Bimanual coordination and motor learning in children with unilateral motor disorders

Introduction Appropriate bimanual coordination is essential for many tasks in daily life. Children with unilateral cerebral palsy (uCP) however struggle with the execution of such tasks. Extensive research has been done investigating motor impairments on a functional level using standardized procedures. There is a lack of studies however looking at the specific problem of coordination of a bimanual task, especially with respect to the different underlying neuropathologies. Aims & Methods Within this thesis, kinematics of bimanual hand movement during a role differentiated bimanual box opening task in children with uCP, as well as in typically developing children (TDC) of similar ages, were investigated. The aims were: i) to identify behavioural changes in peak periods of development of the corpus callosum and areas of the prefrontal cortex, both of which are related to bimanual function in typically developing children; ii) to explore the relation between motor impairments of children with uCP and their bimanual coordination and iii) to investigate the impact of various underlying neuropathologies on bimanual coordination in children with uCP. Results For the first study, a total of 37 TDC between 5 and 16 years were included and allocated to their respective age-group: Young Children (YC: 5-6 years), Old Children (OC: 7-9 years) and Adolescents (AD: 10-16 years). The two older groups performed the task significantly faster than YC. Likewise, a trend (yet without reaching significance) towards a more ideal temporal sequencing was shown between YC and the two older groups. In contrast, spatial accuracy as expressed by the path length increased only in the AD group. For the second study, a total of 37 children with uCP between 7 and 17 years were included. Children presented manual impairments between levels I and III (according to the Manual Ability Classification System). It could be shown that task duration increased and spatial accuracy decreased with increasing levels of impairment, especially in children with higher levels of impairment (level III). Furthermore it could be shown that a subgroup of children experienced an involuntary interference when moving their affected hand, limiting the use of their less affected hand. The third study utilised a multiple case study involving nine children diagnosed with uCP with neuroimaging and neurophysiological data. The children were found to have various neuropathological patterns resulting in different forms and severities of motor impairments. It could be shown that grey-matter lesions had the most severe impact on manual abilities. Conclusion In TDC, performance of bimanual hand movements was temporally related to peak developmental periods of the corpus callosum, emphasizing the importance of interhemispheric exchange of information for bimanual coordination. In children with uCP, bimanual performance was related to the level of impairment of the affected hand. In addition it was found however that some children show excessive bimanual interference when using their affected hand in a bimanual task which limits the functionality of the less affected hand, possibly related to i) ipsilateral corticomotor projection patterns from the less affected hemisphere to the affected hand or ii) lack of suppression of interhemispheric crosstalk. It could also be shown that the various neuropathologies can affect bimanual motor control differently. Detailed diagnosis of the neuropathology and motor impairment are thus essential for the planning of tailored therapy interventions

Changes in movement control and coordination with increasing skill in females and males

In comparisons between the sexes on movement tasks, performance outcome is emphasised with little focus upon the coordination process that underpins this. Motor skills develop through practice; differences between the sexes may therefore reflect differences in the volume of experience with a task. The first study compared groups with increasing surfing experience performing a drop-landing. Sex differences in joint angle measures were accounted for at least in part by experience. Study two investigated whether females and males achieve similar improvement from an equal volume of practice using a slalom-skiing simulator task. Over five days of practice there were no differences in rate of learning for any measure. Performance differences in some cases were attributable to anthropometric differences between the sexes that interacted with the task apparatus. Most importantly, frequency for both sexes moved towards their calculated optimal, given the task constraint meaning performance was comparable. Overall males and females showed similar initial and final performance outcomes and achieved similar gains from an equal volume of practice. The basis of coordinative structure is the coupling and correlation between elements in the motor system. Principal component analysis (PCA) can quantify these relations. A recently developed technique in PCA incorporating overall coherence was applied to kinematic and EMG signals to provide further insight into the changes in coordination that occurred with practice. There were no differences between the male and female performers again supporting the idea that with equal practice, performance is similar despite any differences in anthropometrics. Whole body movement on the skiing-simulator could be defined in a low dimensional space that was further reduced over the course of practice. Previous studies had failed to show this; hidden structure was best revealed when PCA incorporating correlation in the frequency domain was employed

