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

Abstract 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.

[1]  R. C. Oldfield.  The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[2]  M. Brewer.  In-group bias in the minimal intergroup situation: A cognitive-motivational analysis. , 1979 .

[3]  H. Tajfel.  Social Psychology of Intergroup Relations , 1982 .

[4]  L. Lemyre,et al.  Intergroup Discrimination and Self-Esteem in the Minimal Group Paradigm , 1985 .

[5]  D. Tank,et al.  Brain magnetic resonance imaging with contrast dependent on blood oxygenation. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[6]  Karl J. Friston.  Functional and effective connectivity in neuroimaging: A synthesis , 1994 .

[7]  E. Vaughan,et al.  The Significance of Socioeconomic and Ethnic Diversity for the Risk Communication Process , 1995 .

[8]  D. Delpy,et al.  Performance comparison of several published tissue near-infrared spectroscopy algorithms. , 1995, Analytical biochemistry.

[9]  A. Villringer,et al.  Non-invasive optical spectroscopy and imaging of human brain function , 1997, Trends in Neurosciences.

[10]  C. Torrence,et al.  A Practical Guide to Wavelet Analysis. , 1998 .

[11]  J. Desmond,et al.  The role of left prefrontal cortex in language and memory. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[12]  D. Wentura,et al.  About the impact of automaticity in the minimal group paradigm: evidence from affective priming tasks , 1999 .

[13]  E. T. Possing,et al.  Human temporal lobe activation by speech and nonspeech sounds. , 2000, Cerebral cortex.

[14]  David A. Boas,et al.  A Quantitative Comparison of Simultaneous BOLD fMRI and NIRS Recordings during Functional Brain Activation , 2002, NeuroImage.

[15]  C. L. Wyland,et al.  An fMRI investigation of the impact of interracial contact on executive function , 2003, Nature Neuroscience.

[16]  S. Levin,et al.  The Effects of Ingroup and Outgroup Friendships on Ethnic Attitudes in College: A Longitudinal Study , 2003 .

[17]  Jennifer S. Beer,et al.  The regulatory function of self-conscious emotion: insights from patients with orbitofrontal damage. , 2003, Journal of personality and social psychology.

[18]  Karl J. Friston,et al.  Dynamic causal modelling , 2003, NeuroImage.

[19]  R. Malach,et al.  Intersubject Synchronization of Cortical Activity During Natural Vision , 2004, Science.

[20]  E. Harmon-Jones,et al.  Neural Signals for the Detection of Unintentional Race Bias , 2004, Psychological science.

[21]  Anders M. Dale,et al.  Diffuse optical imaging of brain activation: approaches to optimizing image sensitivity, resolution, and accuracy , 2004, NeuroImage.

[22]  T. Owens,et al.  Psychological Well-Being in the Early Life Course: Variations by Socioeconomic Status, Gender, and Race/Ethnicity , 2004 .

[23]  Masako Okamoto,et al.  Automated cortical projection of head-surface locations for transcranial functional brain mapping , 2005, NeuroImage.

[24]  R. Sapolsky.  Sick of poverty. , 2005, Scientific American.

[25]  C. Frith,et al.  Meeting of minds: the medial frontal cortex and social cognition , 2006, Nature Reviews Neuroscience.

[26]  William A. Cunningham,et al.  The Neural Substrates of In-Group Bias , 2008, Psychological science.

[27]  Andrew N. Meltzoff,et al.  Socioeconomic status predicts hemispheric specialisation of the left inferior frontal gyrus in young children , 2008, NeuroImage.

[28]  Sungho Tak,et al.  NIRS-SPM: Statistical parametric mapping for near-infrared spectroscopy , 2009, NeuroImage.

[29]  Rajeev D. S. Raizada,et al.  Effects of Socioeconomic Status on Brain Development, and How Cognitive Neuroscience May Contribute to Levelling the Playing Field , 2009, Front. Hum. Neurosci..

[30]  L. Schilbach.  A second-person approach to other minds , 2010, Nature Reviews Neuroscience.

[31]  Marleen B. Schippers,et al.  Mapping the information flow from one brain to another during gestural communication , 2010, Proceedings of the National Academy of Sciences.

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

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

[34]  Michael D. Hunter,et al.  Higher or lower? The functional anatomy of perceived allocentric social hierarchies , 2011, NeuroImage.

[35]  S. Carey,et al.  Consequences of "minimal" group affiliations in children. , 2011, Child development.

[36]  Gary H. Glover,et al.  A quantitative comparison of NIRS and fMRI across multiple cognitive tasks , 2011, NeuroImage.

[37]  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.

[38]  Christine L. Cox,et al.  Negative stereotype activation alters interaction between neural correlates of arousal, inhibition and cognitive control. , 2012, Social cognitive and affective neuroscience.

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

[40]  P. Fox,et al.  Introspective Minds: Using ALE Meta-Analyses to Study Commonalities in the Neural Correlates of Emotional Processing, Social & Unconstrained Cognition , 2012, PloS one.

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

[42]  Marco Ferrari,et al.  A brief review on the history of human functional near-infrared spectroscopy (fNIRS) development and fields of application , 2012, NeuroImage.

[43]  S. Gilbert,et al.  Evaluative vs. trait representation in intergroup social judgments: Distinct roles of anterior temporal lobe and prefrontal cortex , 2012, Neuropsychologia.

[44]  Abraham Z. Snyder,et al.  A quantitative spatial comparison of high-density diffuse optical tomography and fMRI cortical mapping , 2012, NeuroImage.

[45]  Sterling C. Johnson,et al.  A generalized form of context-dependent psychophysiological interactions (gPPI): A comparison to standard approaches , 2012, NeuroImage.

