Interpersonal synchronization of inferior frontal cortices tracks social interactive learning of a song

&NA; Much of human learning emerges as a result of interaction with others. Yet, this interpersonal process has been poorly characterized from a neurophysiological perspective. This study investigated (i) whether Interpersonal Brain Synchronization (IBS) can reliably mark social interactive learning, and specifically (ii) during what kind of interactive behavior. We recorded brain activity from learner‐instructor dyads using functional Near‐Infrared Spectroscopy (fNIRS) during the acquisition of a music song. We made four fundamental observations. First, during the interactive learning task, brain activity recorded from the bilateral Inferior Frontal Cortex (IFC) synchronized across the learner and the instructor. Second, such IBS was observed in particular when the learner was observing the instructor's vocal behavior and when the learning experience entailed a turn‐taking and more active mode of interaction. Third, this specific enhancement of IBS predicted learner's behavioral performance. Fourth, Granger causality analyses further disclosed that the signal recorded from the instructor's brain better predicted that recorded from the learner's brain than vice versa. Together, these results indicate that social interactive learning can be neurophysiologically characterized in terms of IBS. Furthermore, they suggest that the learner's involvement in the learning experience, alongside the instructor's modeling, are key factors driving the alignment of neural processes across learner and instructor. Such alignment impacts upon the real‐time acquisition of new information and eventually upon the learning (behavioral) performance. Hence, besides providing a biological characterization of social interactive learning, our results hold relevance for clinical and pedagogical practices.

[1]  Peter E. Keller,et al.  A conceptual review on action-perception coupling in the musicians’ brain: what is it good for? , 2014, Front. Hum. Neurosci..

[2]  J. Pine,et al.  Chunking mechanisms in human learning , 2001, Trends in Cognitive Sciences.

[3]  G. Ding,et al.  Leader emergence through interpersonal neural synchronization , 2015, Proceedings of the National Academy of Sciences.

[4]  Peter E. Keller,et al.  What can music tell us about social interaction? , 2015, Trends in Cognitive Sciences.

[5]  Archana K. Singh,et al.  Spatial registration of multichannel multi-subject fNIRS data to MNI space without MRI , 2005, NeuroImage.

[6]  Seung-Goo Kim,et al.  Neural networks for harmonic structure in music perception and action , 2016, NeuroImage.

[7]  Aniruddh D. Patel,et al.  Experimental Evidence for Synchronization to a Musical Beat in a Nonhuman Animal , 2009, Current Biology.

[8]  Frithjof Kruggel,et al.  Age dependency of the hemodynamic response as measured by functional near-infrared spectroscopy , 2003, NeuroImage.

[9]  Parag Chordia,et al.  Inter‐subject synchronization of brain responses during natural music listening , 2013, The European journal of neuroscience.

[10]  P. Janata,et al.  Activation of the inferior frontal cortex in musical priming. , 2003, Annals of the New York Academy of Sciences.

[11]  C. Frith,et al.  Alignment in social interactions , 2017, Consciousness and Cognition.

[12]  R. Hari,et al.  Emotions promote social interaction by synchronizing brain activity across individuals , 2012, Proceedings of the National Academy of Sciences.

[13]  J. Mazziotta,et al.  Neural mechanisms of empathy in humans: A relay from neural systems for imitation to limbic areas , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[14]  Paul D. Umbach,et al.  Faculty do Matter: The Role of College Faculty in Student Learning and Engagement , 2005 .

[15]  Charles H. Kahn,et al.  Plato and the Post-Socratic Dialogue: The Return to the Philosophy of Nature , 2013 .

[16]  Xu Cui,et al.  Sensitivity of fNIRS measurement to head motion: An applied use of smartphones in the lab , 2015, Journal of Neuroscience Methods.

[17]  Masako Okamoto,et al.  Virtual spatial registration of stand-alone fNIRS data to MNI space , 2007, NeuroImage.

[18]  R. Klinger,et al.  Approaches to Children's Song Acquisition: Immersion and Phrase-by-Phrase , 1998 .

[19]  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..

[20]  A. Astin Student involvement: A developmental theory for higher education. , 1999 .

[21]  J. Mazziotta,et al.  Mirror neuron system: basic findings and clinical applications , 2007, Annals of neurology.

[22]  Shin-Ichi Izumi,et al.  Integration of Teaching Processes and Learning Assessment in the Prefrontal Cortex during a Video Game Teaching–learning Task , 2017, Front. Psychol..

[23]  K. Jöreskog,et al.  Intraclass Reliability Estimates: Testing Structural Assumptions , 1974 .

