Functional role of the theory of mind network in integrating mentalistic prior information with action kinematics during action observation.

Inferring intentions from verbal and nonverbal human behaviour is critical for everyday social life. Here, we combined Transcranial Magnetic Stimulation (TMS) with a behavioural priming paradigm to test whether key nodes of the Theory of Mind network (ToMn) contribute to understanding others' intentions by integrating prior knowledge about an agent with the observed action kinematics. We used a modified version of the Faked-Action Discrimination Task (FAD), a forced-choice paradigm in which participants watch videos of actors lifting a cube and judge whether the actors are trying to deceive them concerning the weight of the cube. Videos could be preceded or not by verbal description (prior) about the agent's truthful or deceitful intent. We applied single pulse TMS over three key nodes of the ToMn, namely dorsomedial prefrontal cortex (dmPFC), right posterior superior temporal sulcus (pSTS) and right temporo-parietal junction (rTPJ). Sham-TMS served as a control (baseline) condition. Following sham or rTPJ stimulation, we observed no consistent influence of priors on FAD performance. In contrast, following dmPFC stimulation, and to a lesser extent pSTS stimulation, truthful and deceitful actions were perceived as more deceptive only when the prior suggested a dishonest intention. These findings highlight a functional role of dmPFC and pSTS in coupling prior knowledge about deceptive intents with observed action kinematics in order to judge faked actions. Our study provides causal evidence that fronto-temporal nodes of the ToMn are functionally relevant to mental state inference during action observation.

Human but not robotic gaze facilitates action prediction.

Do people ascribe intentions to humanoid robots as they would to humans or non-human-like animated objects? In six experiments, we compared people's ability to extract non-mentalistic (i.e., where an agent is looking) and mentalistic (i.e., what an agent is looking at; what an agent is going to do) information from gaze and directional cues performed by humans, human-like robots, and a non-human-like object. People were faster to infer the mental content of human agents compared to robotic agents. Furthermore, although the absence of differences in control conditions rules out the use of non-mentalizing strategies, the human-like appearance of non-human agents may engage mentalizing processes to solve the task. Overall, results suggest that human-like robotic actions may be processed differently from humans' and objects' behavior. These findings inform our understanding of the relevance of an object's physical features in triggering mentalizing abilities and its relevance for human-robot interaction.

Brain Dynamics of Action Monitoring in Higher-Order Motor Control Disorders: The Case of Apraxia.

Limb apraxia (LA) refers to a high-order motor disorder characterized by the inability to reproduce transitive actions on commands or after observation. Studies demonstrate that action observation and action execution activate the same networks in the human brain, and provides an onlooker's motor system with appropriate cognitive, motor and sensory-motor cues to flexibly implementing action-sequences and gestures. Tellingly, the temporal dynamics of action monitoring has never been explored in people suffering from LA. To fill this gap, we studied the electro-cortical signatures of error observation in human participants suffering from acquired left-brain lesions with (LA+) and without (LA-) LA, and in a group of healthy controls (H). EEG was acquired while participants observed from a first-person perspective (1PP) an avatar performing correct or incorrect reach-to-grasp a glass action in an immersive-virtual environment. Alterations of typical EEG signatures of error observation in time (early error positivity; Pe) and time-frequency domain (theta band-power) were found reduced in LA+ compared with H. Connectivity analyses showed that LA+ exhibited a decreased theta phase synchronization of both the frontoparietal and frontofrontal network, compared with H and LA-. Moreover, linear regression analysis revealed that the severity of LA [test of upper LA (TULIA) scores] was predicted by mid-frontal error-related theta activity, suggesting a link between error monitoring capacity and apraxic phenotypes. These results provide novel neurophysiological evidence of altered neurophysiological dynamics of action monitoring in individuals with LA and shed light on the performance monitoring changes occurring in this disorder.

Freedom to act enhances the sense of agency, while movement and goal-related prediction errors reduce it.