Dynamic primitives of motor behavior

We present in outline a theory of sensorimotor control based on dynamic primitives, which we define as attractors. To account for the broad class of human interactive behaviors—especially tool use—we propose three distinct primitives: submovements, oscillations, and mechanical impedances, the latter necessary for interaction with objects. Owing to the fundamental features of the neuromuscular system—most notably, its slow response—we argue that encoding in terms of parameterized primitives may be an essential simplification required for learning, performance, and retention of complex skills. Primitives may simultaneously and sequentially be combined to produce observable forces and motions. This may be achieved by defining a virtual trajectory composed of submovements and/or oscillations interacting with impedances. Identifying primitives requires care: in principle, overlapping submovements would be sufficient to compose all observed movements but biological evidence shows that oscillations are a distinct primitive. Conversely, we suggest that kinematic synergies, frequently discussed as primitives of complex actions, may be an emergent consequence of neuromuscular impedance. To illustrate how these dynamic primitives may account for complex actions, we brieflyreviewthree typesof interactivebehaviors: constrained motion, impact tasks, and manipulation of dynamic objects.United States. National Institutes of Health (T32GM008334)American Heart Association (11SDG7270001)National Science Foundation (U.S.) (NSF DMS-0928587

The development of coordination for reaching movement in children

Mémoire numérisé par la Direction des bibliothèques de l'Université de Montréal

Neurophysiological mechanisms of sensorimotor recovery from stroke

Ischemic stroke often results in the devastating loss of nervous tissue in the cerebral cortex, leading to profound motor deficits when motor territory is lost, and ultimately resulting in a substantial reduction in quality of life for the stroke survivor. The International Classification of Functioning, Disability and Health (ICF) was developed in 2002 by the World Health Organization (WHO) and provides a framework for clinically defining impairment after stroke. While the reduction of burdens due to neurological disease is stated as a mission objective of the National Institute of Neurological Disorders and Stroke (NINDS), recent clinical trials have been unsuccessful in translating preclinical research breakthroughs into actionable therapeutic treatment strategies with meaningful progress towards this goal. This means that research expanding another NINDS mission is now more important than ever: improving fundamental knowledge about the brain and nervous system in order to illuminate the way forward. Past work in the monkey model of ischemic stroke has suggested there may be a relationship between motor improvements after injury and the ability of the animal to reintegrate sensory and motor information during behavior. This relationship may be subserved by sprouting cortical axonal processes that originate in the spared premotor cortex after motor cortical injury in squirrel monkeys. The axons were observed to grow for relatively long distances (millimeters), significantly changing direction so that it appears that they specifically navigate around the injury site and reorient toward the spared sensory cortex. Critically, it remains unknown whether such processes ever form functional synapses, and if they do, whether such synapses perform meaningful calculations or other functions during behavior. The intent of this dissertation was to study this phenomenon in both intact rats and rats with a focal ischemia in primary motor cortex (M1) contralateral to the preferred forelimb during a pellet retrieval task. As this proved to be a challenging and resource-intensive endeavor, a primary objective of the dissertation became to provide the tools to facilitate such a project to begin with. This includes the creation of software, hardware, and novel training and behavioral paradigms for the rat model. At the same time, analysis of previous experimental data suggested that plasticity in the neural activity of the bilateral motor cortices of rats performing pellet retrievals after focal M1 ischemia may exhibit its most salient changes with respect to functional changes in behavior via mechanisms that were different than initially hypothesized. Specifically, a major finding of this dissertation is the finding that evidence of plasticity in the unit activity of bilateral motor cortical areas of the reaching rat is much stronger at the level of population features. These features exhibit changes in dynamics that suggest a shift in network fixed points, which may relate to the stability of filtering performed during behavior. It is therefore predicted that in order to define recovery by comparison to restitution, a specific type of fixed point dynamics must be present in the cortical population state. A final suggestion is that the stability or presence of these dynamics is related to the reintegration of sensory information to the cortex, which may relate to the positive impact of physical therapy during rehabilitation in the postacute window. Although many more rats will be needed to state any of these findings as a definitive fact, this line of inquiry appears to be productive for identifying targets related to sensorimotor integration which may enhance the efficacy of future therapeutic strategies

Dynamic Sensorimotor Planning during Long-Term Sequence Learning: The Role of Variability, Response Chunking and Planning Errors

