Neural synchrony within the motor system: what have we learned so far?

Synchronization of neural activity is considered essential for information processing in the nervous system. Both local and inter-regional synchronization are omnipresent in different frequency regimes and relate to a variety of behavioral and cognitive functions. Over the years, many studies have sought to elucidate the question how alpha/mu, beta, and gamma synchronization contribute to motor control. Here, we review these studies with the purpose to delineate what they have added to our understanding of the neural control of movement. We highlight important findings regarding oscillations in primary motor cortex, synchronization between cortex and spinal cord, synchronization between cortical regions, as well as abnormal synchronization patterns in a selection of motor dysfunctions. The interpretation of synchronization patterns benefits from combining results of invasive and non-invasive recordings, different data analysis tools, and modeling work. Importantly, although synchronization is deemed to play a vital role, it is not the only mechanism for neural communication. Spike timing and rate coding act together during motor control and should therefore both be accounted for when interpreting movement-related activity

Исследование электрической активности мозга, связанной с движениями: обзор

Робота присвячена розгляду проблем, що виникають при дослідженні діяльності мозку, пов'язаної з рухами. Зміни в корі головного мозку під час виконання руху, а також його уявлення, відображають нейронні мережі, сформовані для планування і реалізації конкретного руху. Наведено огляд методів первинної обробки зареєстрованої активності головного мозку, які можуть бути використані для підвищення значимості виділених ознак. Описано закономірності, які мають місце до початку руху і після нього. Представлені методи, які підходять для оцінки зв'язку як між активністю мозку і активністю м'язів, так і між активністю областей головного мозку. Крім того, розглянута можливість класифікації та прогнозування рухів разом з реконструкцією кінематичних властивостей.The work is devoted to consideration of different problems which arise in studying of the movement-related brain activity. Changes in the cortex activity during performing of the movement both real and imagery represent neural networks formed for planning and performing of the particular motion. The review of possible preprocessing methods of the registered brain activity for increasing significance of extracted features are shown. Regularities and patterns which take place before and after movement onset are described. The methods that suitable for connectivity estimations in case of cortico-muscular relationships and in case of evaluations between brain regions are shown. In addition, possibility of movement classification and prediction together with reconstruction of kinematics features of the motion are considered.Работа посвящена рассмотрению проблем, возникающих при изучении деятельности мозга, связанной с движениями. Изменения в коре головного мозга во время выполнения движения, а также его представления, отображают нейронные сети, сформированные для планирования и реализации конкретного движения. Приведен обзор методов первичной обработки зарегистрированной активности головного мозга, которые могут быть использованы для повышения значимости выделенных признаков. Описаны закономерности, которые имеют место до начала движения и после него. Представлены методы, подходящие для оценки связи как между активностью мозга и активностью мышц, так и между активностью областей головного мозга. Кроме того, рассмотрена возможность классификации и прогнозирования движений вместе с реконструкцией кинематических свойств

Neurobehavioral Strategies of Skill Acquisition in Left and Right Hand Dominant Individuals

The brain consists of vast networks of connected pathways communicating through synchronized electrochemical activity propagated along fiber tracts. The current understanding is that the brain has a modular organization where regions of specialized processes are dynamically coupled through long-range projections of dense axonal networks connecting spatially distinct regions enabling signal transfer necessary for all complex thought and behavior, including regulation of movement. The central objective of the dissertation was to understand how sensorimotor information is integrated, allowing for adaptable motor behavior and skill acquisition in the left-and right-hand dominant populations. To this end participants, of both left- and right-hand dominance, repeatedly completed a visually guided, force matching task while neurobiological and neurobehavioral outcome measurements were continuously recorded via EEG and EMG. Functional connectivity and graph theoretical measurements were derived from EEG. Cortico-cortical coherence patterns were used to infer neurostrategic discrepancies employed in the execution of a motor task for each population. EEG activity was also correlated with neuromuscular activity from EMG to calculate cortico-muscular connectivity. Neurological patterns and corresponding behavioral changes were used to express how hand dominance influenced the developing motor plan, thereby increasing understanding of the sensorimotor integration process. The cumulative findings indicated fundamental differences in how left- and right-hand dominant populations interact with the world. The right-hand dominant group was found to rely on visual information to inform motor behavior where the left-hand dominant group used visual information to update motor behavior. The left-hand group was found to have a more versatile motor plan, adaptable to both dominant, nondominant, and bimanual tasks. Compared to the right-hand group it might be said that they were more successful in encoding the task, however behaviorally they performed the same. The implications of the findings are relevant to both clinical and performance applications providing insight as to potential alternative methods of information integration. The inclusion of the left-hand dominant population in the growing conceptualization of the brain will generate a more complete, stable, and accurate understanding of our complex biology