[24]  Martin Wolf,et al.  Between-brain connectivity during imitation measured by fNIRS , 2012, NeuroImage.

[25]  Isabelle Peretz,et al.  Brain specialization for music. , 2002, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[26]  C. Snow,et al.  Social influences on vocal development: Social influences on vocal learning in human and nonhuman primates , 1997 .

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

[28]  Aslak Grinsted,et al.  Nonlinear Processes in Geophysics Application of the Cross Wavelet Transform and Wavelet Coherence to Geophysical Time Series , 2022 .

[29]  Michael Erb,et al.  Cerebral pathways in processing of affective prosody: A dynamic causal modeling study , 2006, NeuroImage.

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

[31]  D. Kimura Functional Asymmetry of the Brain in Dichotic Listening , 1967 .

[32]  B. Millis Making the Most of College: Students Speak Their Minds , 2002 .

[33]  Angela D. Friederici,et al.  Syntax in Action Has Priority over Movement Selection in Piano Playing: An ERP Study , 2016, Journal of Cognitive Neuroscience.

[34]  Guadalupe Anaya,et al.  Latina/o Student Achievement: Exploring the Influence of Student-Faculty Interactions on College Grades. , 2001 .

[35]  C. Fiebach,et al.  The role of left inferior frontal and superior temporal cortex in sentence comprehension: localizing syntactic and semantic processes. , 2003, Cerebral cortex.

[36]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[37]  G. Novembre,et al.  Syntax in a pianist's hand: ERP signatures of “embodied” syntax processing in music , 2013, Cortex.

[38]  G. Schwarz Estimating the Dimension of a Model , 1978 .

[39]  Yasushi Miyashita,et al.  From Perception to Sentence Comprehension: The Convergence of Auditory and Visual Information of Language in the Left Inferior Frontal Cortex , 2002, NeuroImage.

[40]  Kazuo Hiraki,et al.  Sustained decrease in oxygenated hemoglobin during video games in the dorsal prefrontal cortex: A NIRS study of children , 2006, NeuroImage.

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

[42]  A. Ziehe,et al.  Estimation of Directional Coupling between Cortical Areas Using Near-infrared Spectroscopy (nirs) References and Links , 2022 .

[43]  Micah R Bregman,et al.  Experimental evidence for synchronization to a musical beat in a nonhuman animal. , 2009, Current biology : CB.

[44]  Richard Mooney,et al.  Neurobiology of song learning , 2009, Current Opinion in Neurobiology.

[45]  C. Frith,et al.  Mechanisms of social cognition. , 2012, Annual review of psychology.

[46]  Richard E. Mayer,et al.  e-Learning and the Science of Instruction: Proven Guidelines for Consumers and Designers of Multimedia Learning , 2002 .

[47]  J. Fletcher Learning Disabilities : From Identification to Intervention , 2006 .

[48]  Andrew N. Meltzoff,et al.  The neural bases of cooperation and competition: an fMRI investigation , 2004, NeuroImage.

[49]  G. Schlaug,et al.  Congenital amusia: an auditory-motor feedback disorder? , 2007, Restorative neurology and neuroscience.

[50]  M. Iacoboni,et al.  Listening to speech activates motor areas involved in speech production , 2004, Nature Neuroscience.

[51]  A. Lockey,et al.  Teaching and learning , 2001, Emergency medicine journal : EMJ.

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

[53]  Luciano Fadiga,et al.  When gaze opens the channel for communication: Integrative role of IFG and MPFC , 2015, NeuroImage.

[54]  Aniruddh D. Patel,et al.  Language, music, syntax and the brain , 2003, Nature Neuroscience.

[55]  Wilkin Chau,et al.  Rhythmic brain activities related to singing in humans , 2007, NeuroImage.

[56]  Masako Okamoto,et al.  Three-dimensional probabilistic anatomical cranio-cerebral correlation via the international 10–20 system oriented for transcranial functional brain mapping , 2004, NeuroImage.

[57]  Yong He,et al.  BrainNet Viewer: A Network Visualization Tool for Human Brain Connectomics , 2013, PloS one.

[58]  Aniruddh D. Patel Musical Rhythm, Linguistic Rhythm, and Human Evolution , 2006 .

[59]  Dongrong Xu,et al.  A conditional Granger causality model approach for group analysis in functional magnetic resonance imaging. , 2011, Magnetic resonance imaging.

[60]  Yousuke Ogata,et al.  Behavioral and near-infrared spectroscopy study of the effects of distance and choice in a number comparison task , 2008, Neuroscience Research.

[61]  Takayuki Nozawa,et al.  Steady Beat Sound Facilitates both Coordinated Group Walking and Inter-Subject Neural Synchrony , 2017, Front. Hum. Neurosci..

