Spike-timing-dependent plasticity induction reveals dissociable supplementary- and premotor-motor pathways to automatic imitation.

Humans tend to spontaneously imitate others' behavior, even when detrimental to the task at hand. The action observation network (AON) is consistently recruited during imitative tasks. However, whether automatic imitation is mediated by cortico-cortical projections from AON regions to the primary motor cortex (M1) remains speculative. Similarly, the potentially dissociable role of AON-to-M1 pathways involving the ventral premotor cortex (PMv) or supplementary motor area (SMA) in automatic imitation is unclear. Here, we used cortico-cortical paired associative stimulation (ccPAS) to enhance or hinder effective connectivity in PMv-to-M1 and SMA-to-M1 pathways via Hebbian spike-timing-dependent plasticity (STDP) to test their functional relevance to automatic and voluntary motor imitation. ccPAS affected behavior under competition between task rules and prepotent visuomotor associations underpinning automatic imitation. Critically, we found dissociable effects of manipulating the strength of the two pathways. While strengthening PMv-to-M1 projections enhanced automatic imitation, weakening them hindered it. On the other hand, strengthening SMA-to-M1 projections reduced automatic imitation but also reduced interference from task-irrelevant cues during voluntary imitation. Our study demonstrates that driving Hebbian STDP in AON-to-M1 projections induces opposite effects on automatic imitation that depend on the targeted pathway. Our results provide direct causal evidence of the functional role of PMv-to-M1 projections for automatic imitation, seemingly involved in spontaneously mirroring observed actions and facilitating the tendency to imitate them. Moreover, our findings support the notion that SMA exerts an opposite gating function, controlling M1 to prevent overt motor behavior when inadequate to the context.

Transcranial cortico-cortical paired associative stimulation (ccPAS) over ventral premotor-motor pathways enhances action performance and corticomotor excitability in young adults more than in elderly adults.

Transcranial magnetic stimulation (TMS) methods such as cortico-cortical paired associative stimulation (ccPAS) can increase the strength of functional connectivity between ventral premotor cortex (PMv) and primary motor cortex (M1) via spike timing-dependent plasticity (STDP), leading to enhanced motor functions in young adults. However, whether this STDP-inducing protocol is effective in the aging brain remains unclear. In two groups of young and elderly healthy adults, we evaluated manual dexterity with the 9-hole peg task before and after ccPAS of the left PMv-M1 circuit. We observed that ccPAS enhanced dexterity in young adults, and this effect was anticipated by a progressive increase in motor-evoked potentials (MEPs) during ccPAS administration. No similar effects were observed in elderly individuals or in a control task. Across age groups, we observed that the magnitude of MEP changes predicted larger behavioral improvements. These findings demonstrate that left PMv-to-M1 ccPAS induces functionally specific improvements in young adults' manual dexterity and an increase in corticomotor excitability, but altered plasticity prevents the effectiveness of ccPAS in the elderly.

The dopaminergic system supports flexible and rewarding dyadic motor interactive behaviour in Parkinson's Disease.

Studies indicate that the dopaminergic system (DAS) supports individual flexible behaviour. While flexibility is quintessential to effective dyadic motor interactions, whether DAS mediates adaptations of one's own motor behaviour to that of a partner is not known. Here, we asked patients with Parkinson's Disease (PD) to synchronize their grasping movements with those of a virtual partner in conditions that did (Interactive) or did not (Cued) require to predict and adapt to its actions. PD performed the task during daily antiparkinsonian treatment ('On' condition) or after drug-withdrawal ('Off' condition). A group of healthy individuals also served as control group. In the Interactive condition, PDs performed better and found the interaction more enjoyable when in 'On' than in 'Off' condition. Crucially, PD performance in the 'On' condition did not differ from that of healthy controls. This pattern of results hints at the key role of the DAS in supporting the flexible adaptation of one's own actions to the partner's during motor interactions.

