Neuromodulation of the Left Inferior Frontal Cortex Affects Social Monitoring during Motor Interactions.

Motor interactions require observing and monitoring a partner's performance as the interaction unfolds. Studies in monkeys suggest that this form of social monitoring might be mediated by the activity of the ventral premotor cortex (vPMc), a critical brain region in action observation and motor planning. Our previous fMRI studies in humans showed that the left vPMc is indeed recruited during social monitoring, but its causal role is unexplored. In three experiments, we applied online anodal or cathodal transcranial direct current stimulation over the left lateral frontal cortex during a music-like interactive task to test the hypothesis that neuromodulation of the left vPMc affects participants' performance when a partner violates the agent's expectations. Participants played short musical sequences together with a virtual partner by playing one note each in turn-taking. In 50% of the trials, the partner violated the participant's expectations by generating the correct note through an unexpected movement. During sham stimulation, the partner's unexpected behavior led to a slowdown in the participant's performance (observation-induced posterror slowing). A significant interaction with the stimulation type showed that cathodal and anodal transcranial direct current stimulation induced modulation of the observation-induced posterror slowing in opposite directions by reducing or enhancing it, respectively. Cathodal stimulation significantly reduced the effect compared to sham stimulation. No effect of neuromodulation was found when the partner behaved as expected or when the observed violation occurred within a context that was perceptually matched but noninteractive in nature. These results provide evidence for the critical causal role that the left vPMc might play in social monitoring during motor interactions, possibly through the interplay with other brain regions in the posterior medial frontal cortex.

Visuo-motor interference is modulated by task interactivity: A kinematic study.

Extensive evidence shows that action observation can influence action execution, a phenomenon often referred to as visuo-motor interference. Little is known about whether this effect can be modulated by the type of interaction agents are involved in, as different studies show conflicting results. In the present study, we aimed at shedding light on this question by recording and analyzing the kinematic unfolding of reach-to-grasp movements performed in interactive and noninteractive settings. Using a machine learning approach, we investigated whether the extent of visuo-motor interference would be enhanced or reduced in two different joint action settings compared with a noninteractive one. Our results reveal that the detrimental effect of visuo-motor interference is reduced when the action performed by the partner is relevant to achieve a common goal, regardless of whether this goal requires to produce a concrete sensory outcome in the environment (joint outcome condition) or only a joint movement configuration (joint movement condition). These findings support the idea that during joint actions we form dyadic motor plans, in which both our own and our partner's actions are represented in predictive terms and in light of the common goal to be achieved. The formation of a dyadic motor plan might allow agents to shift from the automatic simulation of an observed action to the active prediction of the consequences of a partner's action. Overall, our results demonstrate the unavoidable impact of others' action on our motor behavior in social contexts, and how strongly this effect can be modulated by task interactivity.

Emergent and planned interpersonal synchronization are both sensitive to 'tempo aftereffect contagion'.

Interpersonal synchronization is fundamental for motor coordination during social interactions. Discerning emergent (entrainment) from planned synchronization represents a non-trivial issue in visually bonded individuals acting together, as well as assessing whether inter-individual differences, e.g., in autistic traits, modulate both types of synchronization. In a visuomotor finger-tapping task, two participants replicated a target tempo either synchronizing ('joint' condition) or not ('non-interactive' condition, 'non-int') with each other. One participant was exposed ('induced') to tempo aftereffect (a medium tempo seems faster or slower after exposure to slower or faster inducing tempi), but not the other participant ('not induced'); thus they had different timing perceptions of the same target. We assessed to what degree emergent and/or planned synchronization affected dyads by analyzing inter-tap-intervals, synchronization indexes, and cross-correlation coefficients. Results revealed a 'tempo aftereffect contagion': inter-tap-intervals of both induced and not-induced participants showed aftereffect in both the joint and non-int conditions. Moreover, aftereffects did not correlate across conditions suggesting they might be due to (at least in part) different processes, but the propensity for tempo aftereffect contagion correlated with individuals' autistic traits only in the non-int condition. Finally, participants co-adjusted their tapping more in the joint condition than in the non-int one, as confirmed by higher synchronization indexes and the mutual adaptation pattern of cross-correlation coefficients. Altogether, these results show the subtle interplay between emergent and planned interpersonal synchronization mechanisms that act on a millisecond timescale independently from synching or not with the partner.

