What binds us? Inter-brain neural synchronization and its implications for theories of human consciousness

Abstract The association between neural oscillations and functional integration is widely recognized in the study of human cognition. Large-scale synchronization of neural activity has also been proposed as the neural basis of consciousness. Intriguingly, a growing number of studies in social cognitive neuroscience reveal that phase synchronization similarly appears across brains during meaningful social interaction. Moreover, this inter-brain synchronization has been associated with subjective reports of social connectedness, engagement, and cooperativeness, as well as experiences of social cohesion and ‘self-other merging’. These findings challenge the standard view of human consciousness as essentially first-person singular and private. We therefore revisit the recent controversy over the possibility of extended consciousness and argue that evidence of inter-brain synchronization in the fastest frequency bands overcomes the hitherto most convincing sceptical position. If this proposal is on the right track, our understanding of human consciousness would be profoundly transformed, and we propose a method to test this proposal experimentally.

[1]  Yan Mu,et al.  Neural mechanisms underlying interpersonal coordination: A review of hyperscanning research , 2018, Social and Personality Psychology Compass.

[2]  E. Rosch,et al.  The Embodied Mind: Cognitive Science and Human Experience , 1993 .

[3]  Francisco J. Varela,et al.  The Embodied Mind , 2018 .

[4]  A. Engel,et al.  Spectral fingerprints of large-scale neuronal interactions , 2012, Nature Reviews Neuroscience.

[5]  Steven Brown,et al.  Feeling the pain of others is associated with self-other confusion and prior pain experience , 2013, Front. Hum. Neurosci..

[6]  Flavio Fröhlich,et al.  Randomized trial of transcranial alternating current stimulation for treatment of auditory hallucinations in schizophrenia , 2018, European Psychiatry.

[7]  Evan Thompson,et al.  Empathy and consciousness. , 2001 .

[8]  Will Mcneill Keeping Together in Time , 1997 .

[9]  D. DeSteno,et al.  The rhythm of joint action: Synchrony promotes cooperative ability , 2010 .

[10]  F. Varela,et al.  Perception's shadow: long-distance synchronization of human brain activity , 1999, Nature.

[11]  R. Llinás I of the Vortex , 2000 .

[12]  J. A. Scott Kelso,et al.  Brain coordination dynamics: True and false faces of phase synchrony and metastability , 2009, Progress in Neurobiology.

[13]  Ronald H. Stevens,et al.  Are Neurodynamic Organizations A Fundamental Property of Teamwork? , 2017, Front. Psychol..

[14]  Dave Ward Enjoying the Spread: Conscious Externalism Reconsidered , 2012 .

[15]  Caroline Szymanski,et al.  Teams on the same wavelength perform better: Inter-brain phase synchronization constitutes a neural substrate for social facilitation , 2017, NeuroImage.

[16]  A. Clark,et al.  The Extended Mind , 1998, Analysis.

[17]  A. Schnitzler,et al.  Normal and pathological oscillatory communication in the brain , 2005, Nature Reviews Neuroscience.

[18]  Xu Cui,et al.  NIRS-based hyperscanning reveals increased interpersonal coherence in superior frontal cortex during cooperation , 2012, NeuroImage.

[19]  C. Koch,et al.  Towards a neurobiological theory of consciousness , 1990 .

[20]  V. Calhoun,et al.  Information flow between interacting human brains: Identification, validation, and relationship to social expertise , 2015, Proceedings of the National Academy of Sciences.

[21]  Michal Lavidor,et al.  Prefrontal oscillatory stimulation modulates access to cognitive control references in retrospective metacognitive commentary , 2014, Clinical Neurophysiology.

[22]  Hermann Haken Principles of Brain Functioning: A Synergetic Approach to Brain Activity, Behavior and Cognition , 2012 .

[23]  D. Poeppel,et al.  Brain-to-Brain Synchrony Tracks Real-World Dynamic Group Interactions in the Classroom , 2017, Current Biology.

[24]  W. Singer,et al.  Abnormal neural oscillations and synchrony in schizophrenia , 2010, Nature Reviews Neuroscience.

[25]  Y. Hu,et al.  Cooperation in lovers: An fNIRS‐based hyperscanning study , 2017, Human Brain Mapping.