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

[63]  Tao Liu,et al.  Role of the right inferior frontal gyrus in turn-based cooperation and competition: A near-infrared spectroscopy study , 2015, Brain and Cognition.

[64]  Arne D. Ekstrom,et al.  Single-Neuron Responses in Humans during Execution and Observation of Actions , 2010, Current Biology.

[65]  Jianfeng Feng,et al.  Uncovering Interactions in the Frequency Domain , 2008, PLoS Comput. Biol..

[66]  Scott Makeig,et al.  EEG imaging of toddlers during dyadic turn-taking: Mu-rhythm modulation while producing or observing social actions , 2015, NeuroImage.

[67]  Yoshihiro Miyake,et al.  Prior Knowledge Facilitates Mutual Gaze Convergence and Head Nodding Synchrony in Face-to-face Communication , 2016, Scientific Reports.

[68]  L. Davachi,et al.  Enhanced Intersubject Correlations during Movie Viewing Correlate with Successful Episodic Encoding , 2008, Neuron.

[69]  Gottfried Schlaug,et al.  The Therapeutic Effects of Singing in Neurological Disorders. , 2010, Music perception.

[70]  D. Marchiori,et al.  Predicting Human Interactive Learning by Regret-Driven Neural Networks , 2008, Science.

[71]  S. Kotz,et al.  How relevant is social interaction in second language learning? , 2013, Front. Hum. Neurosci..

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

[73]  D. Sathianathan,et al.  Effects of faculty interaction and feedback on gains in student skills , 2002, 32nd Annual Frontiers in Education.

[74]  V. Gallese Mirror neurons, embodied simulation and a second-person approach to mindreading , 2013, Cortex.

[75]  Kembro Jackelyn,et al.  Detrended Fluctuation Analysis , 2015 .

[76]  Joy Hirsch,et al.  Separation of the global and local components in functional near-infrared spectroscopy signals using principal component spatial filtering , 2016, Neurophotonics.

[77]  Sonja A. Kotz,et al.  Help me if I can't: Social interaction effects in adult contextual word learning , 2017, Cognition.

[78]  Robin Mason,et al.  e-Learning and Social Networking Handbook: Resources for Higher Education , 2008 .

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

[80]  P. Montague,et al.  Ready…Go: Amplitude of the fMRI Signal Encodes Expectation of Cue Arrival Time , 2009, PLoS biology.

[81]  Andrew A G Mattar,et al.  Motor Learning by Observing , 2005, Neuron.

[82]  Brandon A. Ally,et al.  Music as a memory enhancer in patients with Alzheimer's disease , 2010, Neuropsychologia.

[83]  Robert T. Tauber,et al.  Self-Fulfilling Prophecy: A Practical Guide to Its Use in Education , 1997 .

[84]  V. Gallese The manifold nature of interpersonal relations: the quest for a common mechanism. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[85]  W. Köhler The task of Gestalt psychology , 1969 .

[86]  Y. Hu,et al.  Brain-to-brain synchronization across two persons predicts mutual prosociality , 2017, Social cognitive and affective neuroscience.

[87]  D. Persellin,et al.  A comparative study on the effectiveness of two song‐teaching methods: holistic vs. phrase‐by‐phrase , 2009 .

[88]  Carol A. Lundberg,et al.  Quality and Frequency of Faculty-Student Interaction as Predictors of Learning: An Analysis by Student Race/Ethnicity , 2004 .

[89]  R. Poldrack,et al.  Recovering Meaning Left Prefrontal Cortex Guides Controlled Semantic Retrieval , 2001, Neuron.

[90]  Chaozhe Zhu,et al.  Interpersonal brain synchronization in the right temporo-parietal junction during face-to-face economic exchange. , 2016, Social cognitive and affective neuroscience.

[91]  Claudio Del Percio,et al.  Brains “in concert”: Frontal oscillatory alpha rhythms and empathy in professional musicians , 2012, NeuroImage.

[92]  Christine Edwards-Groves,et al.  Teaching and Learning as Social Interaction: Salience and Relevance in Classroom Lesson Practices , 2017 .

[93]  Xu Cui,et al.  Functional near infrared spectroscopy (NIRS) signal improvement based on negative correlation between oxygenated and deoxygenated hemoglobin dynamics , 2010, NeuroImage.

[94]  Peter E. Keller,et al.  A grammar of action generates predictions in skilled musicians , 2011, Consciousness and Cognition.

[95]  Peter E. Keller,et al.  Simultaneous Cooperation and Competition in the Evolution of Musical Behavior: Sex-Related Modulations of the Singer's Formant in Human Chorusing , 2017, Front. Psychol..

