Experimental Psychology (Russia)
2021. Vol. 14, no. 4, 205–223
doi:10.17759/exppsy.2021140411
ISSN: 2072-7593 / 2311-7036 (online)
Studies of Interrelated Changes in Brain Activity During Social Interactions Using Hyperscanning
Abstract
General Information
Keywords: social interaction, hyperscanning, synchronous brain activity, electroencephalography, magnetoencephalography, functional near-infrared spectroscopy, functional magnetic resonance imaging
Journal rubric: Psychophysiology
Article type: review article
DOI: https://doi.org/10.17759/exppsy.2021140411
Funding. The reported study was funded by Russian Foundation for Basic Research (RFBR), project number 19-115-50143.
Acknowledgements. The authors are grateful for anonymous reviewer for insightful suggestings and helpful comments on our manuscript.
Received: 17.08.2020
Accepted:
For citation: Murtazina E.P., Buyanova I.S. Studies of Interrelated Changes in Brain Activity During Social Interactions Using Hyperscanning. Eksperimental'naâ psihologiâ = Experimental Psychology (Russia), 2021. Vol. 14, no. 4, pp. 205–223. DOI: 10.17759/exppsy.2021140411. (In Russ., аbstr. in Engl.)
References
- Alexandrov Yu.I. Makrostruktura deyatel’nosti I ierarhiya funkcional’nyh system [Macrostructure of activity and hierarchy of functional systems]. Psihologicheskij Zhurnal. 1995. Vol. 16. № 1. pp. 26—30. (In Russ., а in Engl.).
- Anohin P.K. Uzlovye voprosy teorii funkcional’noj sistemy [Key questions of the theory of functional systems]. K. Anohin, Izd-vo «Nauka». 1980. 196 P. (In Russ.).
- Apanovich V.V., Bezdenezhnyh B.N., Znakov V.V., Sams M., Yaaskelajnen I., Aleksandrov Yu.I. Razlichiya mozgovogo obespecheniya individual’nogo, kooperativnogo I konkurentnogo povedeniya u sub”ektov s analiticheskim i holisticheskim kognitivnymi stilyami [Differences in the brain supply of individual, cooperative and competitive behavior in subjects with analytical and holistic cognitive styles]. Eksperimental’naya psihologiya. 2016. Vol. 9. № 2. pp. 5—22. DOI:10.17759/exppsy.2016090202 DOI:10.17759/exppsy.2016090202 (In Russ., а in Engl.)
- Zhuravlev A.L., Yurevich A.V. Vmesto vvedeniya: osnovnye tipy tendencij razvitiya psihologii [Instead of an introduction: the main types of trends in the development of psychology]. Novye tendencii I perspektivy psihologicheskoj nauki / Otv. red. A.L. Zhuravlev, A.V. Yurevich. : IP RAN. 2019. pp. 5—8. (In Russ.).
- Murtazina E.P., Matyul’ko I.S., Zhuravlev B.V. Somatovegetativnye komponenty social’nyh vzaimodejstvij (obzor) [Somato-vegetative components of social interactions (review)]. Zhurnal Mediko-Biologicheskih Issledovanij. 2019. Vol. 7. № 3. pp. 349—362. DOI:10.17238/issn2542-1298.2019.7.3.349. (In Russ., а in Engl.).
