Transient alpha and beta synchrony underlies preparatory recruitment of directional motor networks

Modulations in motor cortical beta and alpha activity have been implicated in the preparation, execution, and termination of voluntary movements. The functional role of motor cortex beta activity is yet to be defined, though two opposing theories prevail. The idling cortex theory suggests that large-scale motor networks, in the absence of input, revert to an intrinsic oscillatory state. The alternative theory proposes that beta activity promotes postural tone at the expense of voluntary movement. These theories are primarily based on observations of event-related desynchronization associated with movement onset. Here, we explore the changes in alpha and beta oscillatory activity associated with the specific behavioral patterns during an established directional uncertainty paradigm. We demonstrate that, consistent with current proposals, alpha and beta desynchronization reflects a process of disengagement from existing networks to enable the creation of functional assemblies. We demonstrate that, following desynchronization, a novel signature of transient alpha synchrony underlies the recruitment of functional assemblies required for directional control. Although alpha and beta desynchronization are dependent upon the number of cues presented, they are not predictive of movement preparation. However, the transient alpha synchrony occurs only when participants have sufficient information to prepare for movement and shows a direct relationship with behavioral performance measures. </jats:p

Neuronal Network Oscillations in the Control of Human Movement

The overarching aim of this thesis was to use neuroimaging and neuromodulation techniques to further understand the relationship between cortical oscillatory activity and the control of human movement. Modulations in motor cortical beta and alpha activity have been consistently implicated in the preparation, execution, and termination of movement. Here, I describe the outcome of four studies designed to further elucidate these motor-related changes in oscillatory activity. In Chapter 3, I report the findings of a study that used an established behavioural paradigm to vary the degree of uncertainty during the preparation of movement. I demonstrate that preparatory alpha and beta desynchronisation reflect a process of disengagement from the existing network to enable the creation of functional assemblies required for movement. Importantly, I also demonstrate a novel neural signature of transient alpha synchrony, that occurs after preparatory desynchronisation, that underlies the recruitment of functional assemblies required for directional control. The study described in Chapter 4 was designed to further investigate the functional role of preparatory alpha and beta desynchronisation by entraining oscillatory activity in the primary motor cortex (M1) using frequency-specific transcranial alternating current stimulation. No significant effects of stimulation were found on participant response times. However, no clear conclusion could be drawn due to limitations of the stimulation parameters that were used. In Chapter 5, I explored the inverse relationship between M1 beta power and cortical excitability using single-pulse transcranial magnetic stimulation to elicit motor-evoked potentials (MEPs). The amplitude of MEPs collected during a period of beta desynchronisation was significantly greater than during a resting baseline. Conversely, the amplitude of MEPs collected during the post-movement beta rebound that follows the termination of a movement was significantly reduced compared to baseline. This finding confirms the inverse relationship between M1 beta power and cortical excitability. The study in Chapter 6 explored the effect of experimental context on M1 beta power. When the participant was cued to expect an upcoming motor task, resting beta power was significantly increased, then when the likelihood of an upcoming motor requirement decreased, there was a significant concurrent decrease in resting beta power. This reflects increased coherence and functional connectivity within M1 and other motor areas, to ‘recalibrate’ the motor system in preparation for a synchronous input signal to more readily recruit the required functional assembly

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

Role of Anterior Cingulate Cortex in Saccade Control

Cognitive control is referred to the guidance of behavior based on internal goals rather than external stimuli. It has been postulated that prefrontal cortex is mainly involved in higher order cognitive functions. Specifically, anterior cingulate cortex (ACC), which is part of the prefrontal cortex, is suggested to be involved in performance monitoring and conflict monitoring that are considered to be cognitive control functions. Saccades are the fast eye movements that align the fovea on the objects of interest in the environment. In this thesis, I have explored the role of ACC in control of saccadic eye movements. First, I performed a resting-state fMRI study to identify areas within the ACC that are functionally connected to the frontal eye fields (FEF). It has been shown that FEF is involved in saccade generation. Therefore, the ACC areas that are functionally connected to FEF could be hypothesized to have a role in saccade control. Then, I performed simultaneous electrophysiological recordings in the ACC and FEF. Furthermore, I explored whether ACC exerts control over FEF. My results show that ACC is involved in cognitive control of saccades. Furthermore, the ACC and FEF neurons communicate through synchronized theta and beta band activity in these areas. The results of this thesis shine light on the mechanisms by which these brain areas communicate. Moreover, my findings support the notion that ACC and FEF have a unique oscillatory property, and more specifically ACC has a prominent theta band, and to a lesser extent beta band activity

Neural correlates of motor imagery and execution in real-world dynamic behavior : evidence for similarities and differences

This work was supported by a scholarship from the University of Stirling and a research grant from SINAPSE (Scottish Imaging Network: A Platform for Scientific excellence).A large body of evidence shows that motor imagery and action execution behaviours result from overlapping neural substrates, even in the absence of overt movement during motor imagery. To date it is unclear how neural activations in motor imagery and execution compare for naturalistic whole-body movements, such as walking. Neuroimaging studies have not directly compared imagery and execution during dynamic walking movements. Here we recorded brain activation with mobile EEG during walking compared to during imagery of walking, with mental counting as a control condition. We asked twenty-four healthy participants to either walk six steps on a path, imagine taking six steps or mentally count from one to six. We found beta and alpha power modulation during motor imagery resembling action execution patterns; a correspondence not found performing the control task of mentally counting. Neural overlap occurred early in the execution and imagery walking actions, suggesting activation of shared action representations.Remarkably, a distinctive walking-related beta rebound occurred both during action execution and imagery at the end of the action suggesting that, like actual walking, motor imagery involves resetting or inhibition of motor processes. However, we also found that motor imagery elicits a distinct pattern of more distributed beta activity especially at the beginning of the task. These results indicate that motor imagery and execution of naturalistic walking involve shared motorcognitive activations, but that motor imagery requires additional cortical resources.Peer reviewe