[96]  Alexander W. Astin,et al.  Involvement in Learning Revisited: Lessons We Have Learned. , 1999 .

[97]  Catie Chang,et al.  Time–frequency dynamics of resting-state brain connectivity measured with fMRI , 2010, NeuroImage.

[98]  G. A. Miller THE PSYCHOLOGICAL REVIEW THE MAGICAL NUMBER SEVEN, PLUS OR MINUS TWO: SOME LIMITS ON OUR CAPACITY FOR PROCESSING INFORMATION 1 , 1956 .

[99]  Chaozhe Zhu,et al.  Neural Synchronization during Face-to-Face Communication , 2012, The Journal of Neuroscience.

[100]  Marco Ferrari,et al.  Functional Near-Infrared Spectroscopy (fNIRS) for Assessing Cerebral Cortex Function During Human Behavior in Natural/Social Situations: A Concise Review , 2019 .

[101]  Darnell G. Cole,et al.  Comparing international and American students: involvement in college life and overall satisfaction , 2017 .

[102]  Scott T. Grafton,et al.  Action outcomes are represented in human inferior frontoparietal cortex. , 2008, Cerebral cortex.

[103]  Vinod Menon,et al.  Musical structure is processed in “language” areas of the brain: a possible role for Brodmann Area 47 in temporal coherence , 2003, NeuroImage.

[104]  A. Meltzoff,et al.  Learning the rules: observation and imitation of a sorting strategy by 36-month-old children. , 2010, Developmental psychology.

[105]  R. Handberg,et al.  Automated preparation of Kepler time series of planet hosts for asteroseismic analysis , 2014, 1409.1366.

[106]  R. Zatorre,et al.  Structure and function of auditory cortex: music and speech , 2002, Trends in Cognitive Sciences.

[107]  Michel Belyk,et al.  The Neural Basis of Vocal Pitch Imitation in Humans , 2016, Journal of Cognitive Neuroscience.

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

[109]  U. Hasson,et al.  Speaker–listener neural coupling underlies successful communication , 2010, Proceedings of the National Academy of Sciences.

[110]  C. Haas,et al.  Detrended Fluctuation Analysis and Adaptive Fractal Analysis of Stride Time Data in Parkinson's Disease: Stitching Together Short Gait Trials , 2014, PloS one.

[111]  Koji Shimada,et al.  Neural substrates of shared attention as social memory: A hyperscanning functional magnetic resonance imaging study , 2016, NeuroImage.

[112]  Peter E. Keller,et al.  Interpersonal synchrony enhanced through 20 Hz phase-coupled dual brain stimulation , 2017, Social cognitive and affective neuroscience.

[113]  E. Markman,et al.  Prior experiences and perceived efficacy influence 3-year-olds' imitation. , 2008, Developmental psychology.

[114]  Y. Hu,et al.  Synchronous brain activity during cooperative exchange depends on gender of partner: A fNIRS‐based hyperscanning study , 2015, Human brain mapping.

[115]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[116]  Masamichi J. Hayashi,et al.  “Stay Tuned”: Inter-Individual Neural Synchronization During Mutual Gaze and Joint Attention , 2010, Front. Integr. Neurosci..

[117]  Diana Denton,et al.  Holistic Learning and Spirituality in Education: Breaking New Ground , 2005 .

[118]  Takayuki Nozawa,et al.  Interpersonal frontopolar neural synchronization in group communication: An exploration toward fNIRS hyperscanning of natural interactions , 2016, NeuroImage.

[119]  Uri Hasson,et al.  Mirroring and beyond: coupled dynamics as a generalized framework for modelling social interactions , 2016, Philosophical Transactions of the Royal Society B: Biological Sciences.

[120]  Michiyo Azuma,et al.  Changes in Cerebral Blood Flow during Olfactory Stimulation in Patients with Multiple Chemical Sensitivity: A Multi-Channel Near-Infrared Spectroscopic Study , 2013, PloS one.

[121]  M. Iacoboni,et al.  The mirror neuron system and the consequences of its dysfunction , 2006, Nature Reviews Neuroscience.

[122]  Kelong Lu,et al.  Cooperation makes two less-creative individuals turn into a highly-creative pair , 2018, NeuroImage.

[123]  S. Bressler,et al.  Frequency decomposition of conditional Granger causality and application to multivariate neural field potential data , 2006, Journal of Neuroscience Methods.

[124]  Yoko Hoshi,et al.  Functional near-infrared spectroscopy: current status and future prospects. , 2007, Journal of biomedical optics.