Lateralised dynamic modulations of corticomuscular coherence associated with bimanual learning of rhythmic patterns

Supplementary Information: The online version contains supplementary material available at https://doi.org/ 10.1038/s41598-022-10342-5Human movements are spontaneously attracted to auditory rhythms, triggering an automatic activation of the motor system, a central phenomenon to music perception and production. Cortico- muscular coherence (CMC) in the theta, alpha, beta and gamma frequencies has been used as an index of the synchronisation between cortical motor regions and the muscles. Here we investigated how learning to produce a bimanual rhythmic pattern composed of low- and high-pitch sounds affects CMC in the beta frequency band. Electroencephalography (EEG) and electromyography (EMG) from the left and right First Dorsal Interosseus and Flexor Digitorum Superficialis muscles were concurrently recorded during constant pressure on a force sensor held between the thumb and index finger while listening to the rhythmic pattern before and after a bimanual training session. During the training, participants learnt to produce the rhythmic pattern guided by visual cues by pressing the force sensors with their left or right hand to produce the low- and high-pitch sounds, respectively. Results revealed no changes after training in overall beta CMC or beta oscillation amplitude, nor in the correlation between the left and right sides for EEG and EMG separately. However, correlation analyses indicated that left- and right-hand beta EEG–EMG coherence were positively correlated over time before training but became uncorrelated after training. This suggests that learning to bimanually produce a rhythmic musical pattern reinforces lateralised and segregated cortico-muscular communication.This work was supported by a grant from the Australian Research Council (DP170104322)

Translating novel findings of perceptual-motor codes into the neuro-rehabilitation of movement disorders

The bidirectional flow of perceptual and motor information has recently proven useful as rehabilitative tool for re-building motor memories. We analyzed how the visual-motor approach has been successfully applied in neurorehabilitation, leading to surprisingly rapid and effective improvements in action execution. We proposed that the contribution of multiple sensory channels during treatment enables individuals to predict and optimize motor behavior, having a greater effect than visual input alone. We explored how the state-of-the-art neuroscience techniques show direct evidence that employment of visual-motor approach leads to increased motor cortex excitability and synaptic and cortical map plasticity. This super-additive response to multimodal stimulation may maximize neural plasticity, potentiating the effect of conventional treatment, and will be a valuable approach when it comes to advances in innovative methodologies

Investigating the Cortical, Metabolic and Behavioral Effects of Transcranial Direct Current Stimulation in Preparation for Combined Rehabilitation

The goal of this thesis was to determine the cortical reorganization that occurs in patients with cervical spondylotic myelopathy (CSM) after surgical decompression and to implement this knowledge into a new rehabilitation strategy. Transcranial direct current stimulation (tDCS) is a non-invasive technique to modulate human behavior. Due to the novel electrode montage used, it was first pertinent that we determine how tDCS would modulate cortical, metabolic and motor behavior in healthy individuals. We observed the longitudinal functional adaptations that occur in patients with CSM using functional MRI. Enhanced excitation of supplementary motor area (SMA) was observed following surgical decompression and associated with increased function following surgery. This novel finding of enhanced excitation of motivated us to use a bihemispheric tDCS protocol, exciting bilateral motor areas to provide optimal motor enhancement. This novel tDCS electrode montage, targeting the SMA and primary motor cortex (M1) was implemented in healthy older adults to determine its effects on enhancing manual dexterity. Furthermore, to determine the frequency with which to apply tDCS, a single and tri session protocol was used. We observed a differential pattern of action with anti-phase and in-phase motor tasks during multisession tDCS. We used ultra-high field (7T) MRI to examined the metabolic changes that occur following tDCS. After the stimulation period we observed no significant metabolite modulation. A trend towards an increase in the NAA/tCr ratio, with a concomitant decrease in the absolute concentration of tCr was observed. Finally, we examined the functional connectivity before, during and after tDCS with the use of resting-state fMRI at 7T. We observed enhanced connectivity within right sensorimotor area after stimulation compared to during stimulation. This result confirmed that cortical modulations differ during versus after tDCS, signifying that optimal modulation of behaviour may be after the stimulation period. Furthermore, we observed an enhanced correlation between motor regions and the caudate, both during and after stimulation. In conclusion, we observed novel cortical adaptations in CSM patients after surgical decompression, which led us to believe that bihemispheric tDCS of M1-SMA network would result in optimal motor enhancement and warrants further investigation in CSM and other neurological disorders