[26]  M. Balconi,et al.  Functional EEG connectivity during competition , 2018, BMC Neuroscience.

[27]  Nicola Knight,et al.  Rowers' high: behavioural synchrony is correlated with elevated pain thresholds , 2010, Biology Letters.

[28]  Viktor Müller,et al.  Intra- and interbrain synchronization and network properties when playing guitar in duets , 2012, Front. Hum. Neurosci..

[29]  D. O. Hebb,et al.  The organization of behavior , 1988 .

[30]  R. Feldman,et al.  Brain-to-Brain Synchrony during Naturalistic Social Interactions , 2017, Scientific Reports.

[31]  Jonathan Berger,et al.  Natural music evokes correlated EEG responses reflecting temporal structure and beat , 2019, NeuroImage.

[32]  K. Vogeley,et al.  Toward a second-person neuroscience 1 , 2013, Behavioral and Brain Sciences.

[33]  J. Kurths,et al.  Phase synchronization: from theory to data analysis , 2003 .

[34]  Andy Clark,et al.  Edinburgh Research Explorer Spreading the Joy? Why the Machinery of Consciousness is (Probably) Still in the Head , 2013 .

[35]  A. Engel,et al.  Entrainment of Brain Oscillations by Transcranial Alternating Current Stimulation , 2014, Current Biology.

[36]  L. Nummenmaa,et al.  The brains of high functioning autistic individuals do not synchronize with those of others☆ , 2013, NeuroImage: Clinical.

[37]  J. Brunelin,et al.  Effects of theta-rhythm transcranial alternating current stimulation (4.5 Hz-tACS) in patients with clozapine-resistant negative symptoms of schizophrenia: a case series , 2016, Journal of neural transmission.

[38]  E. D. Paolo,et al.  Participatory sense-making , 2007 .

[39]  Christina O. Hlutkowsky,et al.  Putting our heads together: interpersonal neural synchronization as a biological mechanism for shared intentionality , 2018, Social cognitive and affective neuroscience.

[40]  F. Varela,et al.  Radical embodiment: neural dynamics and consciousness , 2001, Trends in Cognitive Sciences.

[41]  F. Fröhlich,et al.  Transcranial Alternating Current Stimulation Modulates Large-Scale Cortical Network Activity by Network Resonance , 2013, The Journal of Neuroscience.

[42]  Michela Balconi,et al.  EEG hyperscanning and behavioral synchronization during a joint actions , 2018, Neuropsychological Trends.

[43]  Guillaume Dumas,et al.  Brain-to-brain coupling during handholding is associated with pain reduction , 2018, Proceedings of the National Academy of Sciences.

[44]  Tom Froese,et al.  Searching for the conditions of genuine intersubjectivity , 2018, The Oxford Handbook of 4E Cognition.

[45]  Ole Jensen,et al.  Top–Down Control of Alpha Phase Adjustment in Anticipation of Temporally Predictable Visual Stimuli , 2018, Journal of Cognitive Neuroscience.

[46]  M. Osaka,et al.  How Two Brains Make One Synchronized Mind in the Inferior Frontal Cortex: fNIRS-Based Hyperscanning During Cooperative Singing , 2015, Front. Psychol..

[47]  Philip R. Cohen,et al.  Intentions in Communication. , 1992 .

[48]  Michael D. Kirchhoff Extended cognition & constitution: Re-evaluating the constitutive claim of extended cognition , 2014 .

[49]  Alva Noë,et al.  Out of Our Heads: Why You Are Not Your Brain, and Other Lessons from the Biology of Consciousness , 2009 .

[50]  Justin Dauwels,et al.  EEG hyperscanning study of inter-brain synchrony during cooperative and competitive interaction , 2016, 2016 IEEE International Conference on Systems, Man, and Cybernetics (SMC).

[51]  Michael J. Hove,et al.  It's all in the timing: Interpersonal synchrony increases affiliation , 2009 .

[52]  Tal-Chen Rabinowitch,et al.  Synchronous Rhythmic Interaction Enhances Children’s Perceived Similarity and Closeness towards Each Other , 2015, PloS one.

[53]  S. Kastner,et al.  Communication between Brain Areas Based on Nested Oscillations , 2017, eNeuro.