Many everyday skills are learned by binding otherwise independent actions into a unified sequence of responses across days or weeks of practice. Here we looked at how the dynamics of action planning and response binding change across such long timescales. Subjects (N = 23) were trained on a bimanual version of the serial reaction time task (32-item sequence) for two weeks (10 days total). Response times and accuracy both showed improvement with time, but appeared to be learned at different rates. Changes in response speed across training were associated with dynamic changes in response time variability, with faster learners expanding their variability during the early training days and then contracting response variability late in training. Using a novel measure of response chunking, we found that individual responses became temporally correlated across trials and asymptoted to set sizes of approximately 7 bound responses at the end of the first week of training. Finally, we used a state-space model of the response planning process to look at how predictive (i.e., response anticipation) and error-corrective (i.e., post-error slowing) processes correlated with learning rates for speed, accuracy and chunking. This analysis yielded non-monotonic association patterns between the state-space model parameters and learning rates, suggesting that different parts of the response planning process are relevant at different stages of long-term learning. These findings highlight the dynamic modulation of response speed, variability, accuracy and chunking as multiple movements become bound together into a larger set of responses during sequence learning. © 2012 Verstynen et al

Network mechanisms underlying stable motor actions

While we can learn to produce stereotyped movements and maintain this ability for years, it is unclear how populations of individual neurons change their firing properties to coordinate these skills. This has been difficult to address because there is a lack of tools that can monitor populations of single neurons in freely behaving animals for the durations required to remark on their tuning. This thesis is divided into two main directions- device engineering and systems neuroscience. The first section describes the development of an electrode array comprised of tiny self-splaying carbon fibers that are small and flexible enough to avoid the immune response that typically limits electrophysiological recordings. I also describe the refinement of a head-mounted miniature microscope system, optimized for multi-month monitoring of cells expressing genetically encoded calcium indicators in freely behaving animals. In the second section, these tools are used to answer basic systems neuroscience questions in an animal with one of the most stable, complex learned behaviors in the animal kingdom: songbirds. This section explores the functional organization and long-term network stability of HVC, the songbird premotor cortical microcircuit that controls song. Our results reveal that neural activity in HVC is correlated with a length scale of 100um. At this mesocopic scale, basal-ganglia projecting excitatory neurons, on average, fire at a specific phase of a local 30Hz network rhythm. These results show that premotor cortical activity is inhomogeneous in time and space, and that a mesoscopic dynamical pattern underlies the generation of the neural sequences controlling song. At this mesoscopic level, neural coding is stable for weeks and months. These ensemble patterns persist after peripheral nerve damage, revealing that sensory-motor correspondence is not required to maintain the stability of the underlying neural ensemble. However, closer examination of individual excitatory neurons reveals that the participation of cells can change over the timescale of days- with particularly large shifts occurring over instances of sleep. Our findings suggest that fine-scale drift of projection neurons, stabilized by mesoscopic level dynamics dominated by inhibition, forms the mechanistic basis of memory maintenance and and motor stability

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

Resting-state functional connectivity predicts the ability to adapt to robot-mediated force fields

Motor deficits are common outcomes of neurological conditions such as stroke. In order to design personalised motor rehabilitation programmes such as robot-assisted therapy, it would be advantageous to predict how a patient might respond to such treatment. Spontaneous neural activity has been observed to predict differences in the ability to learn a new motor behaviour in both healthy and stroke populations. This study investigated whether spontaneous resting-state functional connectivity could predict the degree of motor adaptation of right (dominant) upper limb reaching in response to a robot-mediated force field. Spontaneous neural activity was measured using resting-state electroencephalography (EEG) in healthy adults before a single session of motor adaptation. The degree of beta frequency (β; 15–25 Hz) resting-state functional connectivity between contralateral electrodes overlying the left primary motor cortex (M1) and the anterior prefrontal cortex (aPFC) could predict the subsequent degree of motor adaptation. This result provides novel evidence for the functional significance of resting-state synchronization dynamics in predicting the degree of motor adaptation in a healthy sample. This study constitutes a promising first step towards the identification of patients who will likely gain most from using robot-mediated upper limb rehabilitation training based on simple measures of spontaneous neural activity