Simultaneous scalp recorded EEG and local field potentials from monkey ventral premotor cortex during action observation and execution reveals the contribution of mirror and motor neurons to the mu-rhythm

The desynchronization of alpha and beta oscillations (mu rhythm) in the central scalp EEG during action observation and action execution is thought to reflect neural mirroring processes. However, the extent to which mirror neurons (MNs) or other populations of neurons contribute to such EEG desynchronization is still unknown. Here, we provide the first evidence that, in the monkey, the neuronal activity recorded from the ventral premotor cortex (PMv) strongly contributes to the EEG changes occurring in the beta band over central scalp electrodes, during executed and observed actions. We simultaneously recorded scalp EEG and extracellular activity, Multi Unit Activity (MUA) and Local Field Potentials (LFP), from area F5 of two macaques executing and observing grasping actions. We found that MUA highly correlates with an increase in high gamma LFP power and, interestingly, such LFP power increase also correlates to EEG beta – and in part also to alpha – desynchronization. In terms of timing of signal changes, the increase in high gamma LFP power precedes the EEG desynchronization, during both action observation and execution, thus suggesting a causal role of PMv neuronal activity in the modulation of the alpha and beta mu-rhythm. Lastly, neuronal signals from deeper layers of PMv exert a greater contribution than superficial layers to the EEG beta rhythm modulation, especially during the motor task. Our findings have clear implications for EEG studies in that they demonstrate that the activity of different populations of neurons in PMv contribute to the generation of the mu-rhythm

Neural basis of motor planning for object-oriented actions: the role of kinematics and cognitive aspects

The project I have carried out in these three years as PhD student pursued the aim of describing the motor preparation activity related to the object oriented actions actually performed. The importance of these studies comes from the lack of literature on EEG and complex movements actually executed and not just mimed or pantomimed. Using the term ‘complex’ here we refer to actions that are oriented to an object with the intent to interact with it. In order to provide a broader idea about the aim of the project, I have illustrated the complexity of the movements and cortical networks involved in their processing and execution. Several cortical areas concur to the plan and execution of a movement, and the contribution of these different areas changes according to the complexity, in terms of kinematics, of the action. The object-oriented action seems to be a circuit apart: besides motor structures, it also involves a temporo-parietal network that takes part to both planning and performing actions like reaching and grasping. Such findings have been pointed out starting from studies on the Mirror neuron system discovered in monkeys at the beginning of the ‘90s and subsequently extended to humans. Apart from all the speculations this discovery has opened to, many different researchers have started investigating different aspects related to reaching and grasping movements, describing different areas involved, all belonging to the posterior parietal cortex (PPC), and their connections with anterior motor cortices through different paradigms and techniques. Most of the studies investigating movement execution and preparation are studies on monkey or fMRI studies on humans. Limits of this technique come from its low temporal resolution and the impossibility to use self-paced movement, that is, movement performed in more ecological conditions when the subject decides freely to move. On the few studies investigating motor preparation using EEG, only pantomime of action has been used, more than real interactions with objects. Because all of these factors, we decided to get through the description of the motor preparation activity for goal oriented actions pursuing two aims: in the first instance, to describe this activity for grasping and reaching actions actually performed toward a cup (a very ecological object); secondly, we wanted to verify which parameters in these kind of movements are taken into account during their planning and preparation: because of all the variables involved in grasping and reaching movements, like the position of the objects, its features, the goal of the action and its meaning, we tried to verify how these variables could affect motor preparation creating two different experiments. In the first one, subjects were requested to perform a grasping and a reaching action toward a cup and in a third condition we tied up their hands as fist in order to verify what it could happen when people are in the condition of turning an ordinary and easy action into a new one to accomplish the final task requested. In the second experiment, we better accounted for the cognitive aspects beyond the motor preparation of an action. Here, indeed, we tested a very simple action like a key press in two different conditions. In the first one the button press was not related to any kind of consequence, whereas in the second case the same action triggered a video on a screen showing a hand moving toward a cup and grasping it (giving like a video-game effect). Both the experiments have shown results straightening the role cognitive processes have in motor planning. In particular, it seemed that the goal of the action, along with the object we are going to interact with, could create a particular response and activity starting very early in the posterior parietal cortex. Finally, because of the actions used in these experiments, it was important testing the hypothesis that our findings could be generalized even to the observation of those same actions. As I mentioned before, object-oriented actions have received great attention starting from the discovery of the mirror neuron system which showed a correspondence between the cortical activity of the person performing the action with the one produced in the observer. Such a finding allowed to describe our brain as a social brain, able to create a mental representation of what the other person is doing which allows us to understand others gesture and intentions. What we wanted to test in this project was the possibility that such a correspondence between the observer and the actor would had been extended even to the motor preparation period of an upcoming action, giving credit to the hypothesis of considering the human brain as able to even predict others actions and intentions besides understanding them. In the last experiment I carried out in my project, thus, I used the same actions involved in the first experiment but asking this time to observe them passively instead of performing them. The results provided in this study confirmed the cognitive, rather than motor, role the PPC plays in action planning. Indeed, even when no movements are involved, the same structure are active reflecting the activity found in the execution experiment. The main result I have reported in this dissertation is related to the suggestion of a new model to understand the role the PPC has in object-oriented movements. Unlike previous hypothesis and models suggesting the contribution of PPC in extracting affordances from the objects or monitoring and transforming coordinates between us and the object into intention for acting, we suggest here that the role of the parietal areas is more to make a judge about the appropriate match of the action goal with the affordances provided by the object. When actually the action we are going to perform fits well with the object features, the PPC starts its activity, elaborating all those coordinates representation and monitoring the execution and programming phases of movement. This model is well supported by results from both our experiments and well combines the two previous models, but putting more emphasis on the ‘goal-object matching’ function of the PPC and the Superior parietal lobe (SPL) in particular

