The paradox of social avoidance and the yearning for understanding: Elevated interbrain synchrony among socially avoidant individuals during expression of negative emotions.

Social avoidance refers to the tendency to be alone and non-participating to social interactions, which is considered to hamper health interpersonal relationship. However, the neural underpinnings of social and emotional interactions among social avoidant individuals have not been fully studied. In the present study, we used EEG hyperscanning technology to investigate the brain activity and its synchronization of 25 socially avoidant dyads and 28 comparison dyads during an emotional communication task. The emotional communication task consisted of the emotional processing stage and emotional interaction stage. Event-related potentials (ERPs) of the senders during the emotional processing stage and the interbrain synchrony (IBS) of the dyads during the emotional interaction stage were analyzed. Results showed that (1) socially avoidant group showed higher beta, theta and gamma IBS in the negative condition than in the positive and neutral condition; (2) in positive condition, the N1 and LPP amplitudes during the emotional processing stage of socially avoidant individuals were negatively correlated with the IBS within dyads during the emotional communication stage. The findings suggest that the dysfunctional emotional interaction of social avoidant individuals may be attributed to the negative impact of emotional stimuli processing during emotional communication.

Measuring information alignment in hyperscanning research with representational analyses: moving beyond interbrain synchrony.

Hyperscanning, which enables the recording of brain activity from multiple individuals simultaneously, has been increasingly used to investigate the neuropsychological processes underpinning social interaction. Previous hyperscanning research has primarily focused on interbrain synchrony, demonstrating an enhanced alignment of brain waves across individuals during social interaction. However, using EEG hyperscanning simulations, we here show that interbrain synchrony has low sensitivity to information alignment across people. Surprisingly, interbrain synchrony remains largely unchanged despite manipulating whether two individuals are seeing same or different things at the same time. Furthermore, we show that hyperscanning recordings do contain indices of interpersonal information alignment and that they can be captured using representational analyses. These findings highlight major limitations of current hyperscanning research and offer a promising alternative for investigating interactive minds.

Interbrain substrates of role switching during mother-child interaction.

Mother-child interaction is highly dynamic and reciprocal. Switching roles in these back-and-forth interactions serves as a crucial feature of reciprocal behaviors while the underlying neural entrainment is still not well-studied. Here, we designed a role-controlled cooperative task with dual EEG recording to explore how differently two brains interact when mothers and children hold different roles. When children were actors and mothers were observers, mother-child interbrain synchrony emerged primarily within the theta oscillations and the frontal lobe, which highly correlated with children's attachment to their mothers (self-reported by mothers). When their roles were reversed, this synchrony was shifted to the alpha oscillations and the central area and associated with mothers' perception of their relationship with their children. The results suggested an observer-actor neural alignment within the actor's oscillations, which was related to the actor-toward-observer emotional bonding. Our findings contribute to the understanding of how interbrain synchrony is established and dynamically changed during mother-child reciprocal interaction.

Parenting links to parent-child interbrain synchrony: a real-time fNIRS hyperscanning study.

Parent-child interaction is crucial for children's cognitive and affective development. While bio-synchrony models propose that parenting influences interbrain synchrony during interpersonal interaction, the brain-to-brain mechanisms underlying real-time parent-child interactions remain largely understudied. Using functional near-infrared spectroscopy, we investigated interbrain synchrony in 88 parent-child dyads (Mage children = 8.07, 42.0% girls) during a collaborative task (the Etch-a-Sketch, a joint drawing task). Our findings revealed increased interbrain synchrony in the dorsolateral prefrontal cortex and temporo-parietal areas during interactive, collaborative sessions compared to non-interactive, resting sessions. Linear regression analysis demonstrated that interbrain synchrony in the left temporoparietal junction was associated with enhanced dyadic collaboration, shared positive affect, parental autonomy support, and parental emotional warmth. These associations remained significant after controlling for demographic variables including child age, child gender, and parent gender. Additionally, differences between fathers and mothers were observed. These results highlight the significant association between brain-to-brain synchrony in parent-child dyads, the quality of the parent-child relationship, and supportive parenting behaviors. Interbrain synchrony may serve as a neurobiological marker of real-time parent-child interaction, potentially underscoring the pivotal role of supportive parenting in shaping these interbrain synchrony mechanisms.

