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.

Domain-specific and domain-general neural network engagement during human-robot interactions.

To what extent do domain-general and domain-specific neural network engagement generalize across interactions with human and artificial agents? In this exploratory study, we analysed a publicly available functional MRI (fMRI) data set (n = 22) to probe the similarities and dissimilarities in neural architecture while participants conversed with another person or a robot. Incorporating trial-by-trial dynamics of the interactions, listening and speaking, we used whole-brain, region-of-interest and functional connectivity analyses to test response profiles within and across social or non-social, domain-specific and domain-general networks, that is, the person perception, theory-of-mind, object-specific, language and multiple-demand networks. Listening to a robot compared to a human resulted in higher activation in the language network, especially in areas associated with listening comprehension, and in the person perception network. No differences in activity of the theory-of-mind network were found. Results from the functional connectivity analysis showed no difference between interactions with a human or robot in within- and between-network connectivity. Together, these results suggest that although largely similar regions are activated when speaking to a human and to a robot, activity profiles during listening point to a dissociation at a lower level or perceptual level, but not higher order cognitive level.

The promise of two-person neuroscience for developmental psychiatry: using interaction-based sociometrics to identify disorders of social interaction.

Social interactions are fundamental for human development, and disordered social interactions are pervasive in many psychiatric disorders. Recent advances in 'two-person neuroscience' have provided new tools for characterising social interactions. Accordingly, interaction-based 'sociometrics' hold great promise for developmental psychology and psychiatry, particularly in the early identification of social disorders. DECLARATION OF INTEREST: None.

Frontal temporal and parietal systems synchronize within and across brains during live eye-to-eye contact.

Human eye-to-eye contact is a primary source of social cues and communication. In spite of the biological significance of this interpersonal interaction, the underlying neural processes are not well-understood. This knowledge gap, in part, reflects limitations of conventional neuroimaging methods, including solitary confinement in the bore of a scanner and minimal tolerance of head movement that constrain investigations of natural, two-person interactions. However, these limitations are substantially resolved by recent technical developments in functional near-infrared spectroscopy (fNIRS), a non-invasive spectral absorbance technique that detects changes in blood oxygen levels in the brain by using surface-mounted optical sensors. Functional NIRS is tolerant of limited head motion and enables simultaneous acquisitions of neural signals from two interacting partners in natural conditions. We employ fNIRS to advance a data-driven theoretical framework for two-person neuroscience motivated by the Interactive Brain Hypothesis which proposes that interpersonal interaction between individuals evokes neural mechanisms not engaged during solo, non-interactive, behaviors. Within this context, two specific hypotheses related to eye-to-eye contact, functional specificity and functional synchrony, were tested. The functional specificity hypothesis proposes that eye-to-eye contact engages specialized, within-brain, neural systems; and the functional synchrony hypothesis proposes that eye-to-eye contact engages specialized, across-brain, neural processors that are synchronized between dyads. Signals acquired during eye-to-eye contact between partners (interactive condition) were compared to signals acquired during mutual gaze at the eyes of a picture-face (non-interactive condition). In accordance with the specificity hypothesis, responses during eye-to-eye contact were greater than eye-to-picture gaze for a left frontal cluster that included pars opercularis (associated with canonical language production functions known as Broca's region), pre- and supplementary motor cortices (associated with articulatory systems), as well as the subcentral area. This frontal cluster was also functionally connected to a cluster located in the left superior temporal gyrus (associated with canonical language receptive functions known as Wernicke's region), primary somatosensory cortex, and the subcentral area. In accordance with the functional synchrony hypothesis, cross-brain coherence during eye-to-eye contact relative to eye-to-picture gaze increased for signals originating within left superior temporal, middle temporal, and supramarginal gyri as well as the pre- and supplementary motor cortices of both interacting brains. These synchronous cross-brain regions are also associated with known language functions, and were partner-specific (i.e., disappeared with randomly assigned partners). Together, both within and across-brain neural correlates of eye-to-eye contact included components of previously established productive and receptive language systems. These findings reveal a left frontal, temporal, and parietal long-range network that mediates neural responses during eye-to-eye contact between dyads, and advance insight into elemental mechanisms of social and interpersonal interactions.

Functional parcellation of the human primary somatosensory cortex to natural touch.