[54]  Sangtae Ahn,et al.  Targeting reduced neural oscillations in patients with schizophrenia by transcranial alternating current stimulation , 2019, NeuroImage.

[55]  Lauri Parkkonen,et al.  Synchrony of brains and bodies during implicit interpersonal interaction , 2013, Trends in Cognitive Sciences.

[56]  Simon Baron-Cohen,et al.  Absence of Embodied Empathy During Pain Observation in Asperger Syndrome , 2009, Biological Psychiatry.

[57]  Caroline Szymanski,et al.  Hyper-Transcranial Alternating Current Stimulation: Experimental Manipulation of Inter-Brain Synchrony , 2017, Front. Hum. Neurosci..

[58]  Shen Liu,et al.  Interactive Brain Activity: Review and Progress on EEG-Based Hyperscanning in Social Interactions , 2018, Front. Psychol..

[59]  Joseph A. Bulbulia,et al.  To be in synchrony or not? A meta-analysis of synchrony's effects on behavior, perception, cognition and affect , 2017 .

[60]  Jon Andoni Duñabeitia,et al.  Brain-to-brain entrainment: EEG interbrain synchronization while speaking and listening , 2017, Scientific Reports.

[61]  Sebastian Wallot,et al.  The Blue-Collar Brain , 2012, Front. Physio..

[62]  G. Buzsáki,et al.  A neural coding scheme formed by the combined function of gamma and theta oscillations. , 2008, Schizophrenia bulletin.

[63]  Axel Cleeremans,et al.  The Oxford Companion to Consciousness , 2009 .

[64]  Asif A Ghazanfar,et al.  Hebb's Dream: The Resurgence of Cell Assemblies , 1997, Neuron.

[65]  Tom Froese,et al.  Embodied social interaction constitutes social cognition in pairs of humans: A minimalist virtual reality experiment , 2014, Scientific Reports.

[66]  H. Haken,et al.  Synergetics , 1988, IEEE Circuits and Devices Magazine.

[67]  Michael D. Kirchhoff,et al.  Extended Consciousness and Predictive Processing , 2019 .

[68]  Giulio Tononi,et al.  Schizophrenia and the mechanisms of conscious integration , 2000, Brain Research Reviews.

[69]  K. Kubota,et al.  Synchronous activity of two people's prefrontal cortices during a cooperative task measured by simultaneous near-infrared spectroscopy. , 2011, Journal of biomedical optics.

[70]  Laura Astolfi,et al.  Investigating Cooperative Behavior in Ecological Settings: An EEG Hyperscanning Study , 2016, PloS one.

[71]  N. Block On a confusion about a function of consciousness , 1995, Behavioral and Brain Sciences.

[72]  W. Klimesch,et al.  What does phase information of oscillatory brain activity tell us about cognitive processes? , 2008, Neuroscience & Biobehavioral Reviews.

[73]  Michael J. Richardson,et al.  Autism and social disconnection in interpersonal rocking , 2013, Front. Integr. Neurosci..

[74]  Shu-Chen Li,et al.  Brains swinging in concert: cortical phase synchronization while playing guitar , 2009, BMC Neuroscience.

[75]  Scott S. Wiltermuth,et al.  Synchrony and Cooperation , 2009, Psychological science.

[76]  A. Opstal Dynamic Patterns: The Self-Organization of Brain and Behavior , 1995 .

[77]  Catrin Misselhorn,et al.  Collective Agency and Cooperation in Natural and Artificial Systems , 2015 .

[78]  J. A. Scott Kelso,et al.  Coordination Dynamics , 2009, Encyclopedia of Complexity and Systems Science.

[79]  W. Singer Synchronization of cortical activity and its putative role in information processing and learning. , 1993, Annual review of physiology.

[80]  G. Karmos,et al.  Entrainment of Neuronal Oscillations as a Mechanism of Attentional Selection , 2008, Science.

[81]  G. Tononi,et al.  The Neurology of Consciousness: An Overview , 2016 .

[82]  Y. Hu,et al.  Inter-brain synchrony and cooperation context in interactive decision making , 2017, Biological Psychology.