Error observation as a window on performance monitoring in social contexts? A systematic review.

Living in a social world requires social monitoring, i.e., the ability to keep track of others' actions and mistakes. Here, we demonstrate the good reliability of the behavioral and neurophysiological indexes ascribed to social monitoring. We also show that no consensus exists on the cognitive bases of this phenomenology and discuss three alternative hypotheses: (i) the direct matching hypothesis, postulating that observed errors are processed through automatic simulation; (ii) the attentional hypothesis, considering errors as unexpected events that take resources away from task processing; and (iii) the goal representation hypothesis, which weighs social error monitoring depending on how relevant the other's task is to the observer's goals. To date, evidence on the role played by factors that could help to disentangle these hypotheses (e.g., the human vs. non-human nature of the actor, the error rate, and the reward context) is insufficient, although the goal representation hypothesis seems to receive more support. Theory-driven experimental designs are needed to enlighten this debate and clarify the role of error monitoring during interactive exchanges.

Encoding interactive scripts at 10 months of age.

Understanding action-reaction associations that give origin to interactive scripts (e.g., give-and-take interactions) is essential for appreciating social exchanges. However, studies on infants' action understanding have mainly investigated the case of actions performed by individual agents. Moreover, although extensive literature has explored infants' comprehension of action-effect relationships in object functioning, no study has addressed whether it also plays a role when observing social interactions, an issue we addressed here. In a first study, 10-month-old infants observed short videos of dyadic exchanges. We investigated whether they were able to link specific human gestures directed toward another person to specific vocal reactions in the receiver. We used a double-habituation paradigm in which infants were sequentially habituated to two specific action-reaction associations. In the test phase, infants watched one of the two habituated (Familiar) videos, a video with a reversed action-reaction association (Violation), and a Novel video. Results showed that the infants looked longer at both the Novel and Violation test trials than at the Familiar test trials. In a control study, we show that these results could not be accounted for by associative learning; indeed, learning of the action-reaction association did not occur when the vocalization was not produced by the receiver but only contingent on the agent's action. Thus, we show that 10-month-old infants can encode specific social action-effect relationships during the observation of dyadic interactions and that the interactivity of the social context may be critical to shaping young infants' understanding of others' behaviors.

When action prediction grows old: An fMRI study.

Predicting the unfolding of others' actions (action prediction) is crucial for successfully navigating the social world and interacting efficiently. Age-related changes in this domain have remained largely unexplored, especially for predictions regarding simple gestures and independent of contextual information or motor expertise. Here, we evaluated whether healthy aging impacts the neurophysiological processes recruited to anticipate, from the observation of implied-motion postures, the correct conclusion of simple grasping and pointing actions. A color-discrimination task served as a control condition to assess the specificity of the age-related effects. Older adults showed reduced efficiency in performance that was yet not specific to the action prediction task. Nevertheless, fMRI results revealed task-specific age-related differences: while both groups showed stronger recruitment of the lateral occipito-temporal cortex bilaterally during the action prediction than the control task, the younger participants additionally showed a higher bilateral engagement of parietal regions. Importantly, in both groups, the recruitment of visuo-motor processes in the right posterior parietal cortex was a predictor of good performance. These results support the hypothesis of decreased involvement of sensorimotor processes in cognitive tasks when processing action- and body-related stimuli in healthy aging. These results have implications for social interaction, which requires the fast reading of others' gestures.

The unexplored link between aesthetic perception and creativity: A theory-driven meta-analysis of fMRI studies in the visual domain.

