Three-stage Dynamic Brain-cognitive Model of Understanding Action Intention Displayed by Human Body Movements.

The ability to comprehend the intention conveyed through human body movements is crucial for effective interpersonal interactions. If people can't understand the intention behind other individuals' isolated or interactive actions, their actions will become meaningless. Psychologists have investigated the cognitive processes and neural representations involved in understanding action intention, yet a cohesive theoretical explanation remains elusive. Hence, we mainly review existing literature related to neural correlates of action intention, and primarily propose a putative Three-stage Dynamic Brain-cognitive Model of understanding action intention, which involves body perception, action identification and intention understanding. Specifically, at the first stage, body parts/shapes are processed by those brain regions such as extrastriate and fusiform body areas; During the second stage, differentiating observed actions relies on configuring relationships between body parts, facilitated by the activation of the Mirror Neuron System; The last stage involves identifying various intention categories, utilizing the Mentalizing System for recruitment, and different activation patterns concerning the nature of the intentions participants dealing with. Finally, we delves into the clinical practice, like intervention training based on a theoretical model for individuals with autism spectrum disorders who encounter difficulties in interpersonal communication.

Acting with shared intentions: A systematic review on joint action coordination in Autism Spectrum Disorder.

BACKGROUND: Joint actions, described as a form of social interaction in which individuals coordinate their actions in space and time to bring about a change in the environment, rely on sensory-motor processes that play a role in the development of social skills. Two brain networks, associated with "mirroring" and "mentalizing", are engaged during these actions: the mirror neuron and the theory of mind systems. People with autism spectrum disorder (ASD) showed impairment in interpersonal coordination during joint actions. Studying joint action coordination in ASD will contribute to clarify the interplay between sensory-motor and social processes throughout development and the interactions between the brain and the behavior. METHOD: This review focused on empirical studies that reported behavioral and kinematic findings related to joint action coordination in people with ASD. RESULTS: Literature on mechanisms involved in the joint action coordination impairment in ASD is still limited. Data are controversial. Different key-components of joint action coordination may be impaired, such as cooperative behavior, temporal coordination, and motor planning. CONCLUSIONS: Interpersonal coordination during joint actions relies on early sensory-motor processes that have a key role in guiding social development. Early intervention targeting the sensory-motor processes involved in the development of joint action coordination could positively support social skills.

Distinct functional roles of the mirror neuron system and the mentalizing system.

Movements can inform us about what people are doing and also about how they feel. This phenomenologically evident distinction has been suggested to correspond functionally with differential neural correlates denoted as mirror neuron system (MNS) and mentalizing system (MENT). To separate out the roles of the underlying systems we presented identical stimuli under different task demands: character animations showing everyday activities (mopping, sweeping) performed in different moods (angry, happy). Thirty-two participants were undergoing functional magnetic resonance imaging (fMRI) while asked to identify either the performed movement or the displayed mood. Univariate GLM analysis revealed the expected activation of either in MNS or MENT depending on the task. A complementary multivariate pattern-learning analysis based on the "social brain atlas" confirmed the expected recruitment of both systems. In conclusion, both approaches converge onto clearly distinct functional roles of both social neural networks in a novel dynamic social perception paradigm.

Affective and cooperative social interactions modulate effective connectivity within and between the mirror and mentalizing systems.

Decoding the meaning of others' actions, a crucial step for social cognition, involves different neural mechanisms. While the "mirror" and "mentalizing" systems have been associated with, respectively, the processing of biological actions versus more abstract information, their respective contribution to intention understanding is debated. Processing social interactions seems to recruit both neural systems, with a different weight depending on cues emphasizing either shared action goals or shared mental states. We have previously shown that observing cooperative and affective social interactions elicits stronger activity in key nodes of, respectively, the mirror (left posterior superior temporal sulcus (pSTS), superior parietal cortex (SPL), and ventral/dorsal premotor cortex (vPMC/dPMC)) and mentalizing (ventromedial prefrontal cortex (vmPFC)) systems. To unveil their causal organization, we investigated the effective connectivity underlying the observation of human social interactions expressing increasing cooperativity (involving left pSTS, SPL, and vPMC) versus affectivity (vmPFC) via dynamic causal modeling in 36 healthy human subjects. We found strong evidence for a model including the pSTS and vPMC as input nodes for the observed interactions. The extrinsic connectivity of this model undergoes oppositely valenced modulations, with cooperativity promoting positive modulations of connectivity between pSTS and both SPL (forward) and vPMC (mainly backward), and affectivity promoting reciprocal positive modulations of connectivity between pSTS and vmPFC (mainly backward). Alongside fMRI data, such divergent effective connectivity suggests that different dimensions underlying the processing of social interactions recruit distinct, although strongly interconnected, neural pathways associated with, respectively, the bottom-up visuomotor processing of motor intentions, and the top-down attribution of affective/mental states.

