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

Neural and motor basis of inter-individual interactions

The goal of my Ph.D. work was to investigate the behavioral markers and the brain activities responsible for the emergence of sensorimotor communication. Sensorimotor communication can be defined as a form of communication consisting into flexible exchanges based on bodily signals, in order to increase the efficiency of the inter-individual coordination. For instance, a soccer player carving his movements to inform another player about his intention. This form of interaction is highly dependent of the motor system and the ability to produce appropriate movements but also of the ability of the partner to decode these cues. To tackle these facets of human social interaction, we approached the complexity of the problem by splitting my research activities into two separate lines of research. First, we pursued the examination of motor-based humans\u2019 capability to perceive and \u201cread\u201d other\u2019s behaviors in focusing on single-subject experiment. The discovery of mirror neurons in monkey premotor cortex in the early nineties (di Pellegrino et al. 1992) motivated a number of human studies on this topic (Rizzolatti and Craighero 2004). The critical finding was that some ventral premotor neurons are engaged during visual presentation of actions performed by conspecifics. More importantly, those neurons were shown to encode also the actual execution of similar actions (i.e. irrespective of who the acting individual is). This phenomenon has been highly investigated in humans by using cortical and cortico-spinal measures (for review see, fMRI: Molenberghs, Cunnington, and Mattingley 2012; TMS: Naish et al. 2014; EEG: Pineda 2008). During single pulse TMS (over the primary motor cortex), the amplitude of motor evoked potentials (MEPs) provides an index of corticospinal recruitment. During action observation the modulation of this index follow the expected changes during action execution (Fadiga et al. 1995). However, dozens of studies have been published on this topic and revealed important inconsistencies. For instance, MEPs has been shown to be dependent on observed low-level motor features (e.g. kinematic features or electromyography temporal coupling; Gangitano, Mottaghy, and Pascual-Leone 2001; Borroni et al. 2005; Cavallo et al. 2012) as well as high level movement properties (e.g. action goals; Cattaneo et al. 2009; Cattaneo et al. 2013). Furthermore, MEPs modulations do not seem to be related to the observed effectors (Borroni and Baldissera 2008; Finisguerra et al. 2015; Senna, Bolognini, and Maravita 2014), suggesting their independence from low-level movement features. These contradictions call for new paradigms. Our starting hypothesis here is that the organization and function of the mirror mechanism should follow that of the motor system during action execution. Hence, we derived three action observation protocols from classical motor control theories: 1) The first study was motivated by the fact that motor redundancy in action execution do not allow the presence of a one-to-one mapping between (single) muscle activation and action goals. Based on that, we showed that the effect of action observation (observation of an actor performing a power versus a precision grasp) are variable at the single muscle level (MEPs; motor evoked potentials) but robust when evaluating the kinematic of TMS-evoked movements. Considering that movements are based on the coordination of multiple muscle activations (muscular synergies), MEPs may represent a partial picture of the real corticospinal activation. Inversely, movement kinematics is both the final functional byproduct of muscles coordination and the sole visual feedback that can be extracted from action observation (i.e. muscle recruitment is not visible). We conclude that TMS-evoked kinematics may be more reliable in representing the state of the motor system during action observation. 2) In the second study, we exploited the inter-subject variability inherent to everyday whole-body human actions, to evaluate the link between individual motor signatures (or motor styles) and other\u2019s action perception. We showed no group-level effect but a robust correlation between the individual motor signature recorded during action execution and the subsequent modulations of corticospinal excitability during action observation. However, results were at odds with a strict version of the direct matching hypothesis that would suggest the opposite pattern. In fact, the more the actor\u2019s movement was similar to the observer\u2019s individual motor signature, the smaller was the MEPs amplitude, and vice versa. These results conform to the predictive coding hypothesis, suggesting that during AO, the motor system compares our own way of doing the action (individual motor signature) with the action displayed on the screen (actor\u2019s movement). 3) In the third study, we investigated the neural mechanisms underlying the visual perception of action mistakes. According to a strict version of the direct matching hypothesis, the observer should potentially reproduce the neural activation present during the actual execution of action errors (van Schie et al. 2004). Here, instead of observing an increase of cortical inhibition, we showed an early (120 ms) decrease of intracortical inhibition (short intracortical inhibition) when a mismatch was present between the observed action (erroneous) and the observer\u2019s expectation. As proposed by the predictive coding framework, the motor system may be involved in the generation of an error signal potentially relying on an early decrease of intracortical inhibition within the corticomotor system. The second line of research aimed at the investigation of how sensorimotor communication flows between agents engaged in a complementary action coordination task. In this regard, measures of interest where related to muscle activity and/or kinematics as the recording of TMS-related indexes would be too complicated in a joint-action scenario. 1) In the first study, we exploited the known phenomenon of Anticipatory Postural Adjustments (APAs). APAs refers to postural adjustments made in anticipation of a self- or externally-generated disturbance in order to cope for the predicted perturbation and stabilize the current posture. Here we examined how observing someone else lifting an object we hold can affect our own anticipatory postural adjustments of the arm. We showed that the visual information alone (joint action condition), in the absence of efference copy (present only when the subject is unloading by himself the object situated on his hand), were not sufficient to fully deploy the needed anticipatory muscular activations. Rather, action observation elicited a dampened APA response that is later augmented by the arrival of tactile congruent feedback. 2) In a second study, we recorded the kinematic of orchestra musicians (one conductor and two lines of violinists). A manipulation was added to perturb the normal flow of information conveyed by the visual channel. The first line of violinist where rotated 180\ub0, and thus faced the second line. Several techniques were used to extract inter-group (Granger Causality method) and intra-group synchronization (PCA for musicians and autoregression for conductors). The analyses were directed to two kinematic features, hand and head movements, which are central for functionally different action. The hand is essential for instrumental actions, whereas head movements encode ancillary expressive actions. During the perturbation, we observed a complete reshaping of the whole patterns of communication going in the direction of a distribution of the leadership between conductor and violinists, especially for what regards head movements. In fact, in the perturbed condition, the second line acts as an informational hub connecting the first line to the conductor they no longer can see. This study evidences different forms of communications (coordination versus synchronization) flowing via different channels (ancillary versus instrumental) with different time-scales