Creative production (related to art-making) and aesthetic appreciation (related to art-viewing) are inherently linked in visual arts, but their relationship has never been explored explicitly in cognitive neuroscience, nor the nature of such connection. The available literature suggests two cognitive processes as possible foundations of these two experiences: motor simulation or inhibitory control. In a meta-analysis of fMRI studies, we addressed this issue: we investigated whether there are shared neurofunctional underpinnings behind aesthetic and creative experiences in the visual domain; further, we examined whether any shared brain activation may reflect either motor simulation or inhibitory processes. A conjunction analysis revealed a common involvement of the pre-SMA in both classes of studies, a brain region, if anything, more concerned with top-down inhibitory motor and volitional cognitive control rather than bottom-up motor simulation. In the art-viewing domain, this finding was primarily driven by figurative rather than abstract art. The methodological limitations in the available literature are discussed together with possible new ways to expand the existing findings.

How shared goals shape action monitoring.

Cooperation triggers expectations on our partners' contributions to achieve a common goal. A partner, however, may sometimes violate such expectations, driving us to perform immediate adjustments. What neurophysiological mechanisms support these adaptations? We tested the hypothesis of an interaction-specific brain system that can decode a partner's error and promote adaptive responses when cooperating toward a shared goal. During functional magnetic resonance imaging, the participants played short melodies with a virtual partner by performing one note each in turn-taking. A colored cue indicated which melody they had to execute at each trial, thus generating expectations on what notes the partner would play. The participants also performed the task in a perceptually matched Non-Interactive context. The results showed that task interactivity modulates the brain responses to a partner's error in dorsal fronto-temporoparietal and medial cingulo-opercular networks. Multivariate pattern analysis revealed that these neural activations reflect deep decoding of the partner's mistake. Within these networks, the automatic tendency to correct the partner's errors, as indexed by specific reaction times adaptations, depended on the activity of a right-lateralized fronto-opercular system that may enable mutual support during real-life cooperation. Future studies may unveil the role of this putative "interaction monitoring" brain system in social dysfunctions and their motor foundations.

Taking apart what brings us together: The role of action prediction, perspective-taking, and theory of mind in joint action.

The ability to act together with others to achieve common goals is crucial in life, yet there is no full consensus on the underlying cognitive skills. While influential theoretical accounts suggest that interaction requires sophisticated insights into others' minds, alternative views propose that high-level social skills might not be necessary because interactions are grounded on sensorimotor predictive mechanisms. At present, empirical evidence is insufficient to decide between the two. This study addressed this issue and explored the association between performance at joint action tasks and cognitive abilities in three domains-action prediction, perspective-taking, and theory of mind-in healthy adults (N = 58). We found that, while perspective-taking played a role in reading the behaviour of others independently of the social context, action prediction abilities specifically influenced the agents' performance in an interactive task but not in a control (social but non-interactive) task. In our study, performance at a theory of mind test did not play any role, as confirmed by Bayesian analyses. The results suggest that, in adults, sensorimotor predictive mechanisms might play a significant and specific role in supporting interpersonal coordination during motor interactions. We discuss the implications of our findings for the contrasting theoretical views described earlier and propose a way they might be partly reconciled.

Mechanisms for mutual support in motor interactions.

What is the key to successful interaction? Is it sufficient to represent a common goal, or does the way our partner achieves that goal count as well? How do we react when our partner misbehaves? We used a turn-taking music-like task requiring participants to play sequences of notes together with a partner, and we investigated how people adapt to a partner's error that violates their expectations. Errors consisted of either playing a wrong note of a sequence that the agents were playing together (thus preventing the achievement of the joint goal) or playing the expected note with an unexpected action. In both cases, we found post-error slowing and inaccuracy suggesting the participants' implicit tendency to correct the partner's error and produce the action that the partner should have done. We argue that these "joint" monitoring processes depend on the motor predictions made within a (dyadic) motor plan and may represent a basic mechanism for mutual support in motor interactions.

Eyes wide shut: How visual cues affect brain patterns of simulated gait.