Inferring a dual-stream model of mentalizing from associative white matter fibres disconnection.

In the field of cognitive neuroscience, it is increasingly accepted that mentalizing is subserved by a complex frontotemporoparietal cortical network. Some researchers consider that this network can be divided into two distinct but interacting subsystems (the mirror system and the mentalizing system per se), which respectively process low-level, perceptive-based aspects and high-level, inference-based aspects of this sociocognitive function. However, evidence for this type of functional dissociation in a given neuropsychological population is currently lacking and the structural connectivities of the two mentalizing subnetworks have not been established. Here, we studied mentalizing in a large sample of patients (n = 93; 46 females; age range: 18-65 years) who had been resected for diffuse low-grade glioma-a rare tumour that migrates preferentially along associative white matter pathways. This neurological disorder constitutes an ideal pathophysiological model in which to study the functional anatomy of associative pathways. We mapped the location of each patient's resection cavity and residual lesion infiltration onto the Montreal Neurological Institute template brain and then performed multilevel lesion analyses (including conventional voxel-based lesion-symptom mapping and subtraction lesion analyses). Importantly, we estimated each associative pathway's degree of disconnection (i.e. the degree of lesion infiltration) and built specific hypotheses concerning the connective anatomy of the mentalizing subnetworks. As expected, we found that impairments in mentalizing were mainly related to the disruption of right frontoparietal connectivity. More specifically, low-level and high-level mentalizing accuracy were correlated with the degree of disconnection in the arcuate fasciculus and the cingulum, respectively. To the best of our knowledge, our findings constitute the first experimental data on the structural connectivity of the mentalizing network and suggest the existence of a dual-stream hodological system. Our results may lead to a better understanding of disorders that affect social cognition, especially in neuropathological conditions characterized by atypical/aberrant structural connectivity, such as autism spectrum disorders.

Imagining triadic interactions simultaneously activates mirror and mentalizing systems.

Coordinated triadic interactions, involving oneself, another person, and an external object, are considered a uniquely human skill. However, the exact mechanisms underlying the ability to engage in such social interactions remain hitherto unknown. We used functional neuroimaging to investigate the neural signature of triadic interactions. For this purpose, participants viewed pictures of objects in a 3T functional magnetic resonance imaging scanner and were asked whether they could imagine this object in a social interaction with another person. We also aimed to dissociate this process from, as well as to find commonalities with, purely self-referential or other-referential processing. In all trial-types, we found activations in core mentalizing brain areas (medial prefrontal cortex, posterior cingulate cortex, precuneus and temporoparietal junction). Furthermore, triadic engagements, but not self-referential or other-referential processing, were associated with activations in classical mirror neuron areas (inferior frontal gyrus and inferior parietal lobe). Finally, mentalizing networks showed a strong functional connectivity with mirror neuron areas exclusively during triadic engagements. These results suggest that the imagined interaction of two agents is processed in a more complex neural social cognitive network than purely self- or other-referential considerations.

Online chasing action recruits both mirror neuron and mentalizing systems: A pilot fNIRS study.