The Sense of Agency (SoA) is the experience of controlling one's movements and their external consequences. Accumulating evidence suggests that freedom to act enhances SoA, while prediction errors are known to reduce it. Here, we investigated if prediction errors related to movement or to the achievement of the goal of the action exert the same influence on SoA during free and cued actions. Participants pressed a freely chosen or cued-colored button, while observing a virtual hand moving in the same or in the opposite direction-i.e., movement-related prediction error-and pressing the selected or a different color-i.e., goal-related prediction error. To investigate implicit and explicit components of SoA, we collected indirect (i.e., Synchrony Judgments) and direct (i.e., Judgments of Causation) measures. We found that participants judged virtual actions as more synchronous when they were free to act. Additionally, movement-related prediction errors reduced both perceived synchrony and judgments of causation, while goal-related prediction errors impaired exclusively the latter. Our results suggest that freedom to act enhances SoA and that movement and goal-related prediction errors lead to an equivalent reduction of SoA in free and cued actions. Our results also show that the influence of freedom to act and goal achievement may be limited, respectively, to implicit and explicit SoA, while movement information may affect both components. These findings provide support to recent theories that view SoA as a multifaceted construct, by showing that different action cues may uniquely influence the feeling of control.

Error, rather than its probability, elicits specific electrocortical signatures: a combined EEG-immersive virtual reality study of action observation.

Detecting errors in one's own actions, and in the actions of others, is a crucial ability for adaptable and flexible behavior. Studies show that specific EEG signatures underpin the monitoring of observed erroneous actions (error-related negativity, error positivity, mid-frontal theta oscillations). However, the majority of studies on action observation used sequences of trials where erroneous actions were less frequent than correct actions. Therefore, it was not possible to disentangle whether the activation of the performance monitoring system was due to an error, as a violation of the intended goal, or to a surprise/novelty effect, associated with a rare and unexpected event. Combining EEG and immersive virtual reality (IVR-CAVE system), we recorded the neural signal of 25 young adults who observed, in first-person perspective, simple reach-to-grasp actions performed by an avatar aiming for a glass. Importantly, the proportion of erroneous actions was higher than correct actions. Results showed that the observation of erroneous actions elicits the typical electrocortical signatures of error monitoring, and therefore the violation of the action goal is still perceived as a salient event. The observation of correct actions elicited stronger alpha suppression. This confirmed the role of the alpha-frequency band in the general orienting response to novel and infrequent stimuli. Our data provide novel evidence that an observed goal error (the action slip) triggers the activity of the performance-monitoring system even when erroneous actions, which are, typically, relevant events, occur more often than correct actions and thus are not salient because of their rarity. NEW & NOTEWORTHY Activation of the performance-monitoring system (PMS) is typically investigated when errors in a sequence are comparatively rare. However, whether the PMS is activated by errors per se or by their infrequency is not known. Combining EEG-virtual reality techniques, we found that observing frequent (70%) action errors performed by avatars elicits electrocortical error signatures suggesting that deviation from the prediction of how learned actions should correctly deploy, rather than its frequency, is coded in the PMS.

Violation of expectations about movement and goal achievement leads to Sense of Agency reduction.

The control of one's own movements and of their impact on the external world generates a feeling of control referred to as Sense of Agency (SoA). SoA is experienced when actions match predictions and is reduced by unpredicted events. The present study investigated the contribution of monitoring two fundamental components of action-movement execution and goal achievement-that have been most often explored separately in previous research. We have devised a new paradigm in which participants performed goal-directed actions while viewing an avatar's hand in a mixed-reality scenario. The hand performed either the same action or a different one, simultaneously or after various delays. Movement of the virtual finger and goal attainment were manipulated, so that they could match or conflict with the participants' expectations. We collected judgments of correspondence (an explicit index of SoA that overcomes the tendency to over-attribute actions to oneself) by asking participants if the observed action was synchronous or not with their action. In keeping with previous studies, we found that monitoring both movement execution and goal attainment is relevant for SoA. Moreover, we expanded previous findings by showing that movement information may be a more constant source of SoA modulation than goal information. Indeed, an incongruent movement impaired SoA irrespective of delay duration, while a missed goal did so only when delays were short. Our novel paradigm allowed us to simultaneously manipulate multiple action features, a characteristic that makes it suitable for investigating the contribution of different sub-components of action in modulating SoA in healthy and clinical populations.