Investigating the effects of neuromodulatory training on autistic traits: a multi-methods psychophysiological study.

Autism spectrum disorder (ASD) is characterized by noticeable difficulties with social interaction and communication. Building on past research in this area and with the aim of improving methodological perspectives, a multi method approach to the study of ASD, mirror neurons and neurofeedback was taken. This thesis is made up of three main experiments: 1) A descriptive study of the resting state electroencephalography (EEG) across the spectrum of autistic traits in neurotypical individuals, 2) A comparison of 3 EEG protocols on MNs activation (mu suppression) and its difference according to self-reported traits of autism in neurotypical individuals, and 3) Neurofeedback training (NFT) on individuals with high autistic traits. In chapters 3 and 4 we employed simultaneous monitoring of physiological data. For chapter 3 EEG and eye-tracking was used, In the case of chapter 4, EEG and eye-tracking as well functional near infrared spectroscopy (fNIRS). Overall the findings revealed differences in mu rhythm reactivity associated to AQ traits. In chapter 2, the rEEG showed that individuals with high AQ scores showed less activation of frontal and fronto-central regions combined with higher levels of complexity in fronto-temporal, temporal, parietal and parieto-occipital areas. In chapter 3, EEG protocols that elicited Mu reactivity in individuals with different AQ traits suggested that as the AQ traits become more pronounced in neurotypical population, the event-related desynchronization (ERD) in low alpha declines. Chapter 3 was also the basis for the choice of pre/post assessment for chapter 4. In chapter 4 the multi-method physiological approach provided parallel physiological evidence for the effects of NFT in sensorimotor reactivity, namely, an increase in ERD in high alpha, higher levels of oxygenated haemoglobin and changes to the amplitude and frequency in the microstructure of mu for participants who underwent active training as opposed to a sham group