Mapping the mental space of emotional concepts through kinematic measures of decision uncertainty.

Emotional concepts and their mental representations have been extensively studied. Yet, some ecologically relevant aspects, such as how they are processed in ambiguous contexts (e.g., in relation to other emotional stimuli that share similar characteristics), are incompletely known. We employed a similarity judgement of emotional concepts and manipulated the contextual congruency of the responses along the two main affective dimensions of hedonic valence and physiological activation, respectively. Behavioural and kinematics (mouse-tracking) measures were combined to gather a novel 'similarity index' between emotional concepts, to derive topographical maps of their mental representations. Self-report (interoceptive sensibility, positive-negative affectivity, depression) and physiological measures (heart rate variability, HRV) have been collected to explore their possible association with emotional conceptual representation. Results indicate that emotional concepts typically associated with low arousal profit by contextual congruency, with faster responses and reduced uncertainty when contextual ambiguity decreases. The emotional maps recreate two almost orthogonal axes of valence and arousal, and the similarity measure captures the smooth boundaries between emotions. The emotional map of a subgroup of individuals with low positive affectivity reveals a narrower conceptual distribution, with variations in positive emotions and in individuals with reduced arousal (such as those with reduced HRV). Our work introduces a novel methodology to study emotional conceptual representations, bringing the behavioural dynamics of decision-making processes and choice uncertainty into the affective domain. This article is part of the theme issue 'Concepts in interaction: social engagement and inner experiences'.

The performance monitoring system is attuned to others' actions during dyadic motor interactions.

Interpersonal motor interactions require the simultaneous monitoring of one's own and one's partner's actions. To characterize how the action monitoring system tracks self and other behavior during synchronous interactions, we combined electroencephalography recordings and immersive virtual reality in two tasks where participants were asked to synchronize their actions with those of a virtual partner (VP). The two tasks differed in the features to be monitored: the Goal task required participants to predict and monitor the VP's reaching goal; the Spatial task required participants to predict and monitor the VP's reaching trajectory. In both tasks, the VP performed unexpected movement changes to which the participant needed to adapt. By extracting the neural activity locked to the detection of unexpected changes in the VP's action (other-monitoring) or to the participants' action-replanning (self-monitoring), we show that the monitoring system is more attuned to others' than to one's own actions. Additionally, distinctive neural responses to VP's unexpected goals and trajectory corrections were found: goal changes were reflected both in early fronto-central and later posterior neural responses while trajectory deviations were reflected only in later posterior responses. Altogether, our results indicate that the monitoring system adopts an inherent social mode to handle interpersonal motor interactions.

Midfrontal Theta Transcranial Alternating Current Stimulation Facilitates Motor Coordination in Dyadic Human-Avatar Interactions.

Synchronous interpersonal motor interactions require moment-to-moment prediction and proactive monitoring of the partner's actions. Neurophysiologically, this is highlighted by an enhancement of midfrontal theta (4-7 Hz) oscillations. In this study, we explored the causal role of midfrontal theta for interpersonal motor interactions using transcranial alternating current stimulation (tACS). We implemented a realistic human-avatar interaction task in immersive virtual reality where participants controlled a virtual arm and hand to press a button synchronously with a virtual partner. Participants completed the task while receiving EEG-informed theta (Experiment 1) or beta (control frequency, Experiment 2) tACS over the frontal midline, as well as sham stimulation as a control. Results showed that midfrontal theta tACS significantly improved behavioral performance (i.e., reduced interpersonal asynchrony) and participants' motor strategies (i.e., increased movement times and reduced RTs), whereas beta tACS had no effect on these measures. These results suggest that theta tACS over frontal areas facilitates action monitoring and motor abilities supporting interpersonal interactions.

Somatosensory Evoked Potentials Reveal Reduced Embodiment of Emotions in Autism.