[83]  Giulia Galli,et al.  Transcranial Alternating Current Stimulation Affects Decision Making , 2012, Front. Syst. Neurosci..

[84]  Fabio Babiloni,et al.  Cooperation driven coherence: Brains working hard together , 2015, 2015 37th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC).

[85]  Piercarlo Valdesolo,et al.  Synchrony and the social tuning of compassion. , 2011, Emotion.

[86]  Peter König,et al.  Hyperscanning: A Valid Method to Study Neural Inter-brain Underpinnings of Social Interaction , 2020, Frontiers in Human Neuroscience.

[87]  S. Garrod,et al.  Brain-to-brain coupling: a mechanism for creating and sharing a social world , 2012, Trends in Cognitive Sciences.

[88]  S. Shimojo,et al.  Interpersonal body and neural synchronization as a marker of implicit social interaction , 2012, Scientific Reports.

[89]  F. Cincotti,et al.  Neuroelectrical Hyperscanning Measures Simultaneous Brain Activity in Humans , 2010, Brain Topography.

[90]  J. Martinerie,et al.  The brainweb: Phase synchronization and large-scale integration , 2001, Nature Reviews Neuroscience.

[91]  Trysha Galloway,et al.  Tracing Neurodynamic Information Flows during Teamwork. , 2016, Nonlinear dynamics, psychology, and life sciences.

[92]  S. Gallagher,et al.  The Oxford Handbook of 4E Cognition , 2018 .

[93]  Laura Astolfi,et al.  Defecting or Not Defecting: How to “Read” Human Behavior during Cooperative Games by EEG Measurements , 2010, PloS one.

[94]  Jake Yeston,et al.  Inching up the Wall , 2008, Science.

[95]  R. Llinás I of the Vortex: From Neurons to Self , 2000 .

[96]  Andreas K. Engel,et al.  Temporal Binding, Binocular Rivalry, and Consciousness , 1999, Consciousness and Cognition.

[97]  H. W. Veen,et al.  Handbook of Biological Physics , 1996 .

[98]  David Poeppel,et al.  Brain-to-Brain Synchrony and Learning Outcomes Vary by Student–Teacher Dynamics: Evidence from a Real-world Classroom Electroencephalography Study , 2019, Journal of Cognitive Neuroscience.

[99]  C. Herrmann,et al.  Transcranial Alternating Current Stimulation Enhances Individual Alpha Activity in Human EEG , 2010, PloS one.

[100]  R. Hari,et al.  Brain basis of human social interaction: from concepts to brain imaging. , 2009, Physiological reviews.

[101]  Michela Balconi,et al.  Cooperation and Competition with Hyperscanning Methods: Review and Future Application to Emotion Domain , 2017, Front. Comput. Neurosci..

[102]  A. Burgess On the interpretation of synchronization in EEG hyperscanning studies: a cautionary note , 2013, Front. Hum. Neurosci..

[103]  D. Long I of the Vortex: From Neurons to Self , 2002 .

[104]  F. Varela,et al.  Measuring phase synchrony in brain signals , 1999, Human brain mapping.

[105]  Peter E. Keller,et al.  Neural alpha oscillations index the balance between self-other integration and segregation in real-time joint action , 2016, Neuropsychologia.

[106]  Line Garnero,et al.  Inter-Brain Synchronization during Social Interaction , 2010, PloS one.

[107]  Masamichi J. Hayashi,et al.  Hard to “tune in”: neural mechanisms of live face-to-face interaction with high-functioning autistic spectrum disorder , 2012, Front. Hum. Neurosci..

[108]  David Melcher,et al.  Multiple oscillatory rhythms determine the temporal organization of perception , 2017, Proceedings of the National Academy of Sciences.

[109]  A. Engel,et al.  EEG oscillations: From correlation to causality. , 2016, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[110]  W. Singer,et al.  Synchronization of Neural Activity across Cortical Areas Correlates with Conscious Perception , 2007, The Journal of Neuroscience.

[111]  Kevin Shockley,et al.  Interpersonal Synergies , 2010, Front. Psychology.

[112]  W. Tschacher,et al.  Interpersonal synchrony feels good but impedes self-regulation of affect , 2019, Scientific Reports.

