Motor-cortical beta oscillations are modulated by correctness of observed action

Contains fulltext : 73550.pdf (Publisher’s version ) (Closed access)How humans understand the intention of others’ actions remains controversial. Some authors have suggested that intentions are recognized by means of a motor simulation of the observed action with the mirror-neuron system [1–3]. Others emphasize that intention recognition is an inferential process, often called ‘‘mentalizing’’ or employing a ‘‘theory of mind,’’ which activates areas well outside the motor system [4–6]. Here, we assessed the contribution of brain regions involved in motor simulation and mentalizing for understanding action intentions via functional brain imaging. Results show that the inferior frontal gyrus (part of the mirror-neuron system) processes the intentionality of an observed action on the basis of the visual properties of the action, irrespective of whether the subject paid attention to the intention or not. Conversely, brain areas that are part of a ‘‘mentalizing’’ network become active when subjects reflect about the intentionality of an observed action, but they are largely insensitive to the visual properties of the observed action. This supports the hypothesis that motor simulation and mentalizing have distinct but complementary functions for the recognition of others’ intentions

Relationship between activity in human primary motor cortex during action observation and the mirror neuron system

The attenuation of the beta cortical oscillations during action observation has been interpreted as evidence of a mirror neuron system (MNS) in humans. Here we investigated the modulation of beta cortical oscillations with the viewpoint of an observed action. We asked subjects to observe videos of an actor making a variety of arm movements. We show that when subjects were observing arm movements there was a significant modulation of beta oscillations overlying left and right sensorimotor cortices. This pattern of attenuation was driven by the side of the screen on which the observed movement occurred and not by the hand that was observed moving. These results are discussed in terms of the firing patterns of mirror neurons in F5 which have been reported to have similar properties

Effect of Sensory Attenuation on Cortical Movement-Related Oscillations

This study examined the impact of induced sensory deficits on cortical, movement-related oscillations measured using electroencephalography (EEG). We hypothesized that EEG patterns in healthy subjects with induced sensory reduction would be comparable to EEG found after chronic loss of sensory feedback. EEG signals from 64 scalp locations were measured from 10 healthy subjects. Participants dorsiflexed their ankle after prolonged vibration of the tibialis anterior (TA). Beta band time frequency decompositions were calculated using wavelets and compared across conditions. Changes in patterns of movement-related brain activity were observed following attenuation of sensory feedback. A significant decrease in beta power of event-related synchronization was associated with simple ankle dorsiflexion after prolonged vibration of the TA. Attenuation of sensory feedback in young, healthy subjects led to a corresponding decrease in beta band synchronization. This temporary change in beta oscillations suggests that these modulations are a mechanism for sensorimotor integration. The loss of sensory feedback found in spinal cord injury patients contributes to changes in EEG signals underlying motor commands. Similar alterations in cortical signals in healthy subjects with reduced sensory feedback implies these changes reflect normal sensorimotor integration after reduced sensory input rather than brain plasticity

Gearing up for action: attentive tracking dynamically tunes sensory and motor oscillations in the alpha and beta band

Allocation of attention during goal-directed behavior entails simultaneous processing of relevant and attenuation of irrelevant information. How the brain delegates such processes when confronted with dynamic (biological motion) stimuli and harnesses relevant sensory information for sculpting prospective responses remains unclear. We analyzed neuromagnetic signals that were recorded while participants attentively tracked an actor’s pointing movement that ended at the location where subsequently the response-cue indicated the required response. We found the observers’ spatial allocation of attention to be dynamically reflected in lateralized parieto-occipital alpha (8-12Hz) activity and to have a lasting influence on motor preparation. Specifically, beta (16-25Hz) power modulation reflected observers’ tendency to selectively prepare for a spatially compatible response even before knowing the required one. We discuss the observed frequency-specific and temporally evolving neural activity within a framework of integrated visuomotor processing and point towards possible implications about the mechanisms involved in action observation

Relationship between Activity in Human Primary Motor Cortex during Action Observation and the Mirror Neuron System