Older adults exhibit a more pronounced modulation of beta oscillations when performing sustained and dynamic handgrips

Muscle contractions are associated with a decrease in beta oscillatory activity, known as movement-related beta desynchronization (MRBD). Older adults exhibit a MRBD of greater amplitude compared to their younger counterparts, even though their beta power remains higher both at rest and during muscle contractions. Further, a modulation in MRBD has been observed during sustained and dynamic pinch contractions, whereby beta activity during periods of steady contraction following a dynamic contraction is elevated. However, how the modulation of MRBD is affected by aging has remained an open question. In the present work, we investigated the effect of aging on the modulation of beta oscillations and their putative link with motor performance. We collected magnetoencephalography (MEG) data from younger and older adults during a resting-state period and motor handgrip paradigms, which included sustained and dynamic contractions, to quantify spontaneous and motor-related beta oscillatory activity. Beta power at rest was found to be significantly increased in the motor cortex of older adults. During dynamic hand contractions, MRBD was more pronounced in older participants in frontal, premotor and motor brain regions. These brain areas also exhibited age-related decreases in cortical thickness; however, the magnitude of MRBD and cortical thickness were not found to be associated after controlling for age. During sustained hand contractions, MRBD exhibited a decrease in magnitude compared to dynamic contraction periods in both groups and did not show age-related differences. This suggests that the amplitude change in MRBD between dynamic and sustained contractions is larger in older compared to younger adults. We further probed for a relationship between beta oscillations and motor behaviour and found that greater MRBD in primary motor cortices was related to degraded motor performance beyond age, but our results suggested that age-related differences in beta oscillations were not predictive of motor performance

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

Bimanual prehension to a solitary target

Grasping and functionally interacting with a relatively large or awkwardly shaped object requires the independent and cooperative coordination of both limbs. Acknowledging the vital role of visual information in successfully executing any prehensile movements, the present study aimed to clarify how well existing bimanual coordination models (Kelso et al, 1979; Marteniuk & Mackenzie, 1980) can account for bimanual prehension movements targeting a single end-point under varying visual conditions. We therefore, employed two experiments in which vision of the target object and limbs was available or unavailable during a bimanual movement in order to determine the affects of visual or memory-guided control (e.g. feedback vs. feed forward) on limb coordination.Ten right-handed participants (mean age = 24.5) performed a specific bimanual prehension movement targeting a solitary, static object under both visual closed loop (CL) and open loop 2s delay (OL2) conditions. Target location was varied while target amplitude remained constant. Kinematic data (bimanual coupling variables) indicated that regardless of target location, participants employed one of two highly successful movement execution strategies depending on visual feedback availability. During visual (CL) conditions participants employed a ‘dominant-hand initiation’ strategy characterized by a significantly faster right-hand (RH) reaction time and simultaneous hand contact with the target. In contrast, when no visual feedback was available (OL2), participants utilized a ‘search and follow’ strategy characterized by limb coupling at movement onset and a reliance on the dominant RH to contact the target ~62 ms before the left.In conclusion, the common goal parameters of targeting a single object with both hands are maintained and successfully achieved regardless of visual condition. Furthermore, independent programming of each limb is undeniably evident within the behaviours observed providing support for the neural cross-talk theory of bimanual coordination (Marteniuk & Mackenzie, 1980). Whether movement execution is visually (CL) or memory-guided (OL2) there is a clear preference of RH utilization possibly due to its dynamic and/or hemispheric advantages in controlling complex motor behaviours (Gonzalez et al., 2006). Therefore, we propose that bimanual grasping to a solitary target is possibly governed globally by a higher-level structure and successful execution is achieved via independent spinal pathway modulation of limbs

Assessing Performance, Role Sharing, and Control Mechanisms in Human-Human Physical Interaction for Object Manipulation

abstract: Object manipulation is a common sensorimotor task that humans perform to interact with the physical world. The first aim of this dissertation was to characterize and identify the role of feedback and feedforward mechanisms for force control in object manipulation by introducing a new feature based on force trajectories to quantify the interaction between feedback- and feedforward control. This feature was applied on two grasp contexts: grasping the object at either (1) predetermined or (2) self-selected grasp locations (“constrained” and “unconstrained”, respectively), where unconstrained grasping is thought to involve feedback-driven force corrections to a greater extent than constrained grasping. This proposition was confirmed by force feature analysis. The second aim of this dissertation was to quantify whether force control mechanisms differ between dominant and non-dominant hands. The force feature analysis demonstrated that manipulation by the dominant hand relies on feedforward control more than the non-dominant hand. The third aim was to quantify coordination mechanisms underlying physical interaction by dyads in object manipulation. The results revealed that only individuals with worse solo performance benefit from interpersonal coordination through physical couplings, whereas the better individuals do not. This work showed that naturally emerging leader-follower roles, whereby the leader in dyadic manipulation exhibits significant greater force changes than the follower. Furthermore, brain activity measured through electroencephalography (EEG) could discriminate leader and follower roles as indicated power modulation in the alpha frequency band over centro-parietal areas. Lastly, this dissertation suggested that the relation between force and motion (arm impedance) could be an important means for communicating intended movement direction between biological agents.Dissertation/ThesisDoctoral Dissertation Biomedical Engineering 201

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