Engaging in chasing, where an actor actively pursues a target, is considered a crucial activity for the development of social skills. Previous studies have focused predominantly on understanding the neural correlates of chasing from an observer's perspective, but the neural mechanisms underlying the real-time implementation of chasing action remain poorly understood. To gain deeper insights into this phenomenon, the current study employed functional near-infrared spectroscopy (fNIRS) techniques and a novel interactive game. In this interactive game, participants (N = 29) were tasked to engage in chasing behavior by controlling an on-screen character using a gamepad, with the goal of catching a virtual partner. To specifically examine the brain activations associated with the interactive nature of chasing, we included two additional interactive actions: following action of following the path of a virtual partner and free action of moving without a specific pursuit goal. The results revealed that chasing and following actions elicited activation in a broad and overlapping network of brain regions, including the temporoparietal junction (TPJ), medial prefrontal cortex (mPFC), premotor cortex (PMC), primary somatosensory cortex (SI), and primary motor cortex (M1). Crucially, these regions were found to be modulated by the type of interaction, with greater activation and functional connectivity during the chasing interaction than during the following and free interactions. These findings suggested that both the MNS, encompassing regions such as the PMC, M1 and SI, and the mentalizing system (MS), involving the TPJ and mPFC, contribute to the execution of online chasing actions. Thus, the present study represents an initial step toward future investigations into the roles of MNS and MS in real-time chasing interactions.

Differential role of the Mentalizing and the Mirror Neuron system in the imitation of communicative gestures.

Successful social interaction requires recognising the intention of another person's communicative gestures. At a neural level, this process may involve neural activity in different systems, such as the mentalizing system (MS) and the mirror neuron system (MNS). The aim of the present study was to explore the neural correlates of communicative gestures during observation and execution of these gestures. Twenty participants watched video clips of an actor executing social gestures (S), non-social gestures (NS) and meaningless gestures (ML). During fMRI data acquisition, participants were asked to observe (O) and subsequently to execute (E) one of two tasks: imitate the gesture presented (IMI) or perform a motor control task (CT). For the contrast IMI>CT we found activations in the core areas of the MNS [inferior parietal lobule (IPL) and inferior frontal cortex, the posterior part of pars opercularis], as well as in areas related to the MS [superior temporal sulcus (STS) and middle cingulate cortex]. For S>NS, we found activations in the left medial orbitofrontal cortex (mOFC), right superior frontal cortex and middle cingulate cortex. The interaction of stimulus condition (S vs NS) and task (IMI vs CT) revealed activation in the right IPL. For the interaction between observation vs execution (O vs E), task (IMI vs CT) and stimulus condition (S vs NS) we found activation in the right mOFC. Our data suggest that imitation is differentially processed in the MNS as well as in the MS. The activation in IPL is enhanced during the processing of social gestures most likely due to their communicative intention. The activation of IPL together with medial frontal areas may contribute to mentalizing processes. The interaction in the mOFC suggests an involvement of self-referential processes in the processing of social gesture.

Rehabilitation of Severe Impairment in Motor Function after Stroke: Suggestions for Harnessing the Potentials of Mirror Neurons and the Mentalizing Systems to Stimulate Recovery.

Rehabilitation of severe impairment in motor function following stroke is very challenging. This is because one of the driving forces for recovery of motor function is tasks practice, something this category of patients cannot voluntarily perform. However, it has now been shown that tasks practice can equally be carried out cognitively and through observation of another person's practice, using techniques known as mental practice and tasks observation, respectively. Mental practice and tasks observation are believed to activate networks of neurons in the brain known as mirror neurons and mentalizing systems to induce recovery. The effectiveness of these techniques has, however, limited evidence at the moment. One possible explanation for this could be the nature of the protocols of these techniques, especially as regards to the intensity of practice. This article proposes ways the potentials of the mirror neurons and mentalizing systems can be harnessed to optimize recovery of severe impairment in motor function using mental practice and tasks observation. The article suggests, among other ways, protocols where tasks observation or mirror therapy are carried out first, and are then followed by mental practice, increasing the number of times the tasks are observed or mentalized, observation of significant others performing the tasks and mental practice of very familiar tasks.

Weighted Brain Network Metrics for Decoding Action Intention Understanding Based on EEG.