Dynamic mutual predictions during social learning: A computational and interbrain model.

During social interactions, we constantly learn about the thoughts, feelings, and personality traits of our interaction partners. Learning in social interactions is critical for bond formation and acquiring knowledge. Importantly, this type of learning is typically bi-directional, as both partners learn about each other simultaneously. Here we review the literature on social learning and propose a new computational and neural model characterizing mutual predictions that take place within and between interactions. According to our model, each partner in the interaction attempts to minimize the prediction error of the self and the interaction partner. In most cases, these inferential models become similar over time, thus enabling mutual understanding to develop. At the neural level, this type of social learning may be supported by interbrain plasticity, defined as a change in interbrain coupling over time in neural networks associated with social learning, among them the mentalizing network, the observation-execution system, and the hippocampus. The mutual prediction model constitutes a promising means of providing empirically verifiable accounts of how relationships develop over time.

Quantification of inter-brain coupling: A review of current methods used in haemodynamic and electrophysiological hyperscanning studies.

Hyperscanning is a form of neuroimaging experiment where the brains of two or more participants are imaged simultaneously whilst they interact. Within the domain of social neuroscience, hyperscanning is increasingly used to measure inter-brain coupling (IBC) and explore how brain responses change in tandem during social interaction. In addition to cognitive research, some have suggested that quantification of the interplay between interacting participants can be used as a biomarker for a variety of cognitive mechanisms aswell as to investigate mental health and developmental conditions including schizophrenia, social anxiety and autism. However, many different methods have been used to quantify brain coupling and this can lead to questions about comparability across studies and reduce research reproducibility. Here, we review methods for quantifying IBC, and suggest some ways moving forward. Following the PRISMA guidelines, we reviewed 215 hyperscanning studies, across four different brain imaging modalities: functional near-infrared spectroscopy (fNIRS), functional magnetic resonance (fMRI), electroencephalography (EEG) and magnetoencephalography (MEG). Overall, the review identified a total of 27 different methods used to compute IBC. The most common hyperscanning modality is fNIRS, used by 119 studies, 89 of which adopted wavelet coherence. Based on the results of this literature survey, we first report summary statistics of the hyperscanning field, followed by a brief overview of each signal that is obtained from each neuroimaging modality used in hyperscanning. We then discuss the rationale, assumptions and suitability of each method to different modalities which can be used to investigate IBC. Finally, we discuss issues surrounding the interpretation of each method.

Is neuroimaging ready for the classroom? A systematic review of hyperscanning studies in learning.

Whether education research can be informed by findings from neuroscience studies has been hotly debated since Bruer's (1997) famous claim that neuroscience and education are "a bridge too far". However, this claim came before recent advancements in portable electroencephalography (EEG) and functional near-infrared spectroscopy (fNIRS) technologies, and second-person neuroscience techniques that brought about significant headway in understanding instructor-learner interactions in the classroom. To explore whether neuroscience and education are still two very separate fields, we systematically review 15 hyperscanning studies that were conducted in real-world classrooms or that implemented a teaching-learning task to investigate instructor-learner dynamics. Findings from this investigation illustrate that inter-brain synchrony between instructor and learner is an additional and valuable dimension to understand the complex web of instructor- and learner-related variables that influence learning. Importantly, these findings demonstrate the possibility of conducting real-world classroom studies with portable neuroimaging techniques and highlight the potential of such studies in providing translatable real-world implications. Once thought of as incompatible, a successful coupling between neuroscience and education is now within sight.

Hyperscanning Studies on Interbrain Synchrony and Child Development: A Narrative Review.