Reach to grasp movement: a simultaneous recording approach

In our everyday life, we interact continually with objects. We reach for them, we grasp them, we manipulate them. All these actions are apparently very simple. Yet, this is not so. The mechanisms that underlie them are complex, and require multiple visuomotor transformations entailing the capacity to transform the visual features of the object in the appropriate hand configuration, and the capacity to execute and control hand and finger movements. In neural terms, grasping behavior can be dissociated into separate reach and grip components. According to this view, computations regarding the grasp component occurs within a lateral parietofrontal circuit involving the anterior intraparietal area (AIP) and both the dorsal (PMd) and the ventral (PMv) premotor areas. The general agreement is that the processes occurring in AIP constitute the initial step of the transformation leading from representation of objects to movement aimed at interacting with such objects. Evidence supporting this view comes from neurophysiological studies showing that the representation of three-dimensional object features influences both the rostral sector of the ventral premotor cortex (area F5) and the ventro-rostral sector of the dorsal premotor area (area F2vr; for review see Filimon, 2010). With respect to the reach component, there is agreement that it is subserved by a more medial parieto-frontal circuit including the medial intraparietal area (mIP) termed as the parietal reach region (PRR), area V6A, and the dorsal premotor area F2. Human neuroimaging studies go in the same direction. They showed the involvement of the anterior portion of the human AIP in grasping behavior and they proposed human homologues of both the ventral and dorsal premotor cortices during grasping. Whereas, reaching activates the medial intraparietal and the superior parieto-occipital cortex (for review see Castiello & Begliomini, 2008). Altogether these studies suggest that in humans, like in monkeys, reach to grasp movements involve a large network of interconnected structures in the parietal and frontal lobes. And, that this cortical network is differentially involved for the control of distinct aspects characterizing the planning and the control of reach to grasp movement. Nevertheless, how the neural control systems interact with the complex biomechanics of moving limbs - as to help us to identify the operational principles to look for in reach to grasp studies and, more in general, in motor control - remains an open question. In this respect, it is only through the use of converging techniques with different characteristics that we might fully understand how the human brain controls the grasping function. What is so far lacking in the literature on cortical control of grasp in humans is a systematic documentation of the time course of neural activity during performance of reach to grasp movement. To fill this gap the present thesis will consider the co-registration of behavioural and neural events in order to provide deeper insights into the neuro-functional basis of reach to grasp movements in humans. In Chapter 1 an overview on the state of the art in many disciplines investigating reach to grasp processes will be provided, with particular attention to neurophysiology, from which most of the knowledge regarding the neural underpinnings of reach to grasp movements comes from. Furthermore, kinematical as well as neuroimaging, and evoked related potentials (ERP) investigations will be reviewed. Particular emphasis will be given to neuroimaging studies, especially those exploring grasping movements by functional magnetic resonance imaging (fMRI), as the technique adopted to conduct the studies presented in this thesis (Chapter 1). Basic principles of co-registration techniques, which are at the core of the methodological aspect of the present thesis, will be reviewed (Chapter 2). In this respect, a description of the methodologies adopted in the present thesis together with general information regarding signal processing and data analysis for these different techniques will be provided in specific appendices (III, IV). Then, three studies focusing on the co-registration of kinematical with ERP (Chapters 3 and 4) and FMRI with ERP (Chapter 5) will be presented and discussed. In Chapter 3 the co-registration of ERP and kinematical signals will be considered with specific reference to hand shaping, that is the grasp component of the targeted movement. A similar co-registration approach will be adopted in Chapter 4 for investigating the underlying circuits of reaching. The focus for Chapter 5 will be the co-registration of ERPs and fMRI signals as to reveal the time course of activation of the differential cortical areas related to the planning, initiation and on-line control of reaching and grasping movements and how such activity varies depending on object size. A general discussion (Chapter 6), contextualizing the results obtained by the studies presented in this thesis will follow

Pre-movement changes in sensorimotor beta oscillations predict motor adaptation drive

International audienceBeta frequency oscillations in scalp electroencephalography (EEG) recordings over the primary motor cortex have been associated with the preparation and execution of voluntary movements. Here, we test whether changes in beta frequency are related to the preparation of adapted movements in human, and whether such effects generalise to other species (cat). Eleven healthy adult humans performed a joystick visuomotor adaptation task. Beta (15-25 Hz) scalp EEG signals recorded over the motor cortex during a pre-movement preparatory phase were, on average, significantly reduced in amplitude during early adaptation trials compared to baseline, late adaptation, or aftereffect trials. The changes in beta were not related to measurements of reaction time or reach duration. We also recorded local field potential (LFP) activity within the primary motor cortex of three cats during a prism visuomotor adaptation task. Analysis of these signals revealed similar reductions in motor cortical LFP beta frequencies during early adaptation. This effect was present when controlling for any influence of the reaction time and reach duration. Overall, the results are consistent with a reduction in pre-movement beta oscillations predicting an increase in adaptive drive in upcoming task performance when motor errors are largest in magnitude and the rate of adaptation is greatest