THE INFLUENCE OF CONSCIOUS CONTROL OF MOVEMENT ON BRAIN PROCESSES AND THE QUALITY OF COGNITIVE-MOTOR PERFORMANCE

The impact of mental stress on fine motor performance is typically maladaptive. The current research was conducted to investigate the manner by which state anxiety affects performance using a cognitive neuroscience perspective. The basic proposition tested, derived from the Reinvestment Theory and the Psychomotor Efficiency Hypothesis, is that stress introduces neuromotor noise to motor planning processes that translate as excess recruitment of motor units and degrade performance. Electroencephalography (EEG) was employed in Study 1 to assess regional cortical activation and cortico-cortical communication between non-motor associative and motor planning regions during the preparatory period of a dart-throwing task. The task was performed during stress (i.e., social evaluation, monetary incentives, and threat of electrical shock) and a relatively relaxed control condition through a within-subjects design. Regional activation was estimated from bilateral EEG recordings in the frontal, central, temporal, parietal, and occipital regions via spectral analysis to assess low-alpha and high-alpha band power to determine generalized arousal and task-relevant attentional focus, respectively. Cortico-cortical communication was estimated between all bilateral regions and the frontal motor planning area with particular emphasis on the left temporal (T3) to midline frontal (Fz) coherence. Elevated state anxiety was induced and associated with heightened T3-Fz EEG connectivity and synchrony of high-alpha band in the right occipital region. Based on these findings, Study 2 was conducted to determine the psychological processes accounting for the observed elevation in T3-Fz EEG coherence and the quality of muscle action during the throwing task. Specifically, participants employed an internal and an external attentional focus to perform the throwing task while their EEG and electromyography (EMG) were monitored. The use of internal focus, which is consistent with explicit monitoring of movement mechanics, was predicted to result in elevated T3-Fz EEG connectivity. This prediction was supported and, furthermore, the magnitude of connectivity was positively associated with motor unit activity assessed via EMG of four major muscle groups (i.e., flexor carpi ulnaris, extensor carpi radialis, biceps brachii, and triceps brachii). The evidence provided supports the theoretical notion that explicit monitoring promotes inefficient muscle activity, which mediates to impact performance negatively

Evaluating motor cortical oscillations and age-related change in autism spectrum disorder

Autism spectrum disorder (ASD) is primarily characterized by impairments in social communication and the appearance of repetitive behaviors with restricted interests. Increasingly, evidence also points to a general deficit of motor tone and coordination in children and adults with ASD; yet the neural basis of motor functional impairment in ASD remains poorly characterized. In this study we used magnetoencephalography (MEG) to (1) assess potential group differences between typically developing (TD) and ASD participants in motor cortical oscillatory activity observed on a simple button-press task and (2) to do so over a sufficiently broad age-range so as to capture age-dependent changes associated with development. Event-related desynchronization was evaluated in Mu (8-13 Hz) and Beta (15-30 Hz) frequency bands (Mu-ERD, Beta-ERD). In addition, post-movement Beta rebound (PMBR), and movement-related gamma (60-90 Hz) synchrony (MRGS) were also assessed in a cohort of 123 participants (63 typically developing (TD) and 59 with ASD) ranging in age from 8 to 24.9 years. We observed significant age-dependent linear trends in Beta-ERD and MRGS power with age for both TD and ASD groups; which did not differ significantly between groups. However, for PMBR, in addition to a significant effect of age, we also observed a significant reduction in PMBR power in the ASD group (p 13.2 years (p < 0.001) and this group difference was not observed when assessing PMBR activity for the younger PMBR groups (ages 8-13.2 years; p = 0.48). Moreover, for the older ASD cohort, hierarchical regression showed a significant relationship between PMBR activity and clinical scores of ASD severity (SRS-T scores), after regressing out the effect of age (p < 0.05). Our results show substantial age-dependent changes in motor cortical oscillations (Beta-ERD and MRGS) occur for both TD and ASD children and diverge only for PMBR, and most significantly for older adolescents and adults with ASD. While the functional significance of PMBR and reduced PMBR signaling remains to be fully elucidated, these results underscore the importance of considering age as a factor when assessing motor cortical oscillations and group differences in children with ASD

Individual variation in EEG spectral power enhancement and intelligence

This study tested the relationship between short-term neuroplasticity and individual differences in intelligence. Twenty-two participants completed cognitive testing and a visual EEG experiment involving exposures to repeated and novel stimuli. Time-frequency analyses of phase-locked (evoked) and non-phase-locked (induced) power showed a small effect of decreasing evoked/induced theta (4-8 Hz) ratios over stimulus exposures, irrespective of condition. Hypotheses that intelligence would relate to an increase in this ratio over exposures were not supported. However, the magnitude of the ratio positively correlated with intelligence; while the amount of induced gamma (30-50Hz) activation pre- to post-stimulus was highly inversely related to g. Results suggest that transient changes in neural network phase strongly relate to intelligence in physiological measurements acquired over brief intervals