Boosting and Decreasing Action Prediction Abilities Through Excitatory and Inhibitory tDCS of Inferior Frontal Cortex.

Influential theories suggest that humans predict others' upcoming actions by using their own motor system as an internal forward model. However, evidence that the motor system is causally essential for predicting others' actions is meager. Using transcranial direct current stimulation (tDCS), we tested the role of the inferior frontal cortex (IFC), in action prediction (AP). We devised a novel AP task where participants observed the initial phases of right-hand reaching-to-grasp actions and had to predict their outcome (i.e., the goal/object to be grasped). We found that suppression by cathodal (inhibitory) tDCS of the left IFC, but not the left superior temporal sulcus or the right IFC, selectively impaired performance on the AP task, but not on a difficulty-matched control task. Remarkably, anodal (excitatory) tDCS of the left IFC brought about a selective improvement in the AP task. These findings indicate that the left IFC is necessary for predicting the outcomes of observed human right-hand actions. Crucially, our study shows for the first time that down- and up-regulating excitability within the motor system can hinder and enhance AP abilities, respectively. These findings support predictive coding theories of action perception and have implications for enhancement of AP abilities.

Primary somatosensory cortex necessary for the perception of weight from other people's action: A continuous theta-burst TMS experiment.

The presence of a network of areas in the parietal and premotor cortices, which are active both during action execution and observation, suggests that we might understand the actions of other people by activating those motor programs for making similar actions. Although neurophysiological and imaging studies show an involvement of the somatosensory cortex (SI) during action observation and execution, it is unclear whether SI is essential for understanding the somatosensory aspects of observed actions. To address this issue, we used off-line transcranial magnetic continuous theta-burst stimulation (cTBS) just before a weight judgment task. Participants observed the right hand of an actor lifting a box and estimated its relative weight. In counterbalanced sessions, we delivered sham and active cTBS over the hand region of the left SI and, to test anatomical specificity, over the left motor cortex (M1) and the left superior parietal lobule (SPL). Active cTBS over SI, but not over M1 or SPL, impaired task performance relative to sham cTBS. Moreover, active cTBS delivered over SI just before participants were asked to evaluate the weight of a bouncing ball did not alter performance compared to sham cTBS. These findings indicate that SI is critical for extracting somatosensory features (heavy/light) from observed action kinematics and suggest a prominent role of SI in action understanding.

The Role of Audio-Visual Feedback in a Thought-Based Control of a Humanoid Robot: A BCI Study in Healthy and Spinal Cord Injured People.

The efficient control of our body and successful interaction with the environment are possible through the integration of multisensory information. Brain-computer interface (BCI) may allow people with sensorimotor disorders to actively interact in the world. In this study, visual information was paired with auditory feedback to improve the BCI control of a humanoid surrogate. Healthy and spinal cord injured (SCI) people were asked to embody a humanoid robot and complete a pick-and-place task by means of a visual evoked potentials BCI system. Participants observed the remote environment from the robot's perspective through a head mounted display. Human-footsteps and computer-beep sounds were used as synchronous/asynchronous auditory feedback. Healthy participants achieved better placing accuracy when listening to human footstep sounds relative to a computer-generated sound. SCI people demonstrated more difficulty in steering the robot during asynchronous auditory feedback conditions. Importantly, subjective reports highlighted that the BCI mask overlaying the display did not limit the observation of the scenario and the feeling of being in control of the robot. Overall, the data seem to suggest that sensorimotor-related information may improve the control of external devices. Further studies are required to understand how the contribution of residual sensory channels could improve the reliability of BCI systems.

Local and Remote Cooperation With Virtual and Robotic Agents: A P300 BCI Study in Healthy and People Living With Spinal Cord Injury.