In the last 20 years, motor imagery (MI) has been extensively used to train motor abilities in sport and in rehabilitation. However, MI procedures are not all alike as much as their potential beneficiaries. Here we assessed whether the addition of visual cues could make MI performance more comparable with explicit motor performance in gait tasks. With fMRI we also explored the neural correlates of these experimental manipulations. We did this in elderly subjects who are known to rely less on kinesthetic information while favoring visual strategies during motor performance. Contrary to expectations, we found that the temporal coupling between execution and imagery times, an index of the quality of MI, was less precise when participants were allowed to visually explore the environment. While the brain activation patterns of the gait motor circuits were very similar in both an open-eyed and eye-shut virtual walking MI task, these differed for a vast temporo-occipito-parietal additional activation for open-eyed MI. Crucially, the higher was the activity in this posterior network, the less accurate was the MI performance with eyes open at a clinical test of gait. We conclude that both visually-cued and internally-cued MI are associated with the neurofunctional activation of a gait specific motor system. The less precise behavioral coupling between imagined and executed gait while keeping eyes open may be attributed to the processing load implied in visual monitoring and scanning of the environment. The implications of these observations for rehabilitation of gait with MI are discussed.

Motor imagery training speeds up gait recovery and decreases the risk of falls in patients submitted to total knee arthroplasty.

With Motor imagery (MI), movements are mentally rehearsed without overt actions; this procedure has been adopted in motor rehabilitation, primarily in brain-damaged patients. Here we rather tested the clinical potentials of MI in purely orthopaedic patients who, by definition, should maximally benefit of mental exercises because of their intact brain. To this end we studied the recovery of gait after total knee arthroplasty and evaluated whether MI combined with physiotherapy could speed up the recovery of gait and even limit the occurrence of future falls. We studied 48 patients at the beginning and by the end of the post-surgery residential rehabilitation program: half of them completed a specific MI training supported by computerized visual stimulation (experimental group); the other half performed a non-motoric cognitive training (control group). All patients also had standard physiotherapy. By the end of the rehabilitation, the experimental group showed a better recovery of gait and active knee flexion-extension movements, and less pain. The number of falls or near falls after surgery was significantly lower in the experimental group. These results show that MI can improve gait abilities and limit future falls in orthopaedic patients, without collateral risks and with limited costs.

The engaging nature of interactive gestures.

The social interactions that we experience from early infancy often involve actions that are not strictly instrumental but engage the recipient by eliciting a (complementary) response. Interactive gestures may have privileged access to our perceptual and motor systems either because of their intrinsically engaging nature or as a result of extensive social learning. We compared these two hypotheses in a series of behavioral experiments by presenting individuals with interactive gestures that call for motor responses to complement the interaction ('hand shaking', 'requesting', 'high-five') and with communicative gestures that are equally socially relevant and salient, but do not strictly require a response from the recipient ('Ok', 'Thumbs up', 'Peace'). By means of a spatial compatibility task, we measured the interfering power of these task-irrelevant stimuli on the behavioral responses of individuals asked to respond to a target. Across three experiments, our results showed that the interactive gestures impact on response selection and reduce spatial compatibility effects as compared to the communicative (non-interactive) gestures. Importantly, this effect was independent of the activation of specific social scripts that may interfere with response selection. Overall, our results show that interactive gestures have privileged access to our perceptual and motor systems, possibly because they entail an automatic preparation to respond that involuntary engages the motor system of the observers. We discuss the implications from a developmental and neurophysiological point of view.

How aging affects the premotor control of lower limb movements in simulated gait.

Gait control becomes more demanding in healthy older adults, yet what cognitive or motor process leads to this age-related change is unknown. The present study aimed to investigate whether it might depend on specific decay in the quality of gait motor representation and/or a more general reduction in the efficiency of lower limb motor control. Younger and older healthy participants performed in fMRI a virtual walking paradigm that combines motor imagery (MI) of walking and standing on the spot with the presence (Dynamic Motor Imagery condition, DMI) or absence (pure MI condition) of overtly executed ankle dorsiflexion. Gait imagery was aided by the concomitant observation of moving videos simulating a stroll in the park from a first-person perspective. Behaviorally, older participants showed no sign of evident depletion in the quality of gait motor representations, and absence of between-group differences in the neural correlates of MI. However, while younger participants showed increased frontoparietal activity during DMI, older participants displayed stronger activation of premotor areas when controlling the pure execution of ankle dorsiflexion, regardless of the imagery task. These data suggest that reduced automaticity of lower limb motor control in healthy older subjects leads to the recruitment of additional premotor resources even in the absence of basic gait functional disabilities.