Social interactions between parents and children are closely linked with children's development, and interbrain synchrony has been shown to be a neural marker of social interaction. However, to truly capture the essence of social interactions through interbrain synchrony, it is necessary to simultaneously discuss the parental and child brains and adequately record neurological signals during parent-child interactions in interactive tasks. In the current review, we have reviewed three main contents. First, we discuss the correlation between parent-child interbrain synchrony and the development of cognitive (e.g., emotion regulation, attention, and learning) and behavioral abilities (e.g., cooperation, problem-solving) in children. Second, we examine the different neural mechanisms of interbrain synchrony in mother-child and father-child interactions, aiming to highlight the separate roles of mother and father in child development. Last, we have integrated four methods to enhance interbrain synchrony, including communication patterns, nonverbal behavior, music, and multichannel stimulation. A significant correlation exists between parent-child interbrain synchrony and the development of children's cognitive and behavioral abilities. This summary may be useful for expanding researchers' and practitioners' understanding of the ways in which parenting and the parent-child relationship shape children' cognitive and behavioral abilities.

Pseudo-mutual gazing enhances interbrain synchrony during remote joint attention tasking.

INTRODUCTION: Mutual gaze enables people to share attention and increase engagement during social interactions through intentional and implicit messages. Although previous studies have explored gaze behaviors and neural mechanisms underlying in-person eye contact, the growing prevalence of remote communication has raised questions about how to establish mutual gaze remotely and how the brains of interacting individuals synchronize. METHODS: To address these questions, we conducted a study using eye trackers to create a pseudo-mutual gaze channel that mirrors the gazes of each interacting dyad on their respective remote screens. To demonstrate fluctuations in coupling across brains, we incorporated electroencephalographic hyperscanning techniques to simultaneously record the brain activity of interacting dyads engaged in a joint attention task in player-observer, collaborative, and competitive modes. RESULTS: Our results indicated that mutual gaze could improve the efficiency of joint attention activities among remote partners. Moreover, by employing the phase locking value, we could estimate interbrain synchrony (IBS) and observe low-frequency couplings in the frontal and temporal regions that varied based on the interaction mode. While dyadic gender composition significantly affected gaze patterns, it did not impact the IBS. CONCLUSION: These results provide insight into the neurological mechanisms underlying remote interaction through the pseudo-mutual gaze channel and have significant implications for developing effective online communication environments.

Trait mindful awareness predicts inter-brain coupling but not individual brain responses during naturalistic face-to-face interactions.

In recent years, the possible benefits of mindfulness meditation have sparked much public and academic interest. Mindfulness emphasizes cultivating awareness of our immediate experience and has been associated with compassion, empathy, and various other prosocial traits. However, neurobiological evidence pertaining to the prosocial benefits of mindfulness in social settings is sparse. In this study, we investigate neural correlates of trait mindful awareness during naturalistic dyadic interactions, using both intra-brain and inter-brain measures. We used the Muse headset, a portable electroencephalogram (EEG) device often used to support mindfulness meditation, to record brain activity from dyads as they engaged in naturalistic face-to-face interactions in a museum setting. While we did not replicate prior laboratory-based findings linking trait mindfulness to individual brain responses (N = 379 individuals), self-reported mindful awareness did predict dyadic inter-brain synchrony, in theta (~5-8 Hz) and beta frequencies (~26-27 Hz; N = 62 dyads). These findings underscore the importance of conducting social neuroscience research in ecological settings to enrich our understanding of how (multi-brain) neural correlates of social traits such as mindful awareness manifest during social interaction, while raising critical practical considerations regarding the viability of commercially available EEG systems.

Adolescent social anxiety undermines adolescent-parent interbrain synchrony during emotional processing: A hyperscanning study.