Despite the significance of human touch, brain responses to interpersonal manual touch have been rarely investigated. We used functional magnetic resonance imaging to study brain activity in eight healthy adults whose left hand was touched by two individuals, in separate runs and in 20-s blocks, either by holding, smoothing, or poking. Acceleration was measured from both the subject's and the touching person's hands for postimaging control of the stimuli. Independent component analysis of the functional magnetic resonance imaging data unraveled three functional networks involving the primary somatosensory cortex (SI). One network comprised the contralateral and another the ipsilateral Brodmann area 3. The third network included area 2 bilaterally, left-hemisphere middle temporal gyrus and dorsolateral prefrontal regions, ventral prefrontal cortices bilaterally, and middle cingulate cortex. The response shapes and polarities varied between the three networks. The contralateral area 3 differentiated the responses between the three types of touch stimuli, and the response magnitudes depended on the variability of the touch within each block. However, the responses of the other two networks were strikingly similar to all stimuli. The subjects' reports on the pleasantness of the touch did not correlate with the characteristics of the SI responses. These findings imply area-specific processing of the natural human touch in three networks including the SI cortex, with only area 2 connected to a functional network of brain areas that may support social interaction.

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.

Learning from others is good, with others is better: the role of social interaction in human acquisition of new knowledge.

Learning in humans is highly embedded in social interaction: since the very early stages of our lives, we form memories and acquire knowledge about the world from and with others. Yet, within cognitive science and neuroscience, human learning is mainly studied in isolation. The focus of past research in learning has been either exclusively on the learner or (less often) on the teacher, with the primary aim of determining developmental trajectories and/or effective teaching techniques. In fact, social interaction has rarely been explicitly taken as a variable of interest, despite being the medium through which learning occurs, especially in development, but also in adulthood. Here, we review behavioural and neuroimaging research on social human learning, specifically focusing on cognitive models of how we acquire semantic knowledge from and with others, and include both developmental as well as adult work. We then identify potential cognitive mechanisms that support social learning, and their neural correlates. The aim is to outline key new directions for experiments investigating how knowledge is acquired in its ecological niche, i.e. socially, within the framework of the two-person neuroscience approach. This article is part of the theme issue 'Concepts in interaction: social engagement and inner experiences'.

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.].

Bidirectional Connectivity Between Broca's Area and Wernicke's Area During Interactive Verbal Communication.

Aim: This investigation aims to advance the understanding of neural dynamics that underlies live and natural interactions during spoken dialogue between two individuals. Introduction: The underlying hypothesis is that functional connectivity between canonical speech areas in the human brain will be modulated by social interaction. Methods: Granger causality was applied to compare directional connectivity across Broca's and Wernicke's areas during verbal conditions consisting of interactive and noninteractive communication. Thirty-three pairs of healthy adult participants alternately talked and listened to each other while performing an object naming and description task that was either interactive or not during hyperscanning with functional near-infrared spectroscopy (fNIRS). In the noninteractive condition, the speaker named and described a picture-object without reference to the partner's description. In the interactive condition, the speaker performed the same task but included an interactive response about the preceding comments of the partner. Causality measures of hemodynamic responses from Broca's and Wernicke's areas were compared between real, surrogate, and shuffled trials within dyads. Results: The interactive communication was characterized by bidirectional connectivity between Wernicke's and Broca's areas of the listener's brain. Whereas this connectivity was unidirectional in the speaker's brain. In the case of the noninteractive condition, both speaker's and listener's brains showed unidirectional top-down (Broca's area to Wernicke's area) connectivity. Conclusion: Together, directional connectivity as determined by Granger analysis reveals bidirectional flow of neuronal information during dynamic two-person verbal interaction for processes that are active during listening (reception) and not during talking (production). Findings are consistent with prior contrast findings (general linear model) showing neural modulation of the receptive language system associated with Wernicke's area during a two-person live interaction. Impact statement The neural dynamics that underlies real-life social interactions is an emergent topic of interest. Dynamically coupled cross-brain neural mechanisms between interacting partners during verbal dialogue have been shown within Wernicke's area. However, it is not known how within-brain long-range neural mechanisms operate during these live social functions. Using Granger causality analysis, we show bidirectional neural activity between Broca's and Wernicke's areas during interactive dialogue compared with a noninteractive control task showing only unidirectional activity. Findings are consistent with an Interactive Brain Model where long-range neural mechanisms process interactive processes associated with rapid and spontaneous spoken social cues.

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.

Social interaction is a catalyst for adult human learning in online contexts.

Human learning is highly social.1-3 Advances in technology have increasingly moved learning online, and the recent coronavirus disease 2019 (COVID-19) pandemic has accelerated this trend. Online learning can vary in terms of how "socially" the material is presented (e.g., live or recorded), but there are limited data on which is most effective, with the majority of studies conducted on children4-8 and inconclusive results on adults.9,10 Here, we examine how young adults (aged 18-35) learn information about unknown objects, systematically varying the social contingency (live versus recorded lecture) and social richness (viewing the teacher's face, hands, or slides) of the learning episodes. Recall was tested immediately and after 1 week. Experiment 1 (n = 24) showed better learning for live presentation and a full view of the teacher (hands and face). Experiment 2 (n = 27; pre-registered) replicated the live-presentation advantage. Both experiments showed an interaction between social contingency and social richness: the presence of social cues affected learning differently depending on whether teaching was interactive or not. Live social interaction with a full view of the teacher's face provided the optimal setting for learning new factual information. However, during observational learning, social cues may be more cognitively demanding11 and/or distracting,12-14 resulting in less learning from rich social information if there is no interactivity. We suggest that being part of a genuine social interaction catalyzes learning, possibly via mechanisms of joint attention,15 common ground,16 or (inter-)active discussion, and as such, interactive learning benefits from rich social settings.17,18.