The development of technological applications that allow people to control and embody external devices within social interaction settings represents a major goal for current and future brain-computer interface (BCI) systems. Prior research has suggested that embodied systems may ameliorate BCI end-user's experience and accuracy in controlling external devices. Along these lines, we developed an immersive P300-based BCI application with a head-mounted display for virtual-local and robotic-remote social interactions and explored in a group of healthy participants the role of proprioceptive feedback in the control of a virtual surrogate (Study 1). Moreover, we compared the performance of a small group of people with spinal cord injury (SCI) to a control group of healthy subjects during virtual and robotic social interactions (Study 2), where both groups received a proprioceptive stimulation. Our attempt to combine immersive environments, BCI technologies and neuroscience of body ownership suggests that providing realistic multisensory feedback still represents a challenge. Results have shown that healthy and people living with SCI used the BCI within the immersive scenarios with good levels of performance (as indexed by task accuracy, optimizations calls and Information Transfer Rate) and perceived control of the surrogates. Proprioceptive feedback did not contribute to alter performance measures and body ownership sensations. Further studies are necessary to test whether sensorimotor experience represents an opportunity to improve the use of future embodied BCI applications.

Sensorimotor Network Crucial for Inferring Amusement from Smiles.

Understanding whether another's smile reflects authentic amusement is a key challenge in social life, yet, the neural bases of this ability have been largely unexplored. Here, we combined transcranial magnetic stimulation (TMS) with a novel empathic accuracy (EA) task to test whether sensorimotor and mentalizing networks are critical for understanding another's amusement. Participants were presented with dynamic displays of smiles and explicitly requested to infer whether the smiling individual was feeling authentic amusement or not. TMS over sensorimotor regions representing the face (i.e., in the inferior frontal gyrus (IFG) and ventral primary somatosensory cortex (SI)), disrupted the ability to infer amusement authenticity from observed smiles. The same stimulation did not affect performance on a nonsocial task requiring participants to track the smiling expression but not to infer amusement. Neither TMS over prefrontal and temporo-parietal areas supporting mentalizing, nor peripheral control stimulations, affected performance on either task. Thus, motor and somatosensory circuits for controlling and sensing facial movements are causally essential for inferring amusement from another's smile. These findings highlight the functional relevance of IFG and SI to amusement understanding and suggest that EA abilities may be grounded in sensorimotor networks for moving and feeling the body.

Apparent Biological Motion in First and Third Person Perspective.

Apparent biological motion is the perception of plausible movements when two alternating images depicting the initial and final phase of an action are presented at specific stimulus onset asynchronies. Here, we show lower subjective apparent biological motion perception when actions are observed from a first relative to a third visual perspective. These findings are discussed within the context of sensorimotor contributions to body ownership.

Illusion of arm movement evoked by tendon vibration in patients with spinal cord injury.

BACKGROUND: Studies in healthy people show that stimulation of muscle spindles through frequency-specific tendon vibration (TV) induces the illusory perception of movement. Following spinal cord injury (SCI), motor and sensory connections between the brain and parts of the body below-the-lesion level are partially or totally impaired. OBJECTIVE: The present investigation is a descriptive study aimed to investigate whether people living with SCI may experience movement illusions comparable to a control group. METHODS: Healthy and people with SCI were asked to report on three illusion-related features (Vividness, Duration, Illusory Extension) after receiving 70 Hz TV on the biceps brachii tendon of both arms. Two different forces of stimulation were applied: 2.4 N and 4.2 N. RESULTS: Both patients and controls were susceptible to the kinesthetic illusion. However patients presented lower sensitivity to TV than healthy subjects. Participants rated stronger illusions of movement after 4.2 N than 2.4 N stimulation in all the three illusion-related features. Further, patients reported atypical illusory experiences of movement (e.g. as if the arm wanted to extend, or a sensation of pushing against something) that may reflect different reorganization processes following spinal cord injury. CONCLUSION: The study provides a preliminary evidence of the possible use of the proprioceptive stimulation in the upper limbs of people living with SCI. Results are discussed in the light of recent advancements of brain-computer applications based on motor imagery for the control of neuroprosthetic and robotic devices in patients with severe sensorimotor deficits.

Embodying Others in Immersive Virtual Reality: Electro-Cortical Signatures of Monitoring the Errors in the Actions of an Avatar Seen from a First-Person Perspective.