Social anxiety severely impacts adolescents' social interactions with others; however, the underlying neural mechanism has not been revealed. This study examined how adolescent's social anxiety level influences the interbrain synchrony within adolescent-parent dyads during emotional processing by using electroencephalograph (EEG) hyperscanning. A sample of 25 adolescent-parent dyads completed the picture processing task. Adolescents' ages ranged from 10 to 14 years old. The results showed that (1) at parietal areas, greater gamma interbrain synchrony was observed in the high social anxiety adolescent-parent dyads (HSAs) than the low social anxiety adolescent-parent dyads (LSAs) in the positive conditions. However, greater gamma interbrain synchrony of the picture processing task was observed in the LSAs than the HSAs in the negative conditions. (2) Compared with the neutral condition, LSAs induced greater interbrain synchronization in the negative condition than in the neutral condition at central and parietal areas. However, HSAs induced greater interbrain synchronization in the positive condition than in the negative condition at parietal areas. (3) HSAs induced greater interbrain synchronization at parietal areas than in the central areas in positive conditions. The results provide neurological evidence that the way parent and adolescent process different emotions in the same emotional episode could be affected by the adolescent's anxiety level.

Relations between family cohesion and adolescent-parent's neural synchrony in response to emotional stimulations.

BACKGROUND: The interaction between parent and adolescent is more challenging than in other age periods. Family cohesion seriously impacts parent-adolescent emotional interactions. However, the underlying neural mechanism has not been fully examined. This study examined the differences in the neural synchrony in response to emotional film clips between high and low family cohesion adolescent-parent dyads by using the electroencephalograph (EEG) hyperscanning. RESULTS: Simultaneously electroencephalograph (EEG) was recorded while 15 low family cohesion parent-adolescent dyads (LFCs)and 14 high family cohesion parent-adolescent dyads (HFCs)received different emotional induction when viewing film clips. Interbrain phase-locking-value (PLV) in gamma band was used to calculate parent-adolescent dyads' interbrain synchrony. Results showed that higher gamma interbrain synchrony was observed in the HFCs than the LFCs in the positive conditions. However, there was no significant difference between the HFCs and LFCs in other conditions. Also, the HFCs had significantly higher gamma interbrain synchrony in the positive conditions than in the negative conditions. CONCLUSION: Interbrain synchrony may represent an underlying neural mechanism of the parent-adolescent emotional bonding, which is the core of family cohesion.

Recent Trends in Non-invasive Neural Recording Based Brain-to-Brain Synchrony Analysis on Multidisciplinary Human Interactions for Understanding Brain Dynamics: A Systematic Review.

The study of brain-to-brain synchrony has a burgeoning application in the brain-computer interface (BCI) research, offering valuable insights into the neural underpinnings of interacting human brains using numerous neural recording technologies. The area allows exploring the commonality of brain dynamics by evaluating the neural synchronization among a group of people performing a specified task. The growing number of publications on brain-to-brain synchrony inspired the authors to conduct a systematic review using the PRISMA protocol so that future researchers can get a comprehensive understanding of the paradigms, methodologies, translational algorithms, and challenges in the area of brain-to-brain synchrony research. This review has gone through a systematic search with a specified search string and selected some articles based on pre-specified eligibility criteria. The findings from the review revealed that most of the articles have followed the social psychology paradigm, while 36% of the selected studies have an application in cognitive neuroscience. The most applied approach to determine neural connectivity is a coherence measure utilizing phase-locking value (PLV) in the EEG studies, followed by wavelet transform coherence (WTC) in all of the fNIRS studies. While most of the experiments have control experiments as a part of their setup, a small number implemented algorithmic control, and only one study had interventional or a stimulus-induced control experiment to limit spurious synchronization. Hence, to the best of the authors' knowledge, this systematic review solely contributes to critically evaluating the scopes and technological advances of brain-to-brain synchrony to allow this discipline to produce more effective research outcomes in the remote future.

Corrigendum: A Two-Person Neuroscience Approach for Social Anxiety: A Paradigm With Interbrain Synchrony and Neurofeedback.

[This corrects the article DOI: 10.3389/fpsyg.2021.568921.].