Imaging Real-Time Tactile Interaction With Two-Person Dual-Coil fMRI.

Studies of brain mechanisms supporting social interaction are demanding because real interaction only occurs when persons are in contact. Instead, most brain imaging studies scan subjects individually. Here we present a proof-of-concept demonstration of two-person blood oxygenation dependent (BOLD) imaging of brain activity from two individuals interacting inside the bore of a single MRI scanner. We developed a custom 16-channel (8 + 8 channels) two-helmet coil with two separate receiver-coil pairs providing whole-brain coverage, while bringing participants into a shared physical space and realistic face-to-face contact. Ten subject pairs were scanned with the setup. During the experiment, subjects took turns in tapping each other's lip versus observing and feeling the taps timed by auditory instructions. Networks of sensorimotor brain areas were engaged alternatingly in the subjects during executing motor actions as well as observing and feeling them; these responses were clearly distinguishable from the auditory responses occurring similarly in both participants. Even though the signal-to-noise ratio of our coil system was compromised compared with standard 32-channel head coils, our results show that the two-person fMRI scanning is feasible for studying the brain basis of social interaction.

Neural processes for live pro-social dialogue between dyads with socioeconomic disparity.

An emerging theoretical framework suggests that neural functions associated with stereotyping and prejudice are associated with frontal lobe networks. Using a novel neuroimaging technique, functional near-infrared spectroscopy (fNIRS), during a face-to-face live communication paradigm, we explore an extension of this model to include live dynamic interactions. Neural activations were compared for dyads of similar and dissimilar socioeconomic backgrounds. The socioeconomic status of each participant was based on education and income levels. Both groups of dyads engaged in pro-social dialectic discourse during acquisition of hemodynamic signals. Post-scan questionnaires confirmed increased anxiety and effort for high-disparity dyads. Consistent with the frontal lobe hypothesis, left dorsolateral pre-frontal cortex (DLPFC), frontopolar area and pars triangularis were more active during speech dialogue in high than in low-disparity groups. Further, frontal lobe signals were more synchronous across brains for high- than low-disparity dyads. Convergence of these behavioral, neuroimaging and neural coupling findings associate left frontal lobe processes with natural pro-social dialogue under 'out-group' conditions and advance both theoretical and technical approaches for further investigation.

Interpersonal Agreement and Disagreement During Face-to-Face Dialogue: An fNIRS Investigation.

Although the neural systems that underlie spoken language are well-known, how they adapt to evolving social cues during natural conversations remains an unanswered question. In this work we investigate the neural correlates of face-to-face conversations between two individuals using functional near infrared spectroscopy (fNIRS) and acoustical analyses of concurrent audio recordings. Nineteen pairs of healthy adults engaged in live discussions on two controversial topics where their opinions were either in agreement or disagreement. Participants were matched according to their a priori opinions on these topics as assessed by questionnaire. Acoustic measures of the recorded speech including the fundamental frequency range, median fundamental frequency, syllable rate, and acoustic energy were elevated during disagreement relative to agreement. Consistent with both the a priori opinion ratings and the acoustic findings, neural activity associated with long-range functional networks, rather than the canonical language areas, was also differentiated by the two conditions. Specifically, the frontoparietal system including bilateral dorsolateral prefrontal cortex, left supramarginal gyrus, angular gyrus, and superior temporal gyrus showed increased activity while talking during disagreement. In contrast, talking during agreement was characterized by increased activity in a social and attention network including right supramarginal gyrus, bilateral frontal eye-fields, and left frontopolar regions. Further, these social and visual attention networks were more synchronous across brains during agreement than disagreement. Rather than localized modulation of the canonical language system, these findings are most consistent with a model of distributed and adaptive language-related processes including cross-brain neural coupling that serves dynamic verbal exchanges.

Real-Time Eye-to-Eye Contact Is Associated With Cross-Brain Neural Coupling in Angular Gyrus.

