Pre-movement contralateral EEG low beta power is modulated with motor adaptation learning

Various neuroimaging studies aim to understand the complex nature of human motor behavior. There exists a variety of experimental approaches to study neurophysiological correlates of performance during different motor tasks. As distinct from studies based on visuomotor learning, we investigate changes in electroencephalographic (EEG) activity during an actual physical motor adaptation learning experiment. Based on statistical analysis of EEG signals collected during a force-field adaptation task performed with the dominant hand, we observe a modulation of pre-movement upper alpha (10-12 Hz) and lower beta (13-16 Hz) powers over the contralateral region. This modulation is observed to be stronger in lower beta range and, through a regression analysis, is shown to be related with motor adaptation performance on a subject-specific level

L’influence de l'anticipation sur les modulations de puissance dans la bande de fréquence bêta durant la préparation du mouvement et L'effet de la variance dans les rétroactions sensorielles sur la rétention à court terme

La production du mouvement est un aspect primordial de la vie qui permet aux organismes vivants d'interagir avec l'environnement. En ce sens, pour être efficaces, tous les mouvements doivent être planifiés et mis à jour en fonction de la complexité et de la variabilité de l'environnement. Des chercheurs du domaine du contrôle moteur ont étudié de manière approfondie les processus de planification et d’adaptation motrice. Puisque les processus de planification et d'adaptation motrice sont influencés par la variabilité de l'environnement, le présent mémoire cherche à fournir une compréhension plus profonde de ces deux processus moteurs à cet égard. La première contribution scientifique présentée ici tire parti du fait que les temps de réaction (TR) sont réduits lorsqu'il est possible d'anticiper l’objectif moteur, afin de déterminer si les modulations de TR associées à l'anticipation spatiale et temporelle sont sous-tendues par une activité préparatoire similaire. Cela a été fait en utilisant l'électroencéphalographie (EEG) de surface pour analyser l'activité oscillatoire dans la bande de fréquence bêta (13 - 30 Hz) au cours de la période de planification du mouvement. Les résultats ont révélé que l'anticipation temporelle était associée à la désynchronisation de la bande bêta au-dessus des régions sensorimotrices controlatérales à la main effectrice, en particulier autour du moment prévu de l'apparition de la cible. L’ampleur de ces modulations était corrélée aux modulations de TR à travers les participants. En revanche, l'anticipation spatiale a augmenté de manière sélective la puissance de la bande bêta au-dessus des régions pariéto-occipitales bilatérales pendant toute la période de planification. Ces résultats suggèrent des états de préparation distinct en fonction de l’anticipation temporelle et spatiale. D’un autre côté, le deuxième projet traite de la façon dont la variabilité de la rétroaction sensorielle interfère avec la rétention à court terme dans l’étude de l’adaptation motrice. Plus précisément, une tâche d'adaptation visuomotrice a été utilisée au cours de laquelle la variance des rotations a été manipulée de manière paramétrique à travers trois groupes, et ce, tout au long de la période d’acquisition. Par la suite, la rétention de cette nouvelle relation visuomotrice a été évaluée. Les résultats ont révélé que, même si le processus d'adaptation était robuste à la manipulation de la variance, la rétention à court terme était altérée par des plus hauts niveaux de variance. Finalement, la discussion a d'abord cherché à intégrer ces deux contributions en revisitant l'interprétation des résultats sous un angle centré sur l'incertitude et en fournissant un aperçu des potentielles représentations internes de l'incertitude susceptibles de sous-tendre les résultats expérimentaux observés. Par la suite, une partie de la discussion a été réservée à la manière dont le champ du contrôle moteur migre de plus en plus vers l’utilisation de tâches et d’approches expérimentales plus complexes, mais écologiques aux dépends des tâches simples, mais quelque peu dénaturées que l’on retrouve dans les laboratoires du domaine. La discussion a été couronnée par une brève proposition allant dans ce sens.Abstract: Motor behavior is a paramount aspect of life that enables the living to interact with the environment through the production of movement. In order to be efficient, movements need to be planned and updated according to the complexity and the ever-changing nature of the environment. Motor control experts have extensively investigated the planning and adaptation processes. Since both motor planning and motor adaptation processes are influenced by variability in the environment, the present thesis seeks to provide a deeper understanding of both these motor processes in this regard. More specifically, the first scientific contribution presented herein leverages the fact that reaction times (RTs) are reduced when the anticipation of the motor goal is possible to elucidate whether the RT modulations associated with temporal and spatial anticipation are subtended by similar preparatory activity. This was done by using scalp electroencephalography (EEG) to analyze the oscillatory activity in the beta frequency band (13 – 30 Hz) during the planning period. Results revealed that temporal anticipation was associated with beta-band desynchronization over contralateral sensorimotor regions, specifically around the expected moment of target onset, the magnitude of which was correlated with RT modulations across participants. In contrast, spatial anticipation selectively increased beta-band power over bilateral parieto-occipital regions during the entire planning period, suggesting that distinct states of preparation are incurred by temporal and spatial anticipation. Additionally, the second project addressed how variance in the sensory feedback interferes with short-term retention of motor adaptation. Specifically, a visuomotor adaptation task was used during which the variance of exposed rotation was parametrically manipulated across three groups, and retention of the adapted visuomotor relationship was assessed. Results revealed that, although the adaptation process was robust to the manipulation of variance, the short-term retention was impaired. The discussion first sought to integrate these two projects by revisiting the interpretation of both projects under the scope of uncertainty and by providing an overview of the internal representation of uncertainty that might subtend the experimental results. Subsequently, a part of the discussion was reserved to allude how the motor control field is transitioning from laboratory-based tasks to more naturalistic paradigms by using approaches to move motor control research toward real-world conditions. The discussion culminates with a brief scientific proposal along those lines