- Abe M.O., Koike T., Okazaki S., Sugawara S.K., Takahashi K., Watanabe K., Sadato N. Neural correlates of online cooperation during joint force production // NeuroImage. Vol. 191. P. 150—161. DOI:10.1016/j.neuroimage.2019.02.003
- Ahn S., Cho H., Kwon M., Kim K., Kwon H., Kim B.S., Chang W.S., Chang W.J., Jun S.Ch. Interbrain phase synchronization during turn-taking verbal interaction—a hyperscanning study using simultaneous EEG/MEG // Human Brain Mapping. Vol. 39. № 1. P. 171—188. DOI:10.1002/hbm.23834
- Allsop J.S., Vaitkus T., Marie D., Miles L. Coordination and collective performance: cooperative goals boost interpersonal synchrony and task outcomes // Frontiers in Psychology. Vol. 7. P. 1462. DOI:10.3389/fpsyg.2016.01462
- Anders S., Heinzle J., Weiskopf N., Ethofer T., John-Dylan Haynes J.-D. Flow of affective information between communicating brains // NeuroImage. Vol. 54. № 1. P. 439—446. DOI:10.1016/j. neuroimage.2010.07.004
- Ayrolles A., Brun F., Chen P., Djalovski A., Beauxis Y., Delorme R., Bourgeron T., Dikker S., Dumas G. HyPyP: a Hyperscanning Python Pipeline for inter-brain connectivity analysis // Soc Cogn Affect Neurosci. Vol. 16. № 1-2). P. 72-83. DOI:10.1093/scan/nsaa141
- Babiloni F., Astolfi L. Social neuroscience and hyperscanning techniques: past, present and future // Neuroscience and biobehavioral reviews. Vol. 44. P. 76—93. DOI:10.1016/j.neubiorev.2012.07.006
- Babiloni F., Astolfi L., Cincotti F., Mattia D., Tocci A., Tarantino A., Marciani Mg., Salinari S., Gao S., Colosimo A., De Vico Fallani F. Cortical activity and connectivity of human brain during the Prisoner’s Dilemma: an EEG hyperscanning study // 2007. 4953—4956. DOI:10.1109/IEMBS.2007.4353452
- Balconi M., Vanutelli M.E. Brains in competition: improved cognitive performance and inter-brain coupling by hyperscanning paradigm with functional near-infrared spectroscopy // Frontiers in Behavioral Neuroscience. Vol. 11. P. 163. DOI:10.3389/fnbeh.2017.00163
- Balconi M., Vanutelli M.E. Cooperation and competition with hyperscanning methods: review and future application to emotion domain // Frontiers in Computational Neuroscience. 2017. Vol. 11. P. 86. DOI:10.3389/fncom.2017.00086
- Bevilacqua D., Davidesco I., Wan L., Chaloner K., Rowland J., Ding M., Poeppel D., Dikker S. Brain-to-Brain synchrony and learning outcomes vary by student—teacher dynamics: evidence from a real-world classroom electroencephalography study // Journal of Cognitive Neuroscienc 2018. Vol. 31. № 3. P. 401— 411. DOI:10.1162/jocn_a_01274
- Bilek E., Ruf M., Schäfer A., Akdeniz C., Calhoun V.D., Schmahl C., Demanuele C., Tost H., Kirsch P., Meyer-Lindenberg A. Information flow between interacting human brains: Identification, validation, and relationship to social expertise // Proceedings of the National Academy of Sciences. Vol. 112. № 16. P. 5207—5212. DOI:10.1073/pnas.1421831112
- Caruana N., Brock J., Woolgar A. A frontotemporoparietal network common to initiating and responding to joint attention bids // NeuroImage. Vol. 108. P. 34—46. DOI:10.1016/j.neuroimage.2014.12.041
- Ciaramidaro A., Becchio C., Colle L., Bara B.G., Walter H. Do you mean me? Communicative intentions recruit the mirror and the mentalizing system // Social Cognitive and Affective Neuroscience. Vol. 9. № 7. P. 909—916. DOI:10.1093/scan/nst062
- Czeszumski A., Eustergerling S., Lang A., Menrath D., Gerstenberger M., Schuberth S., Schreiber F., Rendon Z.Z., König P. Hyperscanning: a valid method to study neural inter-brain underpinnings of social interaction // Frontiers in Human Neuroscience. Vol. 14. P. 39. DOI:10.3389/fnhum.2020.00039
- Davidesco I., Laurent E., Valk H., West T., Dikker S., Milne C., Poeppel D. Brain-to-brain synchrony between students and teachers predicts learning outcomes // bioRxiv. P. 644047. DOI:10.1101/644047
- Dikker S., Wan L., Davidesco I., Kaggen L., Oostrik M., James McClintock J., Rowland J., Michalareas G., Van Bavel J.J., Ding M., Poeppel D. Brain-to-brain synchrony tracks real-world dynamic group interactions in the classroom // Current Biology. Vol. 27. № 9. P. 1375—1380. DOI:10.1016/j.cub.2017.04.002
- Dmochowski J.P., Sajda P., Dias J., Parra L.C. Correlated components of ongoing eeg point to emotionally laden attention — a possible marker of engagement? // Frontiers in Human Neuroscience. Vol. 6. P. 112. DOI:10.3389/fnhum.2012.00112
- Duane T.D., Behrendt T. Extrasensory electroencephalographic induction between identical twins // Science (New York, N.Y.). Vol. 150. № 3694. P. 367. DOI:10.1126/science.150.3694.367
- Dumas G., Martinerie J., Soussignan R., Nadel J. Does the brain know who is at the origin of what in an imitative interaction? // Frontiers in Human Neuroscience. Vol. 6. P. 128. DOI:10.3389/ fnhum.2012.00128
- Dumas G., Nadel J., Soussignan R., Martinerie J., Garnero L. Inter-brain synchