modulated. This knowledge would represent a significant advance in rehab research since it could help develop and optimize lesion-specific protocols for motor RE-learning after injury.

To study central reorganisation in the CNS occurring during adaptive plasticity, in vivo experiments are required to identify dynamic changes that occur during walking. Reflexes has been used in animals and human to be interesting non-invasive probes to test CNS circuits (Misiaszek 2003, Carroll, Baldwin et al. 2006) and could be helpful to identify where structural or biochemical changes take place in the CNS. Indeed, for a same afferent signal, any modulation

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in the reflex efferent response in the muscle would be caused by a change in the reflex’s treatment process in one of the underlying structures of the specific reflex loop used. Force field induced adaptation is, at least, mainly mediated by proprioceptive afferents (Bastian 2008). Thus, stretch reflexes (SR) was thought to be a suitable kind of reflex to access some of the networks since they may be induced by the same sensory information that create movement error. It is not known whether access to the neural networks of motor adaptation involves the neurons constituting the SR’s loops themselves or other neurons carrying a copy of the sensory information. Perturbation of the motor adaptation process using SR also imply that other motor stimuli than conventional FF can induce motor change. Evaluation of different way to initiate adaptation may offer some alternatives to optimize motor re-learning since some force field’s characteristics may correlate better with adaptive plasticity.

The results from the first experiment indicate that a wide range of possibilities has not been explored in locomotor rehabilitation. It may offer some interesting alternatives for optimizing motor re-learning after a CNS injury. The aim of this study is therefore to expand knowledge about locomotor adaptation mechanisms by studying the theoretical potential and limits of adaptive plasticity. To achieve this objective, this study will try to bring a new hypothesis concerning how the circuits underlying adaptation mechanism may work, according to three different aspects: 1) to validate if sporadic perturbations could elicit adaptation, 2) to identify which sensitive afferents is optimal for triggering adaptation and ultimately 3) to better localize where structural or biochemical changes take place in the CNS during motor adaptation.

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3.2 - Materials and methods:

3.2.1 - Subjects

Sixteen subjects (10 females and 6 males), aged 20 to 46 years old, participated in this study. All subjects provide informed consent to the protocol approved by the local ethics committee, and in accordance with the Declaration of Helsinki.