Développement et fonctionnement des mécanismes de résonance motrice chez l'humain

La découverte dans le cerveau du singe macaque de cellules visuo-motrices qui répondent de façon identique à la production et la perception d’actes moteurs soutient l’idée que ces cellules, connues sous le nom de neurones-miroirs, encoderaient la représentation d’actes moteurs. Ces neurones, et le système qu’ils forment, constitueraient un système de compréhension moteur; par delà la simple représentation motrice, il est également possible que ce système participe à des processus de haut niveau en lien avec la cognition sociale. Chez l’humain adulte, des études d’imagerie récentes montrent d’importants chevauchements entre les patrons d’activité liés à l’exécution d’actes moteurs et ceux associés à la perception d’actions. Cependant, malgré le nombre important d’études sur ce système de résonance motrice, étonnamment peu se sont penchées sur les aspects développementaux de ce mécanisme, de même que sa relation avec certaines habiletés sociales dans la population neurotypique. De plus, malgré l’utilisation répandue de certaines techniques neurophysiologiques pour quantifier l’activité de ce système, notamment l’électroencéphalographie et la stimulation magnétique transcrânienne, on ignore en grande partie la spécificité et la convergence de ces mesures dans l’étude des processus de résonance motrice. Les études rassemblées ici visent à combler ces lacunes, c'est-à-dire (1) définir l’existence et les propriétés fonctionnelles du système de résonance motrice chez l’enfant humain, (2) établir le lien entre ce système et certaines habiletés sociales spécifiques et (3) déterminer la validité des outils d’investigation couramment utilisés pour mesurer son activité. Dans l’article 1, l’électroencéphalographie quantitative est utilisée afin de mesurer l’activité des régions sensorimotrices chez un groupe d’enfants d’âge scolaire durant la perception d’actions de la main. On y démontre une modulation de l’activité du rythme mu aux sites centraux non seulement lors de l’exécution de tâches motrices, mais également lors de l’observation passive d’actions. Ces résultats soutiennent l’hypothèse de l’existence d’un système de résonance motrice sensible aux représentations visuelles d’actes moteurs dans le cerveau immature. L’article 2 constitue une étude de cas réalisée chez une jeune fille de 12 ans opérée pour épilepsie réfractaire aux médicaments. L’électroencéphalographie intracrânienne est utilisée afin d’évaluer le recrutement du cortex moteur lors de la perception de sons d’actions. On y montre une modulation de l’activité du cortex moteur, visible dans deux périodes distinctes, qui se reflètent par une diminution de la puissance spectrale des fréquences beta et alpha. Ces résultats soutiennent l’hypothèse de l’existence d’un système de résonance motrice sensible aux représentations auditives d’actions chez l’enfant. L’article 3 constitue une recension des écrits portant sur les données comportementales et neurophysiologiques qui suggèrent la présence d’un système de compréhension d’action fonctionnel dès la naissance. On y propose un modèle théorique où les comportements d’imitation néonataux sont vus comme la résultante de mécanismes d’appariement moteurs non inhibés. Afin de mesurer adéquatement la présence de traits empathiques et autistique dans le but de les mettre en relation avec l’activité du système de résonance motrice, l’article 4 consiste en une validation de versions françaises des échelles Empathy Quotient (Baron-Cohen & Wheelwright, 2004) et Autism Spectrum Quotient (Baron-Cohen et al., 2001) qui seront utilisées dans l’article 5. Les versions traduites de ces échelles ont été administrées à 100 individus sains et 23 personnes avec un trouble du spectre autistique. Les résultats répliquent fidèlement ceux obtenus avec les questionnaires en version anglaise, ce qui suggère la validité des versions françaises. Dans l’article 5, on utilise la stimulation magnétique transcrânienne afin d’investiguer le décours temporel de l’activité du cortex moteur durant la perception d’action et le lien de cette activité avec la présence de traits autistiques et empathiques chez des individus normaux. On y montre que le cortex moteur est rapidement activé suivant la perception d’un mouvement moteur, et que cette activité est corrélée avec les mesures sociocognitives utilisées. Ces résultats suggèrent l’existence d’un système d’appariement moteur rapide dans le cerveau humain dont l’activité est associée aux aptitudes sociales. L’article 6 porte sur la spécificité des outils d’investigation neurophysiologique utilisés dans les études précédentes : la stimulation magnétique transcrânienne et l’électroencéphalographie quantitative. En utilisant ces deux techniques simultanément lors d’observation, d’imagination et d’exécution d’actions, on montre qu’elles évaluent possiblement des processus distincts au sein du système de résonance motrice. En résumé, cette thèse vise à documenter l’existence d’un système de résonance motrice chez l’enfant, d’établir le lien entre son fonctionnement et certaines aptitudes sociales et d’évaluer la validité et la spécificité des outils utilisés pour mesurer