Consistent with current models of embodied emotions, this study investigates whether the somatosensory system shows reduced sensitivity to facial emotional expressions in autistic compared with neurotypical individuals, and whether these differences are independent from between-group differences in visual processing of facial stimuli. To investigate the dynamics of somatosensory activity over and above visual carryover effects, we recorded EEG activity from two groups of autism spectrum disorder (ASD) or typically developing (TD) humans (male and female), while they were performing a facial emotion discrimination task and a control gender task. To probe the state of the somatosensory system during face processing, in 50% of trials we evoked somatosensory activity by delivering task-irrelevant tactile taps on participants' index finger, 105 ms after visual stimulus onset. Importantly, we isolated somatosensory from concurrent visual activity by subtracting visual responses from activity evoked by somatosensory and visual stimuli. Results revealed significant task-dependent group differences in mid-latency components of somatosensory evoked potentials (SEPs). ASD participants showed a selective reduction of SEP amplitudes (P100) compared with TD during emotion task; and TD, but not ASD, showed increased somatosensory responses during emotion compared with gender discrimination. Interestingly, autistic traits, but not alexithymia, significantly predicted SEP amplitudes evoked during emotion, but not gender, task. Importantly, we did not observe the same pattern of group differences in visual responses. Our study provides direct evidence of reduced recruitment of the somatosensory system during emotion discrimination in ASD and suggests that this effect is not a byproduct of differences in visual processing.SIGNIFICANCE STATEMENT The somatosensory system is involved in embodiment of visually presented facial expressions of emotion. Despite autism being characterized by difficulties in emotion-related processing, no studies have addressed whether this extends to embodied representations of others' emotions. By dissociating somatosensory activity from visual evoked potentials, we provide the first evidence of reduced recruitment of the somatosensory system during emotion discrimination in autistic participants, independently from differences in visual processing between typically developing and autism spectrum disorder participants. Our study uses a novel methodology to reveal the neural dynamics underlying difficulties in emotion recognition in autism spectrum disorder and provides direct evidence that embodied simulation of others' emotional expressions operates differently in autistic individuals.

Abstract concepts in interaction: the need of others when guessing abstract concepts smooths dyadic motor interactions.

concepts (ACs, e.g. 'justice') are more complex compared with concrete concepts (CCs) (e.g. 'table'). Indeed, they do not possess a single object as a referent, they assemble quite heterogeneous members and they are more detached from exteroceptive and more grounded in interoceptive experience. Recent views have hypothesized that interpersonal communication is particularly crucial to acquire and use ACs. The current study investigates the reliance of ACs/CCs representation on interpersonal behaviour. We asked participants to perform a motor interaction task with two avatars who embodied two real confederates. Before and after the motor interaction task, the two confederates provided participants with hints in a concept guessing task associated with visual stimuli: one helped in guessing ACs and the other, CCs. A control study we performed both with the materials employed in the main experiment and with other materials, confirmed that associating verbal concepts with visual images was more difficult with ACs than with CCs. Consistently, the results of the main experiment showed that participants asked for more hints with ACs than CCs and were more synchronous when interacting with the avatar corresponding to the AC's confederate. The results highlight an important role of sociality in grounding ACs.

Interpersonal Motor Interactions Shape Multisensory Representations of the Peripersonal Space.

This perspective review focuses on the proposal that predictive multisensory integration occurring in one's peripersonal space (PPS) supports individuals' ability to efficiently interact with others, and that integrating sensorimotor signals from the interacting partners leads to the emergence of a shared representation of the PPS. To support this proposal, we first introduce the features of body and PPS representations that are relevant for interpersonal motor interactions. Then, we highlight the role of action planning and execution on the dynamic expansion of the PPS. We continue by presenting evidence of PPS modulations after tool use and review studies suggesting that PPS expansions may be accounted for by Bayesian sensory filtering through predictive coding. In the central section, we describe how this conceptual framework can be used to explain the mechanisms through which the PPS may be modulated by the actions of our interaction partner, in order to facilitate interpersonal coordination. Last, we discuss how this proposal may support recent evidence concerning PPS rigidity in Autism Spectrum Disorder (ASD) and its possible relationship with ASD individuals' difficulties during interpersonal coordination. Future studies will need to clarify the mechanisms and neural underpinning of these dynamic, interpersonal modulations of the PPS.