Direct eye contact between two individuals is a salient social behavior known to initiate and promote interpersonal interaction. However, the neural processes that underlie these live interactive behaviors and eye-to-eye contact are not well understood. The Dynamic Neural Coupling Hypothesis presents a general theoretical framework proposing that shared interactive behaviors are represented by cross-brain signal coherence. Using functional near-infrared spectroscopy (fNIRS) adapted for hyper scanning, we tested this hypothesis specifically for neural mechanisms associated with eye-to-eye gaze between human participants compared to similar direct eye-gaze at a dynamic video of a face and predicted that the coherence of neural signals between the two participants during reciprocal eye-to-eye contact would be greater than coherence observed during direct eye-gaze at a dynamic video for those signals originating in social and face processing systems. Consistent with this prediction cross-brain coherence was increased for signals within the angular gyrus (AG) during eye-to-eye contact relative to direct eye-gaze at a dynamic face video (p < 0.01). Further, activity in the right temporal-parietal junction (TPJ) was increased in the real eye-to-eye condition (p < 0.05, FDR corrected). Together, these findings advance a functional and mechanistic understanding of the AG and cross-brain neural coupling associated with real-time eye-to-eye contact.

Joint Attention During Live Person-to-Person Contact Activates rTPJ, Including a Sub-Component Associated With Spontaneous Eye-to-Eye Contact.

Eye-to-eye contact is a spontaneous behavior between interacting partners that occurs naturally during social interactions. However, individuals differ with respect to eye gaze behaviors such as frequency of eye-to-eye contacts, and these variations may reflect underlying differences in social behavior in the population. While the use of eye signaling to indicate a shared object of attention in joint attention tasks has been well-studied, the effects of the natural variation in establishing eye contact during joint attention have not been isolated. Here, we investigate this question using a novel two-person joint attention task. Participants were not instructed regarding the use of eye contacts; thus all mutual eye contact events between interacting partners that occurred during the joint attention task were spontaneous and varied with respect to frequency. We predicted that joint attention systems would be modulated by differences in the social behavior across participant pairs, which could be measured by the frequency of eye contact behavior. We used functional near-infrared spectroscopy (fNIRS) hyperscanning and eye-tracking to measure the neural signals associated with joint attention in interacting dyads and to record the number of eye contact events between them. Participants engaged in a social joint attention task in which real partners used eye gaze to direct each other's attention to specific targets. Findings were compared to a non-social joint attention task in which an LED cue directed both partners' attention to the same target. The social joint attention condition showed greater activity in right temporoparietal junction than the non-social condition, replicating prior joint attention results. Eye-contact frequency modulated the joint attention activity, revealing bilateral activity in social and high level visual areas associated with partners who made more eye contact. Additionally, when the number of mutual eye contact events was used to classify each pair as either "high eye contact" or "low eye contact" dyads, cross-brain coherence analysis revealed greater coherence between high eye contact dyads than low eye contact dyads in these same areas. Together, findings suggest that variation in social behavior as measured by eye contact modulates activity in a subunit of the network associated with joint attention.

Differential brain-to-brain entrainment while speaking and listening in native and foreign languages.

The study explores interbrain neural coupling when interlocutors engage in a conversation whether it be in their native or nonnative language. To this end, electroencephalographic hyperscanning was used to study brain-to-brain phase synchronization during a two-person turn-taking verbal exchange with no visual contact, in either a native or a foreign language context. Results show that the coupling strength between brain signals is increased in both, the native language context and the foreign language context, specifically, in the alpha frequency band. A difference in brain-to speech entrainment to native and foreign languages is also shown. These results indicate that between brain similarities in the timing of neural activations and their spatial distributions change depending on the language code used. We argue that factors like linguistic alignment, joint attention and brain-entrainment to speech operate with a language-idiosyncratic neural configuration, modulating the alignment of neural activity between speakers and listeners. Other possible factors leading to the differential interbrain synchronization patterns as well as the potential features of brain-to-brain entrainment as a mechanism are briefly discussed. We concluded that linguistic context should be considered when addressing interpersonal communication. The findings here open doors to quantifying linguistic interactions.

Two-person neuroscience and naturalistic social communication: the role of language and linguistic variables in brain-coupling research.

Social cognitive neuroscience (SCN) seeks to understand the brain mechanisms through which we comprehend others' emotions and intentions in order to react accordingly. For decades, SCN has explored relevant domains by exposing individual participants to predesigned stimuli and asking them to judge their social (e.g., emotional) content. Subjects are thus reduced to detached observers of situations that they play no active role in. However, the core of our social experience is construed through real-time interactions requiring the active negotiation of information with other people. To gain more relevant insights into the workings of the social brain, the incipient field of two-person neuroscience (2PN) advocates the study of brain-to-brain coupling through multi-participant experiments. In this paper, we argue that the study of online language-based communication constitutes a cornerstone of 2PN. First, we review preliminary evidence illustrating how verbal interaction may shed light on the social brain. Second, we advance methodological recommendations to design experiments within language-based 2PN. Finally, we formulate outstanding questions for future research.