[113]  W. Singer,et al.  Neural Synchrony in Cortical Networks: History, Concept and Current Status , 2009, Front. Integr. Neurosci..

[114]  Michael X Cohen,et al.  Analyzing Neural Time Series Data: Theory and Practice , 2014 .

[115]  L. M. Ward,et al.  Synchronous neural oscillations and cognitive processes , 2003, Trends in Cognitive Sciences.

[116]  Shihui Han,et al.  Oxytocin enhances inter-brain synchrony during social coordination in male adults. , 2016, Social cognitive and affective neuroscience.

[117]  Philip R. Cohen,et al.  Collective Intentions and Actions , 2003 .

[118]  Tom Froese,et al.  The brain is not an isolated "black box," nor is its goal to become one. , 2013, The Behavioral and brain sciences.

[119]  M. Nitsche,et al.  Induction of self awareness in dreams through frontal low current stimulation of gamma activity , 2014, Nature Neuroscience.

[120]  Ronald H. Stevens,et al.  A Team’s Neurodynamic Organization is More than the Sum of its Members , 2017 .

[121]  Guillaume Dumas,et al.  Towards a two-body neuroscience , 2011, Communicative & integrative biology.

[122]  C. Schroeder,et al.  Predictive Suppression of Cortical Excitability and Its Deficit in Schizophrenia , 2013, The Journal of Neuroscience.

[123]  C. Herrmann,et al.  Transcranial alternating current stimulation: a review of the underlying mechanisms and modulation of cognitive processes , 2013, Front. Hum. Neurosci..

[124]  G. Buzsáki,et al.  Neuronal Oscillations in Cortical Networks , 2004, Science.

[125]  E. Redcay,et al.  Using second-person neuroscience to elucidate the mechanisms of social interaction , 2019, Nature Reviews Neuroscience.

[126]  Gang Zhang,et al.  Quantitative assessment on the cloning efficiencies of lentiviral transfer vectors with a unique clone site , 2012, Scientific Reports.

[127]  P. Fries Rhythms for Cognition: Communication through Coherence , 2015, Neuron.

[128]  Mukesh Dhamala,et al.  Hyperscanning : Simultaneous fMRI during Linked Social Interactions , 2001 .

[129]  A. Engel,et al.  Neuronal Oscillations, Coherence, and Consciousness , 2016 .

[130]  G. Buzsáki Rhythms of the brain , 2006 .

[131]  J. Kelso,et al.  The Complementary Nature , 2006 .

[132]  Andy Clark,et al.  Dreaming the Whole Cat: Generative Models, Predictive Processing, and the Enactivist Conception of Perceptual Experience , 2012 .

[133]  C. Miniussi,et al.  The Functional Importance of Rhythmic Activity in the Brain , 2012, Current Biology.

[134]  R. Beer Dynamical approaches to cognitive science , 2000, Trends in Cognitive Sciences.

[135]  S. Shamay-Tsoory,et al.  The role of touch in regulating inter-partner physiological coupling during empathy for pain , 2017, Scientific Reports.

[136]  Jacqueline Nadel,et al.  From social behaviour to brain synchronization: Review and perspectives in hyperscanning , 2011 .

[137]  L. Astolfi,et al.  Social neuroscience and hyperscanning techniques: Past, present and future , 2014, Neuroscience & Biobehavioral Reviews.

[138]  C. Herrmann,et al.  Eyes wide shut: Transcranial alternating current stimulation drives alpha rhythm in a state dependent manner , 2016, Scientific Reports.

[139]  Shihui Han,et al.  The role of gamma interbrain synchrony in social coordination when humans face territorial threats , 2017, Social cognitive and affective neuroscience.

[140]  Margaret Wilson,et al.  An oscillator model of the timing of turn-taking , 2005, Psychonomic bulletin & review.

[141]  M. Stapleton,et al.  Is collective agency a coherent idea?: Considerations from the enactive theory of agency , 2015 .

[142]  Leonhard Schilbach,et al.  Towards a second-person neuropsychiatry , 2016, Philosophical Transactions of the Royal Society B: Biological Sciences.

[143]  O. Jensen,et al.  Alpha Oscillations Serve to Protect Working Memory Maintenance against Anticipated Distracters , 2012, Current Biology.