Competence-based social status and implicit preference modulate the ability to coordinate during a joint grasping task.

Studies indicate that social status influences people's social perceptions. Less information is available about whether induced social status influences dyadic coordination during motor interactions. To explore this issue, we designed a study in which two confederates obtained high or low competence-based status by playing a game together with the participant, while the participant always occupied the middle position of the hierarchy. Following this status-inducing phase, participants were engaged in a joint grasping task with the high- and low-status confederates in different sessions while behavioural (i.e., interpersonal asynchrony and movement start time) indexes were measured. Participants' performance in the task (i.e., level of interpersonal asynchrony) when interacting with the low-status partner was modulated by their preference for him. The lower participants' preference for a low- relative to a high-status confederate, the worse participants' performance when interacting with the low-status confederate. Our results show that participants' performance during motor interactions changes according to the social status of the interaction partner.

Dissociating cognitive, behavioral and physiological stress-related responses through dorsolateral prefrontal cortex inhibition.

The left dorsolateral prefrontal cortex (dlPFC) has been implicated in the regulation of stress-related cognitive processes and physiological responses and is the principal target of noninvasive brain stimulation techniques applied to psychiatric conditions. However, existing studies are mostly correlational and causal evidence on the role of this region in mediating specific psychophysiological mechanisms underpinning stress-related responses are needed to make the application of such techniques more efficient. To fill this gap, this study used inhibitory continuous theta burst stimulation (cTBS) in healthy individuals to examine the extent to which activity of the left dlPFC is associated with cognitive (subjective focus on a tracking task), behavioral (reaction times and variability), and physiological responses (heart rate and its variability and cortisol level) following induction of perseverative cognition. Compared to sham and left ventral PreMotor area stimulation (as active control area), inhibition of left dlPFC determined sustained autonomic and neuroendocrine activation and increased the subjective perception of being task-focused, while not changing the behavioral and self-reported stress-related responses. Adopting a causative approach, we describe a role of left dlPFC in inhibitory control of the physiological stress-response associated to perseverative thinking.

Midline frontal and occipito-temporal activity during error monitoring in dyadic motor interactions.

Discrepancies between sensory predictions and action outcome are at the base of error coding. However, these phenomena have mainly been studied focussing on individual performance. Here, we explored EEG responses to motor prediction errors during a human-avatar interaction and show that Theta/Alpha activity of the frontal error-monitoring system works in phase with activity of the occipito-temporal node of the action observation network. Our motor interaction paradigm required healthy individuals to synchronize their reach-to-grasp movements with those of a virtual partner in conditions that did (Interactive) or did not require (Cued) movement prediction and adaptation to the partner's actions. Crucially, in 30% of the trials the virtual partner suddenly and unpredictably changed its movement trajectory thereby violating the human participant's expectation. These changes elicited error-related neuromarkers (ERN/Pe - Theta/Alpha modulations) over fronto-central electrodes during the Interactive condition. Source localization and connectivity analyses showed that the frontal Theta/Alpha activity induced by violations of the expected interactive movements was in phase with occipito-temporal Theta/Alpha activity. These results expand current knowledge about the neural correlates of on-line interpersonal motor interactions linking the frontal error-monitoring system to visual, body motion-related, responses.

Visuo-motor interference with a virtual partner is equally present in cooperative and competitive interactions.

