Brain-to-brain entrainment: EEG interbrain synchronization while speaking and listening

Electroencephalographic hyperscanning was used to investigate interbrain synchronization patterns in dyads of participants interacting through speech. Results show that brain oscillations are synchronized between listener and speaker during oral narratives. This interpersonal synchronization is mediated in part by a lower-level sensory mechanism of speech-to-brain synchronization, but also by the interactive process that takes place in the situation per se. These results demonstrate the existence of brain-to-brain entrainment which is not merely an epiphenomenon of auditory processing, during listening to one speaker. The study highlights the validity of the two-person neuroscience framework for understanding induced brain activity, and suggests that verbal information exchange cannot be fully understood by examining the listener’s or speaker’s brain activity in isolation.

[1]  C. Clifton,et al.  Prosodic phrasing is central to language comprehension , 2006, Trends in Cognitive Sciences.

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

[3]  Richard S. J. Frackowiak,et al.  Endogenous Cortical Rhythms Determine Cerebral Specialization for Speech Perception and Production , 2007, Neuron.

[4]  W. Klimesch Alpha-band oscillations, attention, and controlled access to stored information , 2012, Trends in Cognitive Sciences.

[5]  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.

[6]  D. Poeppel,et al.  Phase Patterns of Neuronal Responses Reliably Discriminate Speech in Human Auditory Cortex , 2007, Neuron.

[7]  U. Hasson,et al.  On the Same Wavelength: Predictable Language Enhances Speaker–Listener Brain-to-Brain Synchrony in Posterior Superior Temporal Gyrus , 2014, The Journal of Neuroscience.

[8]  Steven Greenberg,et al.  On the Possible Role of Brain Rhythms in Speech Perception: Intelligibility of Time-Compressed Speech with Periodic and Aperiodic Insertions of Silence , 2009, Phonetica.

[9]  Lucia Melloni,et al.  Brain Oscillations during Spoken Sentence Processing , 2012, Journal of Cognitive Neuroscience.

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

[11]  A. Cabrini,et al.  Sound representation in higher language areas during language generation , 2015, Proceedings of the National Academy of Sciences.

[12]  Karl J. Friston,et al.  Active inference, communication and hermeneutics , 2015, Cortex.

[13]  D. Poeppel,et al.  Mechanisms Underlying Selective Neuronal Tracking of Attended Speech at a “Cocktail Party” , 2013, Neuron.

[14]  Laura Lee Colgin,et al.  Beta and Gamma Rhythms Go with the Flow , 2015, Neuron.

[15]  D. Poeppel,et al.  Coupled neural systems underlie the production and comprehension of naturalistic narrative speech , 2014, Proceedings of the National Academy of Sciences.

[16]  S. Kotz,et al.  Rhythm's gonna get you: Regular meter facilitates semantic sentence processing , 2012, Neuropsychologia.

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

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

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

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

[21]  Jonas Obleser,et al.  Alpha Phase Determines Successful Lexical Decision in Noise , 2015, The Journal of Neuroscience.

[22]  Hugo Quené,et al.  Effects of Timing Regularity and Metrical Expectancy on Spoken-Word Perception , 2005, Phonetica.

[23]  Gregor Thut,et al.  Lip movements entrain the observers’ low-frequency brain oscillations to facilitate speech intelligibility , 2016, eLife.

[24]  R. Hari,et al.  Attending to and neglecting people: bridging neuroscience, psychology and sociology , 2016, Philosophical Transactions of the Royal Society B: Biological Sciences.

[25]  J. Palva,et al.  New vistas for alpha-frequency band oscillations. , 2007, Trends in neurosciences.

[26]  Arnaud Delorme,et al.  EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis , 2004, Journal of Neuroscience Methods.

[27]  R. Hari,et al.  Centrality of Social Interaction in Human Brain Function , 2015, Neuron.

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

[29]  J. Simon,et al.  Emergence of neural encoding of auditory objects while listening to competing speakers , 2012, Proceedings of the National Academy of Sciences.

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

[31]  Jon Andoni Duñabeitia,et al.  Differential oscillatory encoding of foreign speech , 2015, Brain and Language.

[32]  U. Lindenberger,et al.  Cardiac and Respiratory Patterns Synchronize between Persons during Choir Singing , 2011, PloS one.

[33]  J. Kelso,et al.  Functional dissociation of brain rhythms in social coordination , 2012, Clinical Neurophysiology.

[34]  Joachim Gross,et al.  Phase-Locked Responses to Speech in Human Auditory Cortex are Enhanced During Comprehension , 2012, Cerebral cortex.

[35]  David Poeppel,et al.  Cortical oscillations and speech processing: emerging computational principles and operations , 2012, Nature Neuroscience.

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

[37]  Girijesh Prasad,et al.  Electrophysiological signatures of intentional social coordination in the 10–12Hz range , 2012, NeuroImage.

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

[39]  N. Sadato,et al.  Hyperscanning neuroimaging technique to reveal the “two-in-one” system in social interactions , 2015, Neuroscience Research.

[40]  M. Pickering,et al.  An integrated theory of language production and comprehension. , 2013, The Behavioral and brain sciences.

[41]  J. Kelso,et al.  From the Cover : The phi complex as a neuromarker of human social coordination , 2007 .

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

[43]  J. Palva,et al.  New vistas for α-frequency band oscillations , 2007, Trends in Neurosciences.

[44]  D. Poeppel,et al.  Cortical Tracking of Hierarchical Linguistic Structures in Connected Speech , 2015, Nature Neuroscience.

[45]  Ankoor S. Shah,et al.  An oscillatory hierarchy controlling neuronal excitability and stimulus processing in the auditory cortex. , 2005, Journal of neurophysiology.

[46]  John J. Foxe,et al.  The Role of Alpha-Band Brain Oscillations as a Sensory Suppression Mechanism during Selective Attention , 2011, Front. Psychology.

[47]  J. Wolpaw,et al.  EMG contamination of EEG: spectral and topographical characteristics , 2003, Clinical Neurophysiology.

[48]  Cuntai Guan,et al.  Regularizing Common Spatial Patterns to Improve BCI Designs: Unified Theory and New Algorithms , 2011, IEEE Transactions on Biomedical Engineering.

[49]  Kyungmin Su,et al.  The PREP pipeline: standardized preprocessing for large-scale EEG analysis , 2015, Front. Neuroinform..

[50]  P. Schyns,et al.  Speech Rhythms and Multiplexed Oscillatory Sensory Coding in the Human Brain , 2013, PLoS biology.

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

[52]  Luc H. Arnal,et al.  Delta-Beta Coupled Oscillations Underlie Temporal Prediction Accuracy. , 2015, Cerebral cortex.

[53]  M. Jeannerod The mechanism of self-recognition in humans , 2003, Behavioural Brain Research.

[54]  R. Adolphs,et al.  What does the interactive brain hypothesis mean for social neuroscience? A dialogue , 2016, Philosophical Transactions of the Royal Society B: Biological Sciences.

[55]  A. D’Ausilio,et al.  Beta rhythm modulation by speech sounds: somatotopic mapping in somatosensory cortex , 2016, Scientific Reports.

[56]  D. Schön,et al.  Rhythmic priming enhances the phonological processing of speech , 2012, Neuropsychologia.

[57]  Sabine Weiss,et al.  “Too Many betas do not Spoil the Broth”: The Role of Beta Brain Oscillations in Language Processing , 2012, Front. Psychology.