l’activité au sein de ce système. Bien que des recherches subséquentes s’avèrent nécessaires afin de compléter le travail entamé ici, les études présentées constituent une avancée significative dans la compréhension du développement et du fonctionnement du système de résonance motrice, et pourraient éventuellement contribuer à l’élaboration d’outils diagnostiques et/ou de thérapeutiques chez des populations où des anomalies de ce système ont été répertoriées.The discovery of cells in the macaque brain that respond both to action production and perception brings support to the hypothesis that these mirror-neurons (MN) code for the representation of action. These cells, and the system they form (the so-called mirror neuron system; MNS), appear to underlie action understanding by simulating the perceived action into the observer’s brain. Beyond simple action understanding, it has been suggested that this system contributes to higher-order processes related to social cognition. In human adults, recent imaging studies have shown important ovelaps in the activity patterns during both action production and execution, supporting the existence of a system similar to that shown in monkeys. However, surprisingly few studies have investigated the presence and the development of the MNS in the human child, and its relationship with socio-cognitive abilities in healthy individuals. Moreover, we still ignore the specificity of measures widely used to assess this system. The studies that follow aim at clarifying these issues. More specifically, the main objectives of this work are to : (1) establish the existence and the properties of motor resonance mechanisms in children; (2) clarify the relationship between activity of the MNS and social abilities in healthy individuals; and (3) determine the specificity of neurophysiological tools widely used to measure MNS activity in humans. In the first article, quantitative electroencephalography is used to assess the activity of sensorimotor regions in a group of school-age children during the observation of simple hand movements. We show a modulation of mu rhtyhm activity at central sites not only during motor production, but also during passive action observation. These results support the existence of an action-execution pairing system sensitive to visual actions in the immature brain. In the second article, we present an experiment conducted in a 12 year-old child undergoing presurgical monitoring for intractable epilepsy. Intracranial electroencephalography is used to assess motor cortex involvement in the perception of action-related sounds. We show a modulation of motor cortex activity at two distinct time-periods in the alpha and beta bands. These results suggest the presence of a motor matching system sensitive to auditory stimuli in the child’s brain. In the third article, we present an overview of behavioral and neurophysiological data supporting the idea that an action-understanding system is present from birth in humans. We propose a theoretical model whereby neonatal imitation is the result on an uninhibited motor resonance system. In order to adequatly measure the presence of empathic and autistic traits in healhy individuals to assess their link with motor resonance, article 4 consists of a french validation of questionnaires used in the fifth article, the Empathy Quotient (Baron-Cohen & Wheelwright, 2004) and the Autism Spectrum Quotient (Baron-Cohen et al., 2001). Translated versions of these scales were administered to 100 healthy adults and 23 individuals with autistic spectrum disorders. Our results replicate faithfully those obtained with the original version of the scales. In the fifth article, transcranial magnetic stimulation is used to assess the timecourse of motor cortex activity during action observation, as well as its relationship with empthic and autistic traits in healthy individuals. We show that the motor cortex is rapidly modulated following movement onset, and that its activity correlates with specific socio-cognitives measures. These results suggest the presence of a rapid mechanism taking place in the motor resonance system that is related to social ability. The sixth acticle aims at clarifying the specificity of the neurophysiological tools used in the preceeding studies to quantify MNS, namely transcranial magnetic stimulation and quantitative electroencephalography. Using both techniques simultaneously during action observation, imagination and execution, we show that these measures capture different aspects of motor resonance. In summary, this thesis aims at documenting the existence of a motor resonance mechanism in children, establishing the relationship between MNS activity and socio-cognitive traits and assessing the specificity of the measures used to quantify activity within this system. Although further studies are needed to complete the task begun here, these studies contribute significantly to our understanding of the development and function of motor resonance mechanism is humans. In the long run, they could contribute to the elaboration of diagnostic markers, and ultimately therapeutic targets, in clinical populations where abnormalities of this system have been documented