The attenuation of the beta cortical oscillations during action observation has been interpreted as evidence of a mirror neuron system (MNS) in humans. Here we investigated the modulation of beta cortical oscillations with the viewpoint of an observed action. We asked subjects to observe videos of an actor making a variety of arm movements. We show that when subjects were observing arm movements there was a significant modulation of beta oscillations overlying left and right sensorimotor cortices. This pattern of attenuation was driven by the side of the screen on which the observed movement occurred and not by the hand that was observed moving. These results are discussed in terms of the firing patterns of mirror neurons in F5 which have been reported to have similar properties

Electrocortical underpinnings of error monitoring in health and pathology

It becomes clear from the literature described above (Chapter 1), that the error monitoring mechanisms play a fundamental role in signalling the need for cognitive control. Many studies already provided a consistent evidence on the existence of peculiar ways in which the brain signals this need through electrophysiological changes. However, the following set of empirical studies aims to gain further insight into these complex processes by measuring brain activity changes in situations that alter the way one experience errors. The second Chapter (Chapter 2) consists of a brief commentary that was made in response to an article on the brain activity to action errors. In this commentary we propose new possibilities to explore our topic of interest, by taking advantage of EEG and modern virtual reality facilities. The thesis includes three EEG-VR studies: one on the error-mechanism in healthy participants (Chapter 3) and two studies on error monitoring system in pathological populations (Chapter 4, 5), as main parts of the core of the thesis. As a collateral project, in the Appendix, there is an EEG study on action observation in elite players (Chapter 7). In the first study (Chapter 3), we investigated a very simple but fundamental question. As we saw in the introduction, error-related signatures are evoked when an error occurs. But it is not clear how much of this is due to the occurrence of a violation of the intended goal or simply to the observation of a rare – thus less predictable – event. To this aim, we used a paradigm developed in the former years in our laboratory (Pavone et al., 2016; Spinelli et al., 2017), characterized by a setup in immersive Virtual Reality (VR) and simultaneous EEG recording. Building on the previous findings, we designed an EEG-VR study in which we manipulated the probability of observing errors in actions. In another study (Chapter 4) we investigated how erroneous actions are experienced by people with brain damage and diagnosis of Apraxia. Apraxic patients are people with hemispheric lesions and defective awareness on a variety of aspects that cover perceptuo-motor, cognitive or emotional domains. This study was developed after the results obtained by Canzano and colleagues (2014) in a behavioral study in which apraxic patients were asked to imitate the actions executed by the experimenter and judge their correctness; results revealed that bucco-facial apraxic patients manifest a specific deficit in detecting their own gestural errors when they are explicitly asked to judge them. With the present study we wanted to investigate apraxic brain’ response to action errors, while they embody an avatar in first person perspective (EEG-VR setup). The third study (Chapter 5) investigates the integrity of the error-monitoring system in Parkinson’s Disease and the impact of the dopaminergic treatment in the brain response to errors. To this aim we used the proposed VR action-observation paradigm, in which Parkinson patients observed successful and unsuccessful reach-to-grasp actions in first person perspective while EEG activity was recorded; the same patients were tested while being under dopaminergic treatment and during a dopaminergic withdrawal state. In another chapter we provide a critical overview of the findings of this work (General Discussion, Chapter 6). In the last chapter, the Appendix (Chapter 7), there is a collateral project of another research line of the Laboratory, in which I have being involved. In this study we are investigating the cortical underpinning of elite players during observation of goal-directed actions, in their domain of expertise. We recorded the EEG activity of elite wheelchair basketball players while observing free-throws performed by paraplegic athletes. We expected their brain correlates to be different from novice players and to be able to easily discriminate whether a basketball shot would be successful or unsuccessful (project still ongoing)

Sensorimotor Alpha Activity is Modulated in Response to the Observation of Pain in Others

The perception–action account of empathy states that observation of another person's state automatically activates a similar state in the observer. It is still unclear in what way ongoing sensorimotor alpha oscillations are involved in this process. Although they have been repeatedly implicated in (biological) action observation and understanding communicative gestures, less is known about their role in vicarious pain observation. Their role is understood as providing a graded inhibition through functional inhibition, thereby streamlining information flow through the cortex. Although alpha oscillations have been shown to have at least visual and sensorimotor origins, only the latter are expected to be involved in the empathetic response. Here, we used magnetoencephalography, allowing us to spatially distinguish and localize oscillatory components using beamformer source reconstruction. Subjects observed realistic pictures of limbs in painful and no-pain (control) conditions. As predicted, time–frequency analysis indeed showed increased alpha suppression in the pain condition compared to the no-pain condition. Although both pain and no-pain conditions suppressed alpha- and beta-band activity at both posterior and central sensors, the pain condition suppressed alpha more only at central sensors. Source reconstruction localized these differences along the central sulcus. Our results could not be accounted for by differences in the evoked fields, suggesting a unique role of oscillatory activity in empathetic responses. We argue that alpha oscillations provide a unique measure of the underlying functional architecture of the brain, suggesting an automatic disinhibition of the sensorimotor cortices in response to the observation of pain in others