Automatic imitation of observed actions is thought to be a powerful mechanism, one that may mediate the reward value of interpersonal interactions, but that could also generate visuo-motor interference when interactions involve complementary movements. Since interpersonal coordination seems to be crucial both when cooperating and competing with others, the questions arises as to whether imitation-and thus visuo-motor interference-occurs in both scenarios. To address this issue, we asked human participants to engage in high- or low-interactive (Interactive or Cued condition, respectively), cooperative or competitive, joint reach-to-grasps with a virtual partner. More specifically, interactions occurred in: (i) a Cued condition, where participants simply adapted their movement timing to synchronize with (during cooperation) or anticipate (during competition) the virtual partner's grasp; (ii) an Interactive condition requiring the same adaptation, as well as a real-time selection of their action according to the virtual character's movement. To simulate a realistic human-human interaction, the virtual character would change its movement speed in consecutive trials according to participants' behaviour. Results demonstrate that visuo-motor interference-as indexed by movement kinematics (higher maximum wrist height during complementary compared to imitative power grips)-emerge in both cooperative and competitive motor interactions only when predictions about the partner's movements are needed to perform one's own action (interactive condition). These results support the idea that simulative imitation is heavily present when individuals need to match their behaviours closely.

Modulation of preference for abstract stimuli following competence-based social status primes.

In the present study, we measured whether competence-related high and low social status attributed to two unknown individuals affects participants' implicit reactivity to abstract stimuli associated to the identity of the same individuals. During a status-inducing procedure, participants were asked to play an interactive game with two (fake) players coded as high vs low status based on their game competence. Before and after the game, a modified version of the Affective Misattribution Procedure (AMP) was administered in which the players' faces were used as primes. The evaluation target, as is typical to AMP, was a Chinese ideogram. There were two different presentation timings for the prime image: 75 ms and 17 ms. After the status-inducing procedure, the evaluation targets preceded by the high-status prime (i.e. best player's face) were rated as more pleasant than those preceded by the low-status prime (i.e. worst player's face). This effect was only found, however, for the 75 ms lasting prime. Moreover, explicit ratings of the primes showed that the high-status player was rated as more intelligent, competent and dominant than the low status one. These results indicate that implicit preference and explicit evaluation of unacquainted individuals are rapidly modulated by competence-based social status attribution, thus hinting at the plastic nature of social categorization and, relatedly, the malleability of visual preference.

Role of the occipito-temporal theta rhythm in hand visual identification.

Neuroimaging and EEG studies have shown that passive observation of the full body and of specific body parts is associated with 1) activity of an occipito-temporal region named the extrastriate body area (EBA), 2) amplitude modulations of a specific posterior event-related potential (ERP) component (N1/N190), and 3) a theta-band (4-7 Hz) synchronization recorded from occipito-temporal electrodes compatible with the location of EBA. To characterize the functional role of the occipito-temporal theta-band increase during the processing of body-part stimuli, we recorded EEG from healthy participants while they were engaged in an identification task (match-to-sample) of images of hands and nonbody control images (leaves). In addition to confirming that occipito-temporal electrodes show a larger N1 for hand images compared with control stimuli, cluster-based analysis revealed an occipito-temporal cluster showing an increased theta power when hands are presented (compared with leaves) and show that this theta increase is higher for identified hands compared with nonidentified ones while not being significantly different between not identified nonhand stimuli. Finally, single trial multivariate pattern analysis revealed that time-frequency modulation in the theta band is a better marker for classifying the identification of hand images than the ERP modulation. The present results support the notion that theta activity over the occipito-temporal cortex is an informative marker of hand visual processing and may reflect the activity of a network coding for stimulus identity.NEW & NOTEWORTHY Hands provide crucial information regarding the identity of others, which is a key information for social processes. We recorded EEG activity of healthy participants during the visual identification of hand images. The combination of univariate and multivariate pattern analysis in time- and time-frequency domain highlights the functional role of theta (4-7 Hz) activity over visual areas during hand identification and emphasizes the robustness of this neuromarker in occipito-temporal visual processing dynamics.

Inhibitory Theta Burst Stimulation Highlights the Role of Left aIPS and Right TPJ during Complementary and Imitative Human-Avatar Interactions in Cooperative and Competitive Scenarios.

