Brain-to-Brain Coupling in the Gamma-Band as a Marker of Shared Intentionality

Cooperation and competition are two ways of social interaction keys to life in society. Recent EEG-based hyperscanning studies reveal that cooperative and competitive interactions induce an increase in interbrain coupling. However, whether this interbrain coupling effect is just a reflection of inter-subject motor coordination or can also signal the type of social interaction is unknown. Here, we show that behavioral coordination and social interaction type can be distinguished according to the frequency of oscillation in which the brains are coupled. We use EEG to simultaneously measure the brain activity of pairs of subjects, while they were performing a visual cue-target task in a cooperative and competitive manner. Behavioral responses were quasi-simultaneous between subject pairs for both competitive and cooperative conditions, with faster average response times for the competitive condition. Concerning brain activity, we found increased interbrain coupling in theta band (3–7 Hz) during cooperation and competition, with stronger coupling during competitive interactions. This increase of interbrain theta coupling correlated with a decrease in reaction times of the dyads. Interestingly, we also found an increase in brain-to-brain coupling in gamma band (38–42 Hz) only during cooperative interactions. Unlike the theta coupling effect, the gamma interbrain coupling did not correlate with dyads’ reaction times. Taken together, these results suggest that theta interbrain coupling could be linked to motor coordination processes common to cooperative and competitive interactions, while gamma brain-to-brain coupling emerges as an electrophysiological marker of shared intentionality during cooperative interactions

Neural foundations of cooperative social interactions

The embodied-embedded-enactive-extended (4E) approach to study cognition suggests that interaction with the world is a crucial component of our cognitive processes. Most of our time, we interact with other people. Therefore, studying cognition without interaction is incomplete. Until recently, social neuroscience has only focused on studying isolated human and animal brains, leaving interaction unexplored. To fill this gap, we studied interacting participants, focusing on both intra- and inter-brain (hyperscanning) neural activity. In the first study, we invited dyads to perform a visual task in both a cooperative and a competitive context while we measured EEG. We found that mid-frontal activity around 200-300 ms after receiving monetary rewards was sensitive to social context and differed between cooperative and competitive situations. In the second study, we asked participants to coordinate their movements with each other and with a robotic partner. We found significantly stronger EEG amplitudes at frontocentral electrodes when people interacted with a robotic partner. Lastly, we performed a comprehensive literature review and the first meta-analysis in the emerging field of hyperscanning that validated it as a method to study social interaction. Taken together, our results showed that adding a second participant (human or AI/robotic) fostered our understanding of human cognition. We learned that the activity at frontocentral electrodes is sensitive to social context and type of partner (human or robotic). In both studies, the participants’ interaction was required to show these novel neural processes involved in action monitoring. Similarly, studying inter-brain neural activity allows for the exploration of new aspects of cognition. Many cognitive functions involved in successful social interactions are accompanied by neural synchrony between brains, suggesting the extended form of our cognition

Multivariate model for cooperation: bridging Social Physiological Compliance and Hyperscanning

The neurophysiological analysis of cooperation has evolved over the past 20 years, moving towards the research of common patterns in neurophysiological signals of people interacting. Social Physiological Compliance (SPC) and Hyperscanning represent two frameworks for the joint analysis of autonomic and brain signals respectively. Each of the two approaches allows to know about a single layer of cooperation according to the nature of these signals: SPC provides information mainly related to emotions, and Hyperscanning that related to cognitive aspects. In this work, after the analysis of the state of the art of SPC and Hyperscanning, we explored the possibility to unify the two approaches creating a complete neurophysiological model for cooperation considering both affective and cognitive mechanisms. We synchronously recorded electrodermal activity, cardiac and brain signals of 14 cooperative dyads. Time series from these signals were extracted and Multivariate Granger Causality was computed. The results showed that only when subjects in a dyad cooperate there is a statistically significant causality between the multivariate variables representing each subject. Moreover, the entity of this statistical relationship correlates with the dyad's performance. Finally, given the novelty of this approach and its exploratory nature, we provided its strengths and limitations

Interpersonal neural synchrony when predicting others’ actions during a game of rock-paper-scissors