Language–motor interference reflected in MEG beta oscillations

AbstractThe involvement of the brain's motor system in action-related language processing can lead to overt interference with simultaneous action execution. The aim of the current study was to find evidence for this behavioural interference effect and to investigate its neurophysiological correlates using oscillatory MEG analysis. Subjects performed a semantic decision task on single action verbs, describing actions executed with the hands or the feet, and abstract verbs. Right hand button press responses were given for concrete verbs only. Therefore, longer response latencies for hand compared to foot verbs should reflect interference. We found interference effects to depend on verb imageability: overall response latencies for hand verbs did not differ significantly from foot verbs. However, imageability interacted with effector: while response latencies to hand and foot verbs with low imageability were equally fast, those for highly imageable hand verbs were longer than for highly imageable foot verbs. The difference is reflected in motor-related MEG beta band power suppression, which was weaker for highly imageable hand verbs compared with highly imageable foot verbs. This provides a putative neuronal mechanism for language–motor interference where the involvement of cortical hand motor areas in hand verb processing interacts with the typical beta suppression seen before movements. We found that the facilitatory effect of higher imageability on action verb processing time is perturbed when verb and motor response relate to the same body part. Importantly, this effect is accompanied by neurophysiological effects in beta band oscillations. The attenuated power suppression around the time of movement, reflecting decreased cortical excitability, seems to result from motor simulation during action-related language processing. This is in line with embodied cognition theories

Using Goal- and Grip-Related Information for Understanding the Correctness of Other’s Actions: An ERP Study

Detecting errors in other’s actions is of pivotal importance for joint action, competitive behavior and observational learning. Although many studies have focused on the neural mechanisms involved in detecting low-level errors, relatively little is known about error-detection in everyday situations. The present study aimed to identify the functional and neural mechanisms whereby we understand the correctness of other’s actions involving well-known objects (e.g. pouring coffee in a cup). Participants observed action sequences in which the correctness of the object grasped and the grip applied to a pair of objects were independently manipulated. Observation of object violations (e.g. grasping the empty cup instead of the coffee pot) resulted in a stronger P3-effect than observation of grip errors (e.g. grasping the coffee pot at the upper part instead of the handle), likely reflecting a reorienting response, directing attention to the relevant location. Following the P3-effect, a parietal slow wave positivity was observed that persisted for grip-errors, likely reflecting the detection of an incorrect hand-object interaction. These findings provide new insight in the functional significance of the neurophysiological markers associated with the observation of incorrect actions and suggest that the P3-effect and the subsequent parietal slow wave positivity may reflect the detection of errors at different levels in the action hierarchy. Thereby this study elucidates the cognitive processes that support the detection of action violations in the selection of objects and grips

Semantics in the Motor System: Motor-Cortical Beta Oscillations Reflect Semantic Knowledge of End-Postures for Object Use

In the present EEG study we investigated whether semantic knowledge for object use is represented in motor-related brain areas. Subjects were required to perform actions with everyday objects and to maintain either a meaningful or a meaningless end posture with the object. Analysis of the EEG data focused on the beta-frequency band, as previous studies have indicated that the maintenance of a posture is reflected in stronger beta-oscillations. Time frequency analysis indicated that the execution of actions resulting in a meaningless compared to a meaningful end posture was accompanied by a stronger beta-desynchronization towards the end of the movement and a stronger subsequent beta-rebound after posture-onset. The effect in the beta-frequency band was localized to premotor, parietal and medial frontal areas and could not be attributed to differences in timing or movement complexity between meaningful and meaningless actions. Together these findings directly show that the motor system is differentially activated during the execution and maintenance of semantically correct or incorrect end postures. This suggests that semantic object knowledge is indeed represented in motor-related brain areas, organized around specific end postures associated with the use of objects