[46]  Cathy J. Price,et al.  A review and synthesis of the first 20 years of PET and fMRI studies of heard speech, spoken language and reading , 2012, NeuroImage.

[47]  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..

[48]  Heidrun Wabnitz,et al.  The physiological origin of task-evoked systemic artefacts in functional near infrared spectroscopy , 2012, NeuroImage.

[49]  F. Scholkmann,et al.  Between-brain coherence during joint n-back task performance: A two-person functional near-infrared spectroscopy study , 2012, Behavioural Brain Research.

[50]  A. Roepstorff,et al.  The two-brain approach: how can mutually interacting brains teach us something about social interaction? , 2012, Front. Hum. Neurosci..

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

[52]  Martin Wolf,et al.  End-tidal CO2: An important parameter for a correct interpretation in functional brain studies using speech tasks , 2013, NeuroImage.

[53]  Hiroki Sato,et al.  A NIRS–fMRI investigation of prefrontal cortex activity during a working memory task , 2013, NeuroImage.

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

[55]  F. Scholkmann,et al.  A new methodical approach in neuroscience: assessing inter-personal brain coupling using functional near-infrared imaging (fNIRI) hyperscanning , 2013, Front. Hum. Neurosci..

[56]  Y. Yamaguchi,et al.  Inter-brain synchronization during coordination of speech rhythm in human-to-human social interaction , 2013, Scientific Reports.

[57]  R. Saxe,et al.  Theory of Mind: A Neural Prediction Problem , 2013, Neuron.

[58]  F. Scholkmann,et al.  The effect of inner speech on arterial CO2 and cerebral hemodynamics and oxygenation: a functional NIRS study. , 2013, Advances in experimental medicine and biology.

[59]  D. Amodio.  The neuroscience of prejudice and stereotyping , 2014, Nature Reviews Neuroscience.

[60]  M. Osaka,et al.  Neural Synchronization During Cooperated Humming: A Hyperscanning Study Using fNIRS☆ , 2014 .

[61]  D. Poeppel.  The neuroanatomic and neurophysiological infrastructure for speech and language , 2014, Current Opinion in Neurobiology.

[62]  L. Schilbach,et al.  On the relationship of online and offline social cognition , 2014, Front. Hum. Neurosci..

[63]  David A. Boas,et al.  Twenty years of functional near-infrared spectroscopy: introduction for the special issue , 2014, NeuroImage.

[64]  Abraham Z. Snyder,et al.  Atlas-based head modeling and spatial normalization for high-density diffuse optical tomography: In vivo validation against fMRI , 2014, NeuroImage.

[65]  P. Hagoort.  Nodes and networks in the neural architecture for language: Broca's region and beyond , 2014, Current Opinion in Neurobiology.

[66]  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..

[67]  C. Luzzatti,et al.  Phonological rehabilitation in acquired aphasia , 2015 .

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

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

[70]  Ilias Tachtsidis,et al.  False positives and false negatives in functional near-infrared spectroscopy: issues, challenges, and the way forward , 2016, Neurophotonics.

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

[72]  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.

[73]  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.

[74]  Jingyuan E. Chen,et al.  NIRS-Based Hyperscanning Reveals Inter-brain Neural Synchronization during Cooperative Jenga Game with Face-to-Face Communication , 2016, Front. Hum. Neurosci..

[75]  J. Hirsch,et al.  Neural correlates of conflict between gestures and words: A domain-specific role for a temporal-parietal complex , 2017, PloS one.

[76]  Elise A. Piazza,et al.  Measuring speaker–listener neural coupling with functional near infrared spectroscopy , 2016, Scientific Reports.

[77]  Steve W. C. Chang,et al.  Distributed Neural Activity Patterns during Human-to-Human Competition , 2017, Front. Hum. Neurosci..

[78]  N. Wenderoth,et al.  Beyond Autism: Introducing the Dialectical Misattunement Hypothesis and a Bayesian Account of Intersubjectivity , 2017, Psychopathology.

[79]  Swethasri Dravida,et al.  Signal processing of functional NIRS data acquired during overt speaking , 2017, Neurophotonics.

[80]  Xian Zhang,et al.  Frontal temporal and parietal systems synchronize within and across brains during live eye-to-eye contact , 2017, NeuroImage.

[81]  J. Hirsch,et al.  A cross-brain neural mechanism for human-to-human verbal communication , 2018, Social cognitive and affective neuroscience.

[82]  L. Schilbach,et al.  Observing and participating in social interactions: Action perception and action control across the autistic spectrum , 2017, Developmental Cognitive Neuroscience.

[83]  J. Hirsch,et al.  Communication of emotion via drumming: dual-brain imaging with functional near-infrared spectroscopy , 2018, Social cognitive and affective neuroscience.

[84]  J. Hirsch,et al.  The present and future use of functional near‐infrared spectroscopy (fNIRS) for cognitive neuroscience , 2018, Annals of the New York Academy of Sciences.

[85]  Swethasri Dravida,et al.  Comparison of oxyhemoglobin and deoxyhemoglobin signal reliability with and without global mean removal for digit manipulation motor tasks , 2017, Neurophotonics.

[86]  Ilias Tachtsidis,et al.  A Review on the Use of Wearable Functional Near-Infrared Spectroscopy in Naturalistic Environments. , 2018, The Japanese psychological research.

[87]  M. Yartsev,et al.  Correlated Neural Activity across the Brains of Socially Interacting Bats , 2019, Cell.

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

[89]  P. Golshani,et al.  Correlated Neural Activity and Encoding of Behavior across Brains of Socially Interacting Animals , 2019, Cell.

[90]  Yumie Ono,et al.  Real-Time Eye-to-Eye Contact Is Associated With Cross-Brain Neural Coupling in Angular Gyrus , 2020, Frontiers in Human Neuroscience.