Brain monitoring of errors in one's own and other's actions is crucial for a variety of processes, ranging from the fine-tuning of motor skill learning to important social functions, such as reading out and anticipating the intentions of others. Here, we combined immersive virtual reality and EEG recording to explore whether embodying the errors of an avatar by seeing it from a first-person perspective may activate the error monitoring system in the brain of an onlooker. We asked healthy participants to observe, from a first- or third-person perspective, an avatar performing a correct or an incorrect reach-to-grasp movement toward one of two virtual mugs placed on a table. At the end of each trial, participants reported verbally how much they embodied the avatar's arm. Ratings were maximal in first-person perspective, indicating that immersive virtual reality can be a powerful tool to induce embodiment of an artificial agent, even through mere visual perception and in the absence of any cross-modal boosting. Observation of erroneous grasping from a first-person perspective enhanced error-related negativity and medial-frontal theta power in the trials where human onlookers embodied the virtual character, hinting at the tight link between early, automatic coding of error detection and sense of embodiment. Error positivity was similar in 1PP and 3PP, suggesting that conscious coding of errors is similar for self and other. Thus, embodiment plays an important role in activating specific components of the action monitoring system when others' errors are coded as if they are one's own errors. SIGNIFICANCE STATEMENT: Detecting errors in other's actions is crucial for social functions, such as reading out and anticipating the intentions of others. Using immersive virtual reality and EEG recording, we explored how the brain of an onlooker reacted to the errors of an avatar seen from a first-person perspective. We found that mere observation of erroneous actions enhances electrocortical markers of error detection in the trials where human onlookers embodied the virtual character. Thus, the cerebral system for action monitoring is maximally activated when others' errors are coded as if they are one's own errors. The results have important implications for understanding how the brain can control the external world and thus creating new brain-computer interfaces.

Body visual discontinuity affects feeling of ownership and skin conductance responses.

When we look at our hands we are immediately aware that they belong to us and we rarely doubt about the integrity, continuity and sense of ownership of our bodies. Here we explored whether the mere manipulation of the visual appearance of a virtual limb could influence the subjective feeling of ownership and the physiological responses (Skin Conductance Responses, SCRs) associated to a threatening stimulus approaching the virtual hand. Participants observed in first person perspective a virtual body having the right hand-forearm (i) connected by a normal wrist (Full-Limb) or a thin rigid wire connection (Wire) or (ii) disconnected because of a missing wrist (m-Wrist) or a missing wrist plus a plexiglass panel positioned between the hand and the forearm (Plexiglass). While the analysis of subjective ratings revealed that only the observation of natural full connected virtual limb elicited high levels of ownership, high amplitudes of SCRs were found also during observation of the non-natural, rigid wire connection condition. This result suggests that the conscious embodiment of an artificial limb requires a natural looking visual body appearance while implicit reactivity to threat may require physical body continuity, even non-naturally looking, that allows the implementation of protective reactions to threat.

Illusory movements induced by tendon vibration in right- and left-handed people.

Frequency-specific vibratory stimulation of peripheral tendons induces an illusion of limb movement that may be useful for restoring proprioceptive information in people with sensorimotor disability. This potential application may be limited by inter- and intra-subject variability in the susceptibility to such an illusion, which may depend on a variety of factors. To explore the influence of stimulation parameters and participants' handedness on the movement illusion, we vibrated the right and left tendon of the biceps brachii in a group of right- and left-handed people with five stimulation frequencies (from 40 to 120 Hz in step of 20 Hz). We found that all participants reported the expected illusion of elbow extension, especially after 40 and 60 Hz. Left-handers exhibited less variability in reporting the illusion compared to right-handers across the different stimulation frequencies. Moreover, the stimulation of the non-dominant arm elicited a more vivid illusion with faster onset relative to the stimulation of the dominant arm, an effect that was independent from participants' handedness. Overall, our data show that stimulation frequency, handedness and arm dominance influence the tendon vibration movement illusion. The results are discussed in reference to their relevance in linking motor awareness, improving current devices for motor ability recovery after brain or spinal damage and developing prosthetics and virtual embodiment systems.