Learning and adaptation in brain machine interfaces

Balancing subject learning and decoder adaptation is central to increasing brain machine interface (BMI) performance. We addressed these complementary aspects in two studies: (1) a learning study, in which mice modulated “beta” band activity to control a 1D auditory cursor, and (2) an adaptive decoding study, in which a simple recurrent artificial neural network (RNN) decoded intended saccade targets of monkeys. In the learning study, three mice successfully increased beta band power following trial initiations, and specifically increased beta burst durations from 157 ms to 182 ms, likely contributing to performance. Though the task did not explicitly require specific movements, all three mice appeared to modulate beta activity via active motor control and had consistent vibrissal motor cortex multiunit activity and local field potential relationships with contralateral whisker pad electromyograms. The increased burst durations may therefore by a direct result of increased motor activity. These findings suggest that only a subset of beta rhythm phenomenology can be volitionally modulated (e.g. the tonic “hold” beta), therefore limiting the possible set of successful beta neuromodulation strategies. In the adaptive decoding study, RNNs decoded delay period activity in oculomotor and working memory regions while monkeys performed a delayed saccade task. Adaptive decoding sessions began with brain-controlled trials using pre-trained RNN models, in contrast to static decoding sessions in which 300-500 initial eye-controlled training trials were performed. Closed loop RNN decoding performance was lower than predicted by offline simulations. More consistent delay period activity and saccade paths across trials were associated with higher decoding performance. Despite the advantage of consistency, one monkey’s delay period activity patterns changed over the first week of adaptive decoding, and the other monkey’s saccades were more erratic during adaptive decoding than during static decoding sessions. It is possible that the altered session paradigm eliminating eye-controlled training trials led to either frustration or exploratory learning, causing the neural and behavioral changes. Considering neural control and decoder adaptation of BMIs in these studies, future work should improve the “two-learner” subject-decoder system by better modeling the interaction between underlying brain states (and possibly their modulation) and the neural signatures representing desired outcomes

Adaptation to constant-magnitude assistive forces: kinematic and neural correlates

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EEG and TMS-EEG Studies on the Cortical Excitability and Plasticity associated with Human Motor Control and Learning

More than half of the activities of daily living rely on upper limb functions (Ingram et al., 2008). Humans perform upper limb movements with great ease and flexibility but even simple tasks require complex computations in the brain and can be affected following stroke leaving survivors with debilitating movement impairments. Hemispheric asymmetries related to motor dominance, imbalances between contralateral and ipsilateral primary motor cortices (M1) activity and the ability to adapt movements to novel environments play a key role in upper limb motor control and can affect recovery. Motor learning and control are critical in neurorehabilitation, however to effectively integrate these concepts into upper limb recovery treatments, a deeper understanding of the basic mechanisms of unimanual control is needed. This thesis aimed to investigate hemispheric asymmetries related to motor dominance, to evaluate the relative contribution of the contralateral and ipsilateral M1 during unilateral reaching preparation and finally to identify the neural correlates underlying the formation of a predictive internal model enabling to adapt movements to new environments. To this end electroencephalography (EEG), transcranial magnetic stimulation (TMS), simultaneous TMS-EEG were employed during a simple motor and a highly standardised robot-mediated task. The first study used TMS-EEG to examine differences in cortical excitability related to motor dominance by applying TMS over the dominant and non-dominant M1 at rest and during contraction. No hemispheric asymmetries related to hand dominance were found. The second study assessed the temporal dynamics of bi-hemispheric motor cortical excitability during right arm reaching preparation. TMS was applied either to the ipsilateral or contralateral M1 during different times of movement preparation. Significant bilateral M1 activation during unilateral reaching preparation was observed, with no significant differences between the contralateral and ipsilateral M1. Unimanual reaching preparation was associated with significant interactions of excitatory and inhibitory processes in both motor cortices. The third study investigated the neural correlates of motor adaptation. EEG was recorded during a robot-mediated adaptation task involving right arm reaching movements and cortical excitability was assessed by applying TMS over the contralateral M1 and simultaneously recording TMS responses with EEG before and after motor adaptation. It was found that an error-related negativity (ERN) over fronto-central regions correlated with performance improvements during adaptation, suggesting that this neural activity reflects the formation of a predictive internal model. Motor adaptation underlay significant modulations in cortical excitability (i.e. neuroplasticity) in sensorimotor regions. Finally, it was shown that native cortical excitability was linked to motor learning improvements during motor adaptation and explained the variability in motor learning across individuals. These experiments demonstrated that even unimanual motor control relies on interactions between excitatory and inhibitory mechanisms not only in the contralateral M1 but in a wider range of brain regions, shown by a bi-hemispheric activity during movement preparation, the formation of a predictive model in fronto-central regions during motor adaptation and neuroplastic changes in sensorimotor regions underlying motor adaptation during unimanual reaching