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.

How preschoolers and adults represent their joint action partner's behavior.

We investigated the cognitive mechanisms underlying turn-taking joint action in 42-month-old children (Experiment 1) and adults (Experiment 2) using a behavioral task of dressing a virtual bear together. We aimed to investigate how participants represent a partners' behavior, i.e., in terms of specific action kinematics or of action effects. The bear was dressed by pressing a smaller and a bigger button. In the Action-response task, instructions asked participants to respond to the partner by pressing the same or opposite button; in the Action-effect task they had to respond to the partner's action effect by dressing the bear with the lacking part of the clothing, which in some cases implied pressing the same button and in other cases implied pressing the opposite button. In 50% of the trials, the partner's association between each button and the ensuing effect (dressing the bear with t-shirt or pants) was reversed, while it never changed for participants. Both children and adults showed no effect of physical congruency of actions, but showed impaired performance in the Action-effect task if their partner achieved her effect through a different action-effect association than their own. These results suggest that, when encoding their partner's actions, agents are influenced by action-effect associations that they learnt through their own experience. While interference led to overt errors in children, it caused longer reaction times in adults, suggesting that a flexible cognitive control (that is still in development in young children) is required to take on the partner's perspective.

A functional limitation to the lower limbs affects the neural bases of motor imagery of gait.

Studies on athletes or neurological patients with motor disorders have shown a close link between motor experience and motor imagery skills. Here we evaluated whether a functional limitation due to a musculoskeletal disorder has an impact on the ability to mentally rehearse the motor patterns of walking, an overlearned and highly automatic behaviour. We assessed the behavioural performance (measured through mental chronometry tasks) and the neural signatures of motor imagery of gait in patients with chronic knee arthrosis and in age-matched, healthy controls. During fMRI, participants observed (i) stationary or (ii) moving videos of a path in a park shown in the first-person perspective: they were asked to imagine themselves (i) standing on or (ii) walking along the path, as if the camera were "their own eyes" (gait imagery (GI) task). In half of the trials, participants performed a dynamic gait imagery (DGI) task by combining foot movements with GI. Behavioural tests revealed a lower degree of isochrony between imagined and performed walking in the patients, indicating impairment in the ability to mentally rehearse gait motor patterns. Moreover, fMRI showed widespread hypoactivation during GI in motor planning (premotor and parietal) brain regions, the brainstem, and the cerebellum. Crucially, the performance of DGI had a modulatory effect on the patients and enhanced activation of the posterior parietal, brainstem, and cerebellar regions that the healthy controls recruited during the GI task. These findings show that functional limitations of peripheral origin may impact on gait motor representations, providing a rationale for cognitive rehabilitation protocols in patients with gait disorders of orthopaedic nature. The DGI task may be a suitable tool in this respect.

Inhibition of left anterior intraparietal sulcus shows that mutual adjustment marks dyadic joint-actions in humans.

Creating real-life dynamic contexts to study interactive behaviors is a fundamental challenge for the social neuroscience of interpersonal relations. Real synchronic interpersonal motor interactions involve online, inter-individual mutual adaptation (the ability to adapt one's movements to those of another in order to achieve a shared goal). In order to study the contribution of the left anterior Intra Parietal Sulcus (aIPS) (i.e. a region supporting motor functions) to mutual adaptation, here, we combined a behavioral grasping task where pairs of participants synchronized their actions when performing mutually adaptive imitative and complementary movements, with the inhibition of activity of aIPS via non-invasive brain stimulation. This approach allowed us to investigate whether aIPS supports online complementary and imitative interactions. Behavioral results showed that inhibition of aIPS selectively impairs pair performance during complementary compared to imitative interactions. Notably, this effect depended on pairs' mutual adaptation skills and was higher for pairs composed of participants who were less capable of adapting to each other. Thus, we provide the first causative evidence for a role of the left aIPS in supporting mutually adaptive interactions and show that the inhibition of the neural resources of one individual of a pair is compensated at the dyadic level.