Neural dynamics of human motor control

Beek, P.J. [Promotor]Daffertshofer, A. [Copromotor

Cortico-muscular coherence in sensorimotor synchronisation

This thesis sets out to investigate the neuro-muscular control mechanisms underlying the ubiquitous phenomenon of sensorimotor synchronisation (SMS). SMS is the coordination of movement to external rhythms, and is commonly observed in everyday life. A large body of research addresses the processes underlying SMS at the levels of behaviour and brain. Comparatively, little is known about the coupling between neural and behavioural processes, i.e. neuro-muscular processes. Here, the neuro-muscular processes underlying SMS were investigated in the form of cortico-muscular coherence measured based on Electroencephalography (EEG) and Electromyography (EMG) recorded in human healthy participants. These neuro-muscular processes were investigated at three levels of engagement: passive listening and observation of rhythms in the environment, imagined SMS, and executed SMS, which resulted in the testing of three hypotheses: (i) Rhythms in the environment, such as music, spontaneously modulate cortico-muscular coupling, (ii) Movement intention modulates cortico-muscular coupling, and (iii) Cortico-muscular coupling is dynamically modulated during SMS time-locked to the stimulus rhythm. These three hypotheses were tested through two studies that used Electroencephalography (EEG) and Electromyography (EMG) recordings to measure Cortico-muscular coherence (CMC). First, CMC was tested during passive music listening, to test whether temporal and spectral properties of music stimuli known to induce groove, i.e., the subjective experience of wanting to move, can spontaneously modulate the overall strength of the communication between the brain and the muscles. Second, imagined and executed movement synchronisation was used to investigate the role of movement intention and dynamics on CMC. The two studies indicate that both top-down, and somatosensory and/or proprioceptive processes modulate CMC during SMS tasks. Although CMC dynamics might be linked to movement dynamics, no direct correlation between movement performance and CMC was found. Furthermore, purely passive auditory or visual rhythmic stimulation did not affect CMC. Together, these findings thus indicate that movement intention and active engagement with rhythms in the environment might be critical in modulating CMC. Further investigations of the mechanisms and function of CMC are necessary, as they could have important implications for clinical and elderly populations, as well as athletes, where optimisation of motor control is necessary to compensate for impaired movement or to achieve elite performance

State-dependent modulation of cortico-spinal networks

Beta-band rhythm (13-30 Hz) is a dominant oscillatory activity in the sensorimotor system. Numerous studies reported on links between motor performance and the cortical and cortico-spinal beta rhythm. However, these studies report divergent beta-band frequencies and are, additionally, based on differently performed motor-tasks (e.g., motor imagination, muscle contraction, reach, grasp, and attention). This diversity blurs the role of beta in the sensorimotor system. It consequently challenges the development of beta-band activity-dependent stimulation protocols in the sensorimotor system. In this vein, we studied the functional role of beta-band cortico-cortical and cortico-spinal networks during a motor learning task. We studied how the contribution of cortical and spinal beta changes in the course of learning, and how this modulation is affected by afferent feedback to the sensorimotor system. We furthermore researched the relationship to motor performance. Consider that we made our study in the absence of any residual movement to allow our findings to be translated into rehabilitation programs for severely affected stroke patients. This thesis, at first, investigates evoked responses after transcranial magnetic stimulation (TMS). This revealed two different beta-band networks, i.e., in the low and high beta-band reflecting cortical and cortico-spinal activity. We, then, used a broader frequency range in the beta-band to trigger passive opening of the hand (peripheral feedback) or cortical stimulation (cortical feedback). While a unilateral hemispheric increase in cortico-spinal synchronization was observed in the group with peripheral feedback, a bilateral hemispheric increase in cortico-cortical and cortico-spinal synchronization was observed for the group with cortical feedback. An improvement in motor performance was found in the peripheral group only. Additionally, an enhancement in the directed cortico-spinal synchronization from cortex to periphery was observed for the peripheral group. Similar neurophysiological and behavioral changes were observed for stroke patients receiving peripheral feedback. The results 6 suggest two different mechanisms for beta-band activity-dependent protocols depending on the feedback modality. While the peripheral feedback appears to increase the synchronization among neural groups, cortical stimulation appears to recruit dormant neurons and to extend the involved motor network. These findings may provide insights regarding the mechanism behind novel activity-dependent protocols. It also highlights the importance of afferent feedback for motor restoration in beta-band activity-dependent rehabilitation programs