Failure to Engage Neural Plasticity through Practice of a High-difficulty Task is Accompanied by Reduced Motor Skill Retention in Older Adults

White the difficulty of a motor task can act as a stimulus for learning in younger adults, it is unknown how task difficulty interacts with age-related reductions in motor performance and altered brain activation. We examined the effects of task difficulty on motor performance and used electroencephalography (EEG) to probe task-related brain activation after acquisition and 24-h retention of a mirror star-tracing skill in healthy older adults (N = 36, 65-86 years). The results showed that the difficulty of the motor skill affected both the magnitude of motor skill learning and the underlying neural mechanisms. Behavioral data revealed that practicing a motor task at a high difficulty level hindered motor skill consolidation. The EEG data indicated that task difficulty modulated changes in brain activation after practice. Specifically, a decrease in task-related alpha power in frontal and parietal electrodes was only present after practice of the skill at the low and medium, but not the high difficulty level. Taken together, our findings show that a failure to engage neural plasticity through practice of a highdifficulty task is accompanied by reduced motor skill retention in older adults. The data help us better understand how older adults learn new motor skills and might have implications for prescribing motor skill practice according to its difficulty in rehabilitation settings. (c) 2020 The Author(s). Published by Elsevier Ltd on behalf of IBRO. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/)

Subjective time is predicted by local and early visual processing

Time is as pervasive as it is elusive to study, and how the brain keeps track of millisecond time is still unclear. Here we addressed the mechanisms underlying duration perception by looking for a neural signature of subjective time distortion induced by motion adaptation. We recorded electroencephalographic signals in human partici-pants while they were asked to discriminate the duration of visual stimuli after different types of translational motion adaptation. Our results show that perceived duration can be predicted by the amplitude of the N200 event-related potential evoked by the adapted stimulus. Moreover, we show that the distortion of subjective time can be predicted by the activity in the Beta band frequency spectrum, at the offset of the adaptor and during the presentation of the subsequent adapted stimulus. Both effects were observed from posterior electrodes con-tralateral to the adapted stimulus. Overall, our findings suggest that local and low-level perceptual processes are involved in generating a subjective sense of time

Behavioral/Cognitive Distinct Modulations in Sensorimotor Postmovement and Foreperiod ␤-Band Activities Related to Error Salience Processing and Sensorimotor Adaptation

International audienceIn a recent study, Tan et al. (2014a,b) showed that the increase in ␤-power typically observed after a movement above sensorimotor regions (␤-rebound) is attenuated when movement-execution errors are induced by visual perturbations. Moreover, akin to sensorimo-tor adaptation, the effect depended on the context in which the errors are experienced. Thus the ␤-rebound attenuation might relate to neural processes involved in trial-to-trial adaptive mechanisms. In two EEG experiments with human participants, along with the ␤-rebound, we examine ␤-activity during the preparation of reaches immediately following perturbed movements. In the first experiment , we show that both foreperiod and postmovement ␤-activities are parametrically modulated by the sizes of kinematic errors produced by unpredictable mechanical perturbations (force field) independent of their on-line corrections. In the second experiment, we contrast two types of reach errors: movement-execution errors that trigger trial-to-trial adaptive mechanisms and goal errors that do not elicit sensorimotor adaptation. Movement-execution errors were induced by mechanical or visual perturbations, whereas goal errors were caused by unexpected displacements of the target at movement initiation. Interestingly, foreperiod and postmovement ␤-activities exhibit contrasting patterns, pointing to important functional differences of their underlying neuronal activity. While both types of reach errors attenuate the postmovement ␤-rebound, only the kinematic errors that trigger trial-to-trial motor-command updates influenced ␤-activity during the foreperiod. These findings suggest that the error-related modulation of the ␤-rebound may reflect salience processing , independent of sensorimotor adaptation. In contrast, modulations in the foreperiod ␤-power might relate to the motor-command adjustments activated after movement-execution errors are experienced