A dual-brain therapeutic approach using noninvasive brain stimulation based on two-person neuroscience: A perspective review.

Our actions and decisions in everyday life are heavily influenced by social interactions, which are dynamic feedback loops involving actions, reactions, and internal cognitive processes between individual agents. Social interactions induce interpersonal synchrony, which occurs at different biobehavioral levels and comprises behavioral, physiological, and neurological activities. Hyperscanning-a neuroimaging technique that simultaneously measures the activity of multiple brain regions-has provided a powerful second-person neuroscience tool for investigating the phase alignment of neural processes during interactive social behavior. Neural synchronization, revealed by hyperscanning, is a phenomenon called inter-brain synchrony- a process that purportedly facilitates social interactions by prompting appropriate anticipation of and responses to each other's social behaviors during ongoing shared interactions. In this review, I explored the therapeutic dual-brain approach using noninvasive brain stimulation to target inter-brain synchrony based on second-person neuroscience to modulate social interaction. Artificially inducing synchrony between the brains is a potential adjunct technique to physiotherapy, psychotherapy, and pain treatment- which are strongly influenced by the social interaction between the therapist and patient. Dual-brain approaches to personalize stimulation parameters must consider temporal, spatial, and oscillatory factors. Multiple data fusion analysis, the assessment of inter-brain plasticity, a closed-loop system, and a brain-to-brain interface can support personalized stimulation.

Why behaviour matters: Studying inter-brain coordination during child-caregiver interaction.

Modern technology allows for simultaneous neuroimaging from interacting caregiver-child dyads. Whereas most analyses that examine the coordination between brain regions within an individual brain do so by measuring changes relative to observed events, studies that examine coordination between two interacting brains generally do this by measuring average intra-brain coordination across entire blocks or experimental conditions. In other words, they do not examine changes in inter-brain coordination relative to individual behavioural events. Here, we discuss the limitations of this approach. First, we present data suggesting that fine-grained temporal interdependencies in behaviour can leave residual artifact in neuroimaging data. We show how artifact can manifest as both power and (through that) phase synchrony effects in EEG and affect wavelet transform coherence in fNIRS analyses. Second, we discuss different possible mechanistic explanations of how inter-brain coordination is established and maintained. We argue that non-event-locked approaches struggle to differentiate between them. Instead, we contend that approaches which examine how interpersonal dynamics change around behavioural events have better potential for addressing possible artifactual confounds and for teasing apart the overlapping mechanisms that drive changes in inter-brain coordination.

Neural mechanisms distinguishing two types of cooperative problem-solving approaches: An fNIRS hyperscanning study.

Collaborative cooperation (CC) and division of labor cooperation (DLC) are two prevalent forms of cooperative problem-solving approaches in daily life. Despite extensive research on the neural mechanisms underlying cooperative problem-solving approaches, a notable gap exists between the neural processes that support CC and DLC. The present study utilized a functional near-infrared spectroscopy (fNIRS) hyperscanning technique along with a classic cooperative tangram puzzle task to investigate the neural mechanisms engaged by both friends and stranger dyads during CC versus DLC. The key findings of this study were as follows: (1) Dyads exhibited superior behavioral performance in the DLC task than in the CC task. The CC task bolstered intra-brain functional connectivity and inter-brain synchrony (IBS) in regions linked to the mirror neuron system (MNS), spatial perception (SP) and cognitive control. (2) Friend dyads showed stronger IBS in brain regions associated with the MNS than stranger dyads. (3) Perspective-taking predicted not only dyads' behavioral performance in the CC task but also their IBS in brain regions associated with SP during the DLC task. Taken together, these findings elucidate the divergent behavioral performance and neural connection patterns between the two cooperative problem-solving approaches. This study provides novel insights into the various neurocognitive processes underlying flexible coordination strategies in real-world cooperative contexts.

The Effects of Distancing Design Collaboration Necessitated by COVID-19 on Brain Synchrony in Teams Compared to Co-Located Design Collaboration: A Preliminary Study.