Rubber hand illusion highlights massive visual capture and sensorimotor face-hand remapping in a tetraplegic man.

PURPOSE: The illusory ownership of a fake hand as part the body follows synchronous tactile stimulation over a visible rubber hand and a covered hand. Whether brain plasticity mechanisms after sensory and motor disconnection modulates this illusion remain unexplored. METHODS: We tested a tetraplegic man after synchronous and asynchronous stimulation of the hand and face. RESULTS: The illusory ownership of the fake hand was tested four times in separate days and always reported. To verify whether this ownership feeling generalized also to object not resembling the human body we tested this illusion with a plastic bottle and a rubber hand. The illusionary perception of owning an external object using the rubber hand paradigm showed that the temporally matched tactile stimulation on a fake hand and visual capture mechanism create the illusionary feeling that the rubber hand was part of his body. CONCLUSIONS: Despite lesions that dramatically disconnect the access to sensory inputs and motor outputs our data suggests a strong visual capture of a rubber hand and a possible remapping of hand-face representations after the spinal lesion. We suggest that vision and brain plasticity may represent a supportive tool for motor rehabilitation in patients with sensory deficits.

Audio-visual feedback improves the BCI performance in the navigational control of a humanoid robot.

Advancement in brain computer interfaces (BCI) technology allows people to actively interact in the world through surrogates. Controlling real humanoid robots using BCI as intuitively as we control our body represents a challenge for current research in robotics and neuroscience. In order to successfully interact with the environment the brain integrates multiple sensory cues to form a coherent representation of the world. Cognitive neuroscience studies demonstrate that multisensory integration may imply a gain with respect to a single modality and ultimately improve the overall sensorimotor performance. For example, reactivity to simultaneous visual and auditory stimuli may be higher than to the sum of the same stimuli delivered in isolation or in temporal sequence. Yet, knowledge about whether audio-visual integration may improve the control of a surrogate is meager. To explore this issue, we provided human footstep sounds as audio feedback to BCI users while controlling a humanoid robot. Participants were asked to steer their robot surrogate and perform a pick-and-place task through BCI-SSVEPs. We found that audio-visual synchrony between footsteps sound and actual humanoid's walk reduces the time required for steering the robot. Thus, auditory feedback congruent with the humanoid actions may improve motor decisions of the BCI's user and help in the feeling of control over it. Our results shed light on the possibility to increase robot's control through the combination of multisensory feedback to a BCI user.

Rubber hand illusion induced by touching the face ipsilaterally to a deprived hand: evidence for plastic "somatotopic" remapping in tetraplegics.

BACKGROUND: Studies in animals and humans indicate that the interruption of body-brain connections following spinal cord injury (SCI) leads to plastic cerebral reorganization. OBJECTIVE: To explore whether inducing the Rubber Hand Illusion (RHI) via synchronous multisensory visuo-tactile bodily stimulation may reveal any perceptual correlates of plastic remapping in SCI. METHODS: In 16 paraplegic, 16 tetraplegic and 16 healthy participants we explored whether RHI may be induced by tactile stimuli involving not only the left hand but also the left hemi-face. Touching the participants actual hand or face was either synchronous or asynchronous with tactile stimuli seen on a rubber hand. We assessed two components of the illusion, namely perceived changes in the real hand in space (indexed by proprioceptive drift) and ownership of the rubber hand (indexed by subjective responses to an ad-hoc questionnaire). RESULTS: Proprioceptive drift and ownership were found in the healthy group only in the condition where the left real and fake hand were touched simultaneously. In contrast, no drift was found in the SCI patients who, however, showed ownership after both synchronous and asynchronous hand stroking. Importantly, only tetraplegics showed the effect also after synchronous face stroking. CONCLUSIONS: RHI may reveal plastic phenomena in SCI. In hand representation-deprived tetraplegics, stimuli on the face (represented contiguously in the somatic and motor systems), drive the sense of hand ownership. This hand-face remapping phenomenon may be useful for restoring a sense of self in massively deprived individuals.