Cooperative Behavior Evokes Interbrain Synchrony in the Prefrontal and Temporoparietal Cortex: A Systematic Review and Meta-Analysis of fNIRS Hyperscanning Studies.

Single-brain neuroimaging studies have shown that human cooperation is associated with neural activity in frontal and temporoparietal regions. However, it remains unclear whether single-brain studies are informative about cooperation in real life, where people interact dynamically. Such dynamic interactions have become the focus of interbrain studies. An advantageous technique in this regard is functional near-infrared spectroscopy (fNIRS) because it is less susceptible to movement artifacts than more conventional techniques like electroencephalography (EEG) or functional magnetic resonance imaging (fMRI). We conducted a systematic review and the first quantitative meta-analysis of fNIRS hyperscanning of cooperation, based on thirteen studies with 890 human participants. Overall, the meta-analysis revealed evidence of statistically significant interbrain synchrony while people were cooperating, with large overall effect sizes in both frontal and temporoparietal areas. All thirteen studies observed significant interbrain synchrony in the prefrontal cortex (PFC), suggesting that this region is particularly relevant for cooperative behavior. The consistency in these findings is unlikely to be because of task-related activations, given that the relevant studies used diverse cooperation tasks. Together, the present findings support the importance of interbrain synchronization of frontal and temporoparietal regions in interpersonal cooperation. Moreover, the present article highlights the usefulness of meta-analyses as a tool for discerning patterns in interbrain dynamics.

What has social neuroscience learned from hyperscanning studies of spoken communication? A systematic review.

A growing body of literature examining the neurocognitive processes of interpersonal linguistic interaction indicates the emergence of neural alignment as participants engage in oral communication. However, questions have arisen whether the study results can be interpreted beyond observations of cortical functionality and extended to the mutual understanding between communicators. This review presents evidence from electroencephalography (EEG) and functional near-infrared spectroscopy (fNIRS) hyperscanning studies of interbrain synchrony (IBS) in which participants communicated via spoken language. The studies are classified into: knowledge sharing; turn-taking speech co-ordination; cooperation, problem-solving and creativity; and naturalistic discussion paradigms according to the type of interaction specified in each study. Alignment predominantly occurred in the frontal and temporo-parietal areas, which may reflect activation of the mirror and mentalizing systems. We argue that the literature presents a significant contribution to advancing our understanding of IBS and mutual understanding between communicators. We end with suggestions for future research, including analytical approaches and experimental conditions and hypothesize that brain-inspired neural networks are promising techniques for better understanding of IBS through hyperscanning.

Interbrain Synchrony of Team Collaborative Decision-Making: An fNIRS Hyperscanning Study.

In many situations, decision-making behaviors are mostly composed of team patterns (i.e., more than two persons). However, brain-based models that inform how team interactions contribute and impact team collaborative decision-making (TCDM) behavior, is lacking. To examine the neural substrates activated during TCDM in realistic, interpersonal interaction contexts, dyads were asked to model TCDM toward their opponent, in a multi-person prisoner's dilemma game, while neural activity was measured using functional near infrared spectroscopy. These experiments resulted in two main findings. First, there are different neural substrates between TCDM and ISDM, which were modulated by social environmental cues. i.e., the low incentive reward yielded higher activation within the left inferior frontal gyrus (IFG), in individual separately decision-making (ISDM) stage while the dorsolateral prefrontal cortex (DLPFC) and the middle frontopolar area was activated in TCDM stage. The high incentive reward evoked a higher interbrain synchrony (IBS) value in the right IFG in TCDM stage. Second, males showed higher activation in the DLPFC and the middle frontopolar area during ISDM, while females evoked higher IBS in the right IFG during TCDM. These sex effects suggest that in individual social dilemma situations, males and females may separately depend on non-social and social cognitive ability to make decisions, while in the social interaction situations of TCDM, females may depend on both social and non-social cognitive abilities. This study provide a compelling basis and interesting perspective for future neuroscience work of TCDM behaviors.