As members of a social species, we spend most of our time interacting with others. In interactions, we tend to mutually align our behavior and brain responses to communicate more effectively. In a semi-computerized version of the Rock-Paper-Scissors game, we investigated whether people show enhanced interpersonal neural synchronization when making explicit predictions about others’ actions. Across four experimental conditions, we measured the dynamic brain activity using the functional near-infrared spectroscopy (fNIRS) hyperscanning method. Results showed that interpersonal neural synchrony was enhanced when participants played the game together as they would do in real life in comparison to when they played the game on their own. We found no evidence of increased neural synchrony when participants made explicit predictions about others’ actions. Hence, neural synchrony may depend on mutual natural interaction rather than an explicit prediction strategy. This study is important, as it examines one of the presumed functions of neural synchronization namely facilitating predictions

Exploring the Connected Brain by fNIRS: Human-to-Human Interactions Engineering

Functional Near Infrared Spectroscopy (fNIRS) is a relatively new neuroimaging technique adequate and useful for exploring neural activity in social contexts involving human interactions. Compared to functional Magnetic Resonance Imaging (fMRI), fNIRS is easy-to-use safe, noninvasive, silent, relatively low cost and portable, and applicable to subjects of all ages, thus resulting in a good option for ecological studies involving humans in their real-life context. Moreover, by using hyperscanning technique, fNIRS allows recording the hemodynamic cerebral activity of two interacting subjects in an ecological context or during a shared performance. Thus, moving from a simple analysis about each subject\u2019s neural response during joint actions towards more complex computations makes possible to investigate brain synchrony, that is the if and how one\u2019s brain activity is related to that of another interacting partner simultaneously recorded. Here, we discuss how connectivity analyses, with respect to both time and frequency domain procedures, permitted to deepen some aspects of inter-brain synchrony in relation to emotional closeness, and to highlight how concurrent, cooperative actions can lead to interpersonal synchrony and bond construction

Multimodal hyperscanning reveals that synchrony of body and mind are distinct in mother-child dyads

Hyperscanning studies have begun to unravel the brain mechanisms underlying social interaction, indicating a functional role for interpersonal neural synchronization (INS), yet the mechanisms that drive INS are poorly understood. The current study, thus, addresses whether INS is functionally-distinct from synchrony in other systems – specifically the autonomic nervous system and motor behavior. To test this, we used concurrent functional near-infrared spectroscopy - electrocardiography recordings, while N = 34 mother-child and stranger-child dyads engaged in cooperative and competitive tasks. Only in the neural domain was a higher synchrony for mother-child compared to stranger-child dyads observed. Further, autonomic nervous system and neural synchrony were positively related during competition but not during cooperation. These results suggest that synchrony in different behavioral and biological systems may reflect distinct processes. Furthermore, they show that increased mother-child INS is unlikely to be explained solely by shared arousal and behavioral similarities, supporting recent theories that postulate that INS is higher in close relationships

Beyond physical entrainment: Competitive and cooperative mental stances during identical joint-action tasks differently affect inter-subjective neural synchrony and judgments of agency

10.1080/17470919.2020.1727949Social Neuroscience1503368-37

Inter-brain synchronization occurs without physical co-presence during cooperative online gaming

Inter-brain synchronization during social interaction has been linked with several positive phenomena, including closeness, cooperation, prosociality, and team performance. However, the temporal dynamics of inter-brain synchronization during collaboration are not yet fully understood. Furthermore, with collaboration increasingly happening online, the dependence of inter-brain phase synchronization of oscillatory activity on physical presence is an important but understudied question. In this study, physically isolated participants performed a collaborative coordination task in the form of a cooperative multiplayer game. We measured EEG from 42 subjects working together as pairs in the task. During the measurement, the only interaction between the participants happened through on-screen movement of a racing car, controlled by button presses of both participants working with distinct roles, either controlling the speed or the direction of the car. Pairs working together in the task were found to have elevated neural coupling in the alpha, beta, and gamma frequency bands, compared to performance matched false pairs. Higher gamma synchrony was associated with better momentary performance within dyads and higher alpha synchrony was associated with better mean performance across dyads. These results are in line with previous findings of increased inter-brain synchrony during interaction, and show that phase synchronization of oscillatory activity occurs during online real-time joint coordination without any physical co-presence or video and audio connection. Synchrony decreased during a playing session, but was found to be higher during the second session compared to the first. The novel paradigm, developed for the measurement of real-time collaborative performance, demonstrates that changes in inter-brain EEG phase synchrony can be observed continuously during interaction.Peer reviewe