Due to the widespread involvement of distributed collaboration triggered by COVID-19, it has become a new trend that has continued into the post-pandemic era. This study investigated collective performance within two collaborative environments (co-located and distancing settings) by assessing inter-brain synchrony patterns (IBS) among design collaborators using functional near-infrared spectroscopy. The preliminary study was conducted with three dyads who possessed 2-3 years of professional product design experience. Each dyad completed two designated design tasks in distinct settings. In the distributed condition, participants interacted through video conferencing in which they were allowed to communicate by verbalization and sketching using a shared digital whiteboard. To prevent the influences of different sketching tools on design outputs, we employed digital sketching for both environments. The interactions between collaborators were identified in three behaviors: verbal only, sketch only, and mixed communication (verbal and sketch). The consequences revealed a higher level of IBS when mixed communication took place in distributed conditions than in co-located conditions. Comparably, the occurrence of IBS increased when participants solely utilized sketching as the interaction approach within the co-located setting. A mixed communication method combining verbalization and sketching might lead to more coordinated cognitive processes when in physical isolation. Design collaborators are inclined to adjust their interaction behaviors in order to adapt to different design environments, strengthen the exchange of ideas, and construct design consensus. Overall, the present paper discussed the performance of virtual collaborative design based on a neurocognitive perspective, contributing valuable insights for the future intervention design that promotes effective virtual teamwork.

The role of mindfulness on theta inter-brain synchrony during cooperation feedback processing: An EEG-based hyperscanning study

Mindfulness appears to improve empathy and understanding in relationships, which are necessary for successful cooperation. However, the impact of mindfulness on cooperation has not been fully studied. This study used hyperscanning technique to examine the effect of mindfulness on the inter-brain synchrony of interacting individuals during the cooperative tasks. Forty-one dyads were randomly assigned to a mindfulness group or a non-mindfulness group. Dyads of the mindfulness group performed a short mindfulness exercise following a 15-minute mindfulness audio guidance. Dyads of the non-mindfulness group were instructed to rest quietly with their eyes closed. Then, simultaneously and continuously EEG was recorded from all dyads when they completed a computer-based cooperative game task. Reaction times (RTs) and success rates were used to indicate the behavioral performance, and phase locking value (PLV) was used to indicate the inter-brain synchrony. The results showed that (1) Greater theta inter-brain synchrony during the cooperative computer game tasks was observed in the mindfulness group than in the non-mindfulness group; (2) Greater theta inter-brain synchrony was observed in the successful cooperation conditions as compared to those in the failure cooperation conditions; (3) Greater theta inter-brain synchrony was observed at the frontal region as compared to those at the parietal-occipital region in the successful cooperation condition. The results expand the neural basis of the effects of mindfulness on cooperation feedback processing. (AU)

Client-counselor behavioral and inter-brain synchronization among dismissing and secure clients and its association with alliance quality and outcome.

Objective This study aimed to explore whether behavioral synchrony (BS) and inter-brain synchrony (IBS) could serve as potential biomarkers for alliance quality or outcomes among clients with different adult attachment styles. Method: We assessed the clients' self-report working alliance and clinical outcomes as well as simultaneously measured BS using motion energy analysis (MEA) and IBS with functional near-infrared spectroscopy (fNIRS) among 37 secure (N = 21) or dismissing (N = 16) clients with their counselors during the first psychological counseling meeting. Results: Dismissing dyads manifested significantly higher late-stage counselor-led and client-led IBS (p = .018) than secure dyads. Adult attachment style served as the moderators in the correlation of both whole-stage client-led BS with bond dimension of alliance (p = .015) as well as in the correlation of both whole-stage no-lag IBS with CORE-10 score changes (p = .022). Moreover, increases in the whole-stage client-led BS were significantly associated with decreases in early-stage, late-stage and whole-stage no-lag IBS (all ps ≤ 0.01). Conclusion: These findings revealed the potentially impeding role of interpersonal synchrony in alliance quality for dismissing clients, at least during the first psychological counseling meetings. They also might partially validate the relationship between different modalities of interpersonal synchrony.

The role of mindfulness on theta inter-brain synchrony during cooperation feedback processing: An EEG-based hyperscanning study.

Mindfulness appears to improve empathy and understanding in relationships, which are necessary for successful cooperation. However, the impact of mindfulness on cooperation has not been fully studied. This study used hyperscanning technique to examine the effect of mindfulness on the inter-brain synchrony of interacting individuals during the cooperative tasks. Forty-one dyads were randomly assigned to a mindfulness group or a non-mindfulness group. Dyads of the mindfulness group performed a short mindfulness exercise following a 15-minute mindfulness audio guidance. Dyads of the non-mindfulness group were instructed to rest quietly with their eyes closed. Then, simultaneously and continuously EEG was recorded from all dyads when they completed a computer-based cooperative game task. Reaction times (RTs) and success rates were used to indicate the behavioral performance, and phase locking value (PLV) was used to indicate the inter-brain synchrony. The results showed that (1) Greater theta inter-brain synchrony during the cooperative computer game tasks was observed in the mindfulness group than in the non-mindfulness group; (2) Greater theta inter-brain synchrony was observed in the successful cooperation conditions as compared to those in the failure cooperation conditions; (3) Greater theta inter-brain synchrony was observed at the frontal region as compared to those at the parietal-occipital region in the successful cooperation condition. The results expand the neural basis of the effects of mindfulness on cooperation feedback processing.