Neurophysiological Synchrony Between Children With Severe Physical Disabilities and Their Parents During Music Therapy.

Although physiological synchronization has been associated with the level of empathy in emotionally meaningful relationships, little is known about the interbrain synchrony between non-speaking children with severe disabilities and their familial caregivers. In a repeated measures observational study, we ascertained the degree of interbrain synchrony during music therapy in 10 child-parent dyads, where the children were non-speaking and living with severe motor impairments. Interbrain synchrony was quantified via measurements of spectral coherence and Granger causality between child and parent electroencephalographic (EEG) signals collected during ten 15-min music therapy sessions per dyad, where parents were present as non-participating, covert observers. Using cluster-based permutation tests, we found significant child-parent interbrain synchrony, manifesting most prominently across dyads in frontal brain regions within ß and low γ frequencies. Specifically, significant dyadic coherence was observed contra-laterally, between child frontal right and parental frontal left regions at ß and lower γ bands in empathy-related brain areas. Furthermore, significant Granger influences were detected bidirectionally (from child to parent and vice versa) in the same frequency bands. In all dyads, significant increases in session-specific coherence and Granger influences were observed over the time course of a music therapy session. The observed interbrain synchrony suggests a cognitive-emotional coupling during music therapy between child and parent that is responsive to change. These findings encourage further study of the socio-empathic capacity and interpersonal relationships formed between caregivers and non-speaking children with severe physical impairments.

Interacting brains coming in sync through their minds: an interbrain neurofeedback study.

Neurophysiological evidence shows that interpersonal action coordination is accompanied by interbrain synchronization (IBS). However, the functional significance of this association remains unclear. Using two experimental designs, we explored whether IBS is amenable to neurofeedback (NFB). Feedback was provided either as two balls approaching each other (so-called ball design), or as two pendula, each reflecting the oscillatory activity of one of the two participants (so-called pendulum design). The NFB was provided at delta (i.e., 2.5 Hz) and theta (i.e., 5 Hz) electroencephalography frequencies, and manipulated by enhanced and inverse feedback. We showed that the participants were able to increase IBS by using NFB, especially when it was fed back at the theta frequency. Apart from intra- and interbrain coupling, other oscillatory activities (e.g., power spectral density, peak amplitude, and peak frequency) also changed during the task compared with the rest. Moreover, all the measures showed specific correlations with the subjective postsurvey item scores, reflecting subjective feeling and appraisal. We conclude that the use of IBS for NFB might help in specifying the contribution of IBS to interpersonal action coordination and in providing important information about the neural mechanisms of social interaction and the causal dimension of IBS.

A Two-Person Neuroscience Approach for Social Anxiety: A Paradigm With Interbrain Synchrony and Neurofeedback.

Social anxiety disorder has been widely recognised as one of the most commonly diagnosed mental disorders. Individuals with social anxiety disorder experience difficulties during social interactions that are essential in the regular functioning of daily routines; perpetually motivating research into the aetiology, maintenance and treatment methods. Traditionally, social and clinical neuroscience studies incorporated protocols testing one participant at a time. However, it has been recently suggested that such protocols are unable to directly assess social interaction performance, which can be revealed by testing multiple individuals simultaneously. The principle of two-person neuroscience highlights the interpersonal aspect of social interactions that observes behaviour and brain activity from both (or all) constituents of the interaction, rather than analysing on an individual level or an individual observation of a social situation. Therefore, two-person neuroscience could be a promising direction for assessment and intervention of the social anxiety disorder. In this paper, we propose a novel paradigm which integrates two-person neuroscience in a neurofeedback protocol. Neurofeedback and interbrain synchrony, a branch of two-person neuroscience, are discussed in their own capacities for their relationship with social anxiety disorder and relevance to the paradigm. The newly proposed paradigm sets out to assess the social interaction performance using interbrain synchrony between interacting individuals, and to employ a multi-user neurofeedback protocol for intervention of the social anxiety.