Neurophysiological correlates of preparation for action measured by electroencephalography

The optimal performance of an action depends to a great extend on the ability of a person to prepare in advance the appropriate kinetic and kinematic parameters at a specific point in time in order to meet the demands of a given situation and to foresee its consequences to the surrounding environment. In the research presented in this thesis, I employed high-density electroencephalography in order to study the neural processes underlying preparation for action. A typical way for studying preparation for action in neuroscience is to divide it in temporal preparation (when to respond) and event preparation (what response to make). In Chapter 2, we identified electrophysiological signs of implicit temporal preparation in a task where such preparation was not essential for the performance of the task. Electrophysiological traces of implicit timing were found in lateral premotor, parietal as well as occipital cortices. In Chapter 3, explicit temporal preparation was assessed by comparing anticipatory and reactive responses to periodically or randomly applied external loads, respectively. Higher (pre)motor preparatory activity was recorded in the former case, which resulted in lower post-load motor cortex activation and consequently to lower long-latency reflex amplitude. Event preparation was the theme of Chapter 4, where we introduced a new method for studying (at the source level) the generator mechanisms of lateralized potentials related to response selection, through the interaction with steady-state somatosensory responses. Finally, in Chapter 5 we provided evidence for the existence of concurrent and mutually inhibiting representations of multiple movement options in premotor and primary motor areas.EThOS - Electronic Theses Online ServiceGBUnited Kingdo

Being an agent or an observer: Different spectral dynamics revealed by MEG

Several neuroimaging studies reported that a common set of regions is recruited during action observation and execution and it has been proposed that the modulation of the μ rhythm, in terms of oscillations in the alpha and beta bands might represent the electrophysiological correlate of the underlying brain mechanisms. However, the specific functional role of these bands within the μ rhythm is still unclear. Here, we used magnetoencephalography (MEG) to analyze the spectral and temporal properties of the alpha and beta bands in healthy subjects during an action observation and execution task. We associated the modulation of the alpha and beta power to a broad action observation network comprising several parieto-frontal areas previously detected in fMRI studies. Of note, we observed a dissociation between alpha and beta bands with a slow-down of beta oscillations compared to alpha during action observation. We hypothesize that this segregation is linked to a different sequence of information processing and we interpret these modulations in terms of internal models (forward and inverse). In fact, these processes showed opposite temporal sequences of occurrence: anterior-posterior during action (both in alpha and beta bands) and roughly posterior-anterior during observation (in the alpha band). The observed differentiation between alpha and beta suggests that these two bands might pursue different functions in the action observation and execution processes

Transcranial alternating current stimulation to areas associated with the human mirror neuron system reveals modulation to mu-suppression and corresponding behaviour

This study was carried out in order to validate the use of EEG mu (μ) suppression as an index of human mirror neuron system (hMNS) related activity. The hMNS is characterized by neuronal activity that responds to both action observation and execution of the same movement. This activity has been directly observed in both macaque monkeys and in humans. There is an abundance of studies using indirect measures of neuronal activity to indicate hMNS-related activity such as TMS, fMRI/PET and EEG/MEG. However, relating indirect indices of neuronal activity to a conceptual group of neurons is controversial because the activity observed could also reflect other neuronal processes. Therefore, the current thesis was designed to establish more direct and causal evidence for the use of EEG in indicating hMNS-related activity through the use of transcranial alternating current stimulation (tACS). This was achieved in six experiments; the first three established an efficient protocol to induce μ-suppression during action observation, and the last three demonstrated by means of tACS that activity in hMNS-related areas is directly related to μ-reactivity during observation of motor movements and in relation to imitation of the movement observed. To this extent, μ-suppression was related to both action observation, and the ability to perform the movement observed. This is interpreted as evidence that EEG μ-suppression is a valid indicator of hMNS-related activity