Competitive and cooperative interactions are based on anticipation or synchronization with the partner's actions. Both forms of interaction may either require performing imitative or complementary movements with respect to those performed by our partner. We explored how parietal regions involved in the control of imitative behavior (temporo-parietal junction, TPJ), goal coding and visuo-motor integration (anterior intraparietal sulcus, aIPS) contribute to the execution of imitative and complementary movements during cooperative and competitive interactions. To this aim, we delivered off-line non-invasive inhibitory brain stimulation to healthy individuals' left aIPS and right TPJ before they were asked to reach and grasp an object together with a virtual partner by either performing imitative or complementary interactions. In different blocks, participants were asked to compete or cooperate with the virtual partner that varied its behavior according to cooperative or competitive contexts. Left aIPS and right TPJ inhibition impaired individuals' performance (i.e., synchrony in cooperative task and anticipation in competition) during complementary and imitative interactions, respectively, in both cooperative and competitive contexts, indicating that aIPS and TPJ inhibition affects own-other action integration and action imitation (that are different in complementary vs imitative interactions) more than action synchronization or anticipation (that are different in cooperative vs competitive contexts).

Contextual and social variables modulate aesthetic appreciation of bodily and abstract art stimuli.

Despite the increasing interest in the plasticity of aesthetic appreciation, we know comparatively little about the role of individuals' cultural (e.g. the appreciators' expertise) and of social emotional-cognitive (e.g. the social influence of people perceived as warm or competent) variables in modulating the appreciation process. In two experiments we investigated 1) whether people with different art-expertise are influenced differently by contextual (i.e. stimuli primed as art) and social (i.e. stimuli rated as beautiful by art-critics) information and 2) whether acknowledging the judgment of a person perceived as warm or as competent has a different influence on individuals' aesthetic appreciation of art works. Warmth and competence are two social dimensions of fundamental importance for categorizing others as in-group or out-group (Fiske, Cuddy, Glick, & Xu, 2002). We found that insinuating that the observed works were pieces of art, highly appreciated by art critics, lead expert participants to judge the stimuli as more beautiful in comparison to when the very same stimuli were not preceded by any manipulation. Moreover, we found that both art-experts and non-experts rated the stimuli as more beautiful when they believed it to be highly appreciated by people perceived as warm vs people perceived as competent. These results provide novel information on the plasticity of aesthetics and pave the way to understanding how tastes and preferences in the domain of aesthetics can be influenced.

Interactor's body shape does not affect visuo-motor interference effects during motor coordination.

The biological-tuning of the Action Observation Network is highly debated. A current open question relates to whether the morphological appearance (body shape) and/or the biological motion of the observed agent triggers action simulation processes. Motor simulation of the partner's action is critical for motor interactions, where two partners coordinate their actions in space and time. It supports interpersonal alignment and facilitates online coordination. However, motor simulation also leads to visuo-motor interference effects when people are required to coordinate with complementary actions, i.e. incongruent movements as compared to the observed ones. Movement kinematics of interactive partners allows us to capture their automatic tendency to simulate and imitate the partner's complementary movements. In an online reach-to-grasp task, we investigated whether visuo-motor interference effects, visible in the kinematics of complementary movements, are modulated by the visual presence of the interactor's body shape. We asked participants to interact with 1) a humanoid agent with a human-like body shape and with real human, biological, movement kinematics, or 2) a non-humanoid agent, which did not resemble the human body-shape but moved with the same real kinematics. Through the combination of inferential and Bayesian statistics, the results show no effect of interactor's body shape on visuo-motor interference in reaching and grasping kinematics during online motor coordination. We discuss the results and propose that the kinematics of the observed movements, during motor interactions, might be the key factor for visuo-motor interference to take place independently from the morphological appearance of the partner. This is particularly relevant in a technological society that constantly asks humans to interact with artificial agents.