Background: Understanding the action intentions of others is important for social and human-robot interactions. Recently, many state-of-the-art approaches have been proposed for decoding action intention understanding. Although these methods have some advantages, it is still necessary to design other tools that can more efficiently classify the action intention understanding signals. New Method: Based on EEG, we first applied phase lag index (PLI) and weighted phase lag index (WPLI) to construct functional connectivity matrices in five frequency bands and 63 micro-time windows, then calculated nine graph metrics from these matrices and subsequently used the network metrics as features to classify different brain signals related to action intention understanding. Results: Compared with the single methods (PLI or WPLI), the combination method (PLI+WPLI) demonstrates some overwhelming victories. Most of the average classification accuracies exceed 70%, and some of them approach 80%. In statistical tests of brain network, many significantly different edges appear in the frontal, occipital, parietal, and temporal regions. Conclusions: Weighted brain networks can effectively retain data information. The integrated method proposed in this study is extremely effective for investigating action intention understanding. Both the mirror neuron and mentalizing systems participate as collaborators in the process of action intention understanding.

Different aberrant mentalizing networks in males and females with autism spectrum disorders: Evidence from resting-state functional magnetic resonance imaging.

Previous studies have found that individuals with autism spectrum disorders show impairments in mentalizing processes and aberrant brain activity compared with typically developing participants. However, the findings are mainly from male participants and the aberrant effects in autism spectrum disorder females and sex differences are still unclear. To address these issues, this study analyzed intrinsic functional connectivity of mentalizing regions using resting-state functional magnetic resonance imaging data of 48 autism spectrum disorder males and females and 48 typically developing participants in autism brain imaging data exchange. Whole-brain analyses showed that autism spectrum disorder males had hyperconnectivity in functional connectivity of the bilateral temporal-parietal junction, whereas autism spectrum disorder females showed hypoconnectivity in functional connectivity of the medial prefrontal cortex, precuneus, and right temporal-parietal junction. Interaction between sex and autism was found in both short- and long-distance functional connectivity effects, confirming that autism spectrum disorder males showed overconnectivity, while autism spectrum disorder females showed underconnectivity. Furthermore, a regression analysis revealed that in autism spectrum disorder, males and females demonstrated different relations between the functional connectivity effects of the mentalizing regions and the core autism spectrum disorder deficits. These results suggest sex differences in the mentalizing network in autism spectrum disorder individuals. Future work is needed to examine how sex interacts with other factors such as age and the sex differences during mentalizing task performance.

Two social brains: neural mechanisms of intersubjectivity.

It is the aim of this article to present an empirically justified hypothesis about the functional roles of the two social neural systems, namely the so-called 'mirror neuron system' (MNS) and the 'mentalizing system' (MENT, also 'theory of mind network' or 'social neural network'). Both systems are recruited during cognitive processes that are either related to interaction or communication with other conspecifics, thereby constituting intersubjectivity. The hypothesis is developed in the following steps: first, the fundamental distinction that we make between persons and things is introduced; second, communication is presented as the key process that allows us to interact with others; third, the capacity to 'mentalize' or to understand the inner experience of others is emphasized as the fundamental cognitive capacity required to establish successful communication. On this background, it is proposed that MNS serves comparably early stages of social information processing related to the 'detection' of spatial or bodily signals, whereas MENT is recruited during comparably late stages of social information processing related to the 'evaluation' of emotional and psychological states of others. This hypothesis of MNS as a social detection system and MENT as a social evaluation system is illustrated by findings in the field of psychopathology. Finally, new research questions that can be derived from this hypothesis are discussed.This article is part of the themed issue 'Physiological determinants of social behaviour in animals'.

Understanding intentional actions from observers' viewpoints: A social neuroscience perspective.

When we see others, we also try to 'see' their unobservable states of minds, such as beliefs, desires, and intentions. We carefully monitor others' actions, as we assume that those actions are outward manifestations of their internal states. Actors and observers can have divergent views on the cause of the same actions. Critically, it is often the observers' view that affects important decisions in social life, from deciding the optimal level of cooperation to judging moral responsibility and court's decisions. Thus, the judgment about intentionality and agency in others' actions determines the way in which the observer deals with the actor. The primate brain has two separate neural systems that function in understanding others' actions and intentions. The mirror system is activated by others' visible actions and predicts their physical consequences in goal terms, whereas the mentalizing system is primarily involved in the prediction of others' intentions and upcoming actions regardless of whether others' actions are directly observable or not. The functional roles of the two systems have sometimes been described as mutually independent or even oppositional. I propose a hypothesis that the two systems may collaborate closely for judging the sense of other-agency.