HyperOptoNet: a MATLAB-based toolbox for inter-brain neuronal synchrony analysis using fNIRS hyperscanning.

Significance: We developed a MATLAB-based toolbox for the analysis of inter-brain synchrony (IBS) and performed an experimental study to confirm its performance. To the best of our knowledge, this is the first toolbox for IBS based on functional near-infrared spectroscopy (fNIRS) hyperscanning data that visually shows the results on two three-dimensional (3D) head models. Aim: Research on IBS using fNIRS hyperscanning is a nascent but expanding field. Although various analysis toolboxes for fNIRS exist, none can show inter-brain neuronal synchrony on a 3D head model. In 2019 and 2020, we released two MATLAB toolboxes named OptoNet I and II, which have helped researchers to analyze functional brain networks using fNIRS. We developed a MATLAB-based toolbox named HyperOptoNet to overcome the limitation of the previous OptoNet series. Approach: The developed HyperOptoNet can easily analyze inter-brain cortical connectivity using fNIRS hyperscanning signals simultaneously measured from two people at the same time. The connectivity results can be easily recognized by representing inter-brain neuronal synchrony with colored lines that are visually expressed on two standard head models. Results: To evaluate the performance of the developed toolbox, we conducted an fNIRS hyperscanning study of 32 healthy adults. The fNIRS hyperscanning data were measured while the subjects performed traditional, paper-and-pencil-based, cognitive tasks or interactive, computer-assisted, cognitive tasks (ICT). The results visualized different inter-brain synchronization patterns according to the interactive nature of the given tasks; a more extensive inter-brain network was seen with the ICT. Conclusions: The developed toolbox has good performance of IBS analysis and helps even unskilled researchers to easily analyze fNIRS hyperscanning data.

Mother-Infant Brain-to-Brain Synchrony Patterns Reflect Caregiving Profiles.

Biobehavioral synchrony, the coordination of physiological and behavioral signals between mother and infant during social contact, tunes the child's brain to the social world. Probing this mechanism from a two-brain perspective, we examine the associations between patterns of mother-infant inter-brain synchrony and the two well-studied maternal behavioral orientations-sensitivity and intrusiveness-which have repeatedly been shown to predict positive and negative socio-emotional outcomes, respectively. Using dual-electroencephalogram (EEG) recordings, we measure inter-brain connectivity between 60 mothers and their 5- to 12-month-old infants during face-to-face interaction. Thirty inter-brain connections show significantly higher correlations during the real mother-infant face-to-face interaction compared to surrogate data. Brain-behavior correlations indicate that higher maternal sensitivity linked with greater mother-infant neural synchrony, whereas higher maternal intrusiveness is associated with lower inter-brain coordination. Post hoc analysis reveals that the mother-right-frontal-infant-left-temporal connection is particularly sensitive to the mother's sensitive style, while the mother-left-frontal-infant-right-temporal connection indexes the intrusive style. Our results support the perspective that inter-brain synchrony is a mechanism by which mature brains externally regulate immature brains to social living and suggest that one pathway by which sensitivity and intrusiveness exert their long-term effect may relate to the provision of coordinated inputs to the social brain during its sensitive period of maturation.

Mobile fNIRS for exploring inter-brain synchrony across generations and time.

While still relatively rare, longitudinal hyperscanning studies are exceptionally valuable for documenting changes in inter-brain synchrony, which may in turn underpin how behaviors develop and evolve in social settings. The generalizability and ecological validity of this experimental approach hinges on the selected imaging technique being mobile-a requirement met by functional near-infrared spectroscopy (fNIRS). fNIRS has most frequently been used to examine the development of inter-brain synchrony and behavior in child-parent dyads. In this position paper, we contend that dedicating attention to longitudinal and intergenerational hyperscanning stands to benefit the fields of social and cognitive neuroscience more broadly. We argue that this approach is particularly relevant for understanding the neural mechanisms underpinning intergenerational social dynamics, and potentially for benchmarking progress in psychological and social interventions, many of which are situated in intergenerational contexts. In line with our position, we highlight areas of intergenerational research that stand to be enhanced by longitudinal hyperscanning with mobile devices, describe challenges that may arise from measuring across generations in the real world, and offer potential solutions.

Dynamic Inter-Brain Networks Correspond With Specific Communication Behaviors: Using Functional Near-Infrared Spectroscopy Hyperscanning During Creative and Non-creative Communication.

Social interaction is a dynamic and variable process. However, most hyperscanning studies implicitly assume that inter-brain synchrony (IBS) is constant and rarely investigate the temporal variability of the multi-brain networks. In this study, we used sliding windows and k-mean clustering to obtain a set of representative inter-brain network states during different group communication tasks. By calculating the network parameters and temporal occurrence of the inter-brain states, we found that dense efficient interbrain states and sparse inefficient interbrain states appeared alternately and periodically, and the occurrence of efficient interbrain states was positively correlated with collaborative behaviors and group performance. Moreover, compared to common communication, the occurrence of efficient interbrain states and state transitions were significantly higher during creative communication, indicating a more active and intertwined neural network. These findings may indicate that there is a close correspondence between inter-brain network states and social behaviors, contributing to the flourishing literature on group communication.

The Role of Neurobiological Bases of Dyadic Emotion Regulation in the Development of Psychopathology: Cross-Brain Associations Between Parents and Children.

Daily interactions between parents and children play a large role in children's emotional development and mental health. Thus, it is important to investigate the neural mechanisms underlying this association within the context of these dyadic social interactions. We suggest that examining cross-brain associations, coordinated brain responses, among parents and children increases our understanding of patterns of social and emotion-related processes that occur during parent-child interactions, which may influence the development of child emotion regulation and psychopathology. Therefore, we extend the Parent-Child Emotion Regulation Dynamics Model (Morris et al., in: Cole and Hollenstein (eds) Dynamics of emotion regulation: A matter of time, Taylor & Francis, 2018) to include cross-brain associations involved in dyadic emotion regulation during parent-child social emotional interactions and discuss how this model can inform future research and its broader applications.

Corrigendum: Interactive Brain Activity: Review and Progress on EEG-Based Hyperscanning in Social Interactions.

[This corrects the article DOI: 10.3389/fpsyg.2018.01862.].

Inter-brain synchrony in teams predicts collective performance.

Despite decades of research in economics and psychology attempting to identify ingredients that make up successful teams, neuroscientists have only just begun to study how multiple brains interact. Recent research has shown that people's brain activity becomes synchronized with others' (inter-brain synchrony) during social engagement. However, little is known as to whether inter-brain synchrony relates to collective behavior within teams. Here, we merge the nascent field of group neuroscience with the extant literature of team dynamics and collective performance. We recruited 174 participants in groups of 4 and randomly assigned them to complete a series of problem-solving tasks either independently or as a team, while simultaneously recording each person's brain activity using an electroencephalography hyperscanning setup. This design allowed us to examine the relationship between group identification and inter-brain synchrony in explaining collective performance. As expected, teammates identified more strongly with one another, cooperated more on an economic game, and outperformed the average individual on most problem-solving tasks. Crucially, inter-brain synchrony, but not self-reported group identification, predicted collective performance among teams. These results suggest that inter-brain synchrony can be informative in understanding collective performance among teams where self-report measures may fail to capture behavior.

A Multi-Brain Framework for Social Interaction.

Social interaction can be seen as a dynamic feedback loop that couples action, reaction, and internal cognitive processes across individual agents. A fuller understanding of the social brain requires a description of how the neural dynamics across coupled brains are linked and how they coevolve over time. We elaborate a multi-brain framework that considers social interaction as an integrated network of neural systems that dynamically shape behavior, shared cognitive states, and social relationships. We describe key findings from multi-brain experiments in humans and animal models that shed new light on the function of social circuits in health and disease. Finally, we discuss recent progress in elucidating the cellular-level mechanisms underlying inter-brain neural dynamics and outline key areas for future research.

Inter-brain synchrony in mother-child dyads during cooperation: An fNIRS hyperscanning study.

Coordinated brain activity between individuals, or inter-brain synchrony, has been shown to increase during cooperation and correlate with cooperation success. However, few studies have examined parent-child inter-brain synchrony and whether it is associated with meaningful aspects of the parent-child relationship. Here, we measured inter-brain synchrony in the right prefrontal (PFC) and temporal cortices in mother-child dyads while they engaged in a cooperative and independent task. We tested whether inter-brain synchrony in mother-child dyads (1) increases during cooperation, (2) differs in mother-son versus mother-daughter dyads, and (3) is related to cooperation performance and the attachment relationship. Overall inter-brain synchrony in the right hemisphere, and the right dorsolateral and frontopolar PFC in particular, was higher during cooperation. Mother-son dyads showed less inter-brain synchrony during the independent task and a stronger increase in synchrony in response to cooperation than mother-daughter dyads. Lastly, we did not find strong evidence for links between inter-brain synchrony and child attachment. Mother-child cooperation may increase overall inter-brain synchrony, although differently for mother-son versus mother-daughter dyads. More research is needed to better understand the potential role of overall inter-brain synchrony in mother-child cooperation, and the potential link between inter-brain synchrony and attachment.

Interactive Brain Activity: Review and Progress on EEG-Based Hyperscanning in Social Interactions.

When individuals interact with others, perceived information is transmitted among their brains. The EEG-based hyperscanning technique, which provides an approach to explore dynamic brain activities between two or more interactive individuals and their underlying neural mechanisms, has been applied to study different aspects of social interactions since 2010. Recently there has been an increase in research on EEG-based hyperscanning of social interactions. This paper summarizes the application of EEG-based hyperscanning on the dynamic brain activities during social interactions according to the experimental designs and contents, discusses the possibility of applying inter-brain synchrony to social communication systems and analyzes the contributions and the limitations of these investigations. Furthermore, this paper sheds light on some new challenges to future EEG-based hyperscanning studies and the emerging field of EEG-based hyperscanning for pursuing the broader research field of social interactions.

Inter-brain synchrony and cooperation context in interactive decision making.

People engaged in interactive decision making rely on prior decision behaviors by other persons to make new choices and they exhibit inter-brain synchrony between each other. The functional meanings of such inter-brain synchrony, however, remains obscure. In the present study, dyads (15 pairs, all female) played the Prisoner's Dilemma game while their brain activities were recorded simultaneously by electroencephalography (EEG)-based hyperscanning technique. We manipulated the context of the game with higher versus lower cooperation index (HCI vs. LCI) and to each participant, we depicted the interaction as involving either another human partner or a machine (H-H vs. H-M). The results showed a higher cooperation rate and larger theta/alpha-band inter-brain synchrony in condition H-H than in H-M. In the condition H-H, there were larger centrofrontal theta-band and centroparietal alpha-band inter-brain synchrony in tasks set for high cooperation (HCI vs. LCI). Enhanced inter-brain synchrony covaried with increased cooperative choices observed between LCI and HCI. Furthermore, a subjective measure of perceived cooperativeness mediated the relationship between game context and inter-brain synchrony. These findings provide evidence for a role of cooperation on inter-brain synchrony during interactive decision making, and suggest distinct underlying neural processes recruited by cooperation contexts to enable high-level social cognitive processing in decision making.

Oxytocin enhances inter-brain synchrony during social coordination in male adults.

Recent brain imaging research has revealed oxytocin (OT) effects on an individual's brain activity during social interaction but tells little about whether and how OT modulates the coherence of inter-brain activity related to two individuals' coordination behavior. We developed a new real-time coordination game that required two individuals of a dyad to synchronize with a partner (coordination task) or with a computer (control task) by counting in mind rhythmically. Electroencephalography (EEG) was recorded simultaneously from a dyad to examine OT effects on inter-brain synchrony of neural activity during interpersonal coordination. Experiment 1 found that dyads showed smaller interpersonal time lags of counting and greater inter-brain synchrony of alpha-band neural oscillations during the coordination (vs control) task and these effects were reliably observed in female but not male dyads. Moreover, the increased alpha-band inter-brain synchrony predicted better interpersonal behavioral synchrony across all participants. Experiment 2, using a double blind, placebo-controlled between-subjects design, revealed that intranasal OT vs placebo administration in male dyads improved interpersonal behavioral synchrony in both the coordination and control tasks but specifically enhanced alpha-band inter-brain neural oscillations during the coordination task. Our findings provide first evidence that OT enhances inter-brain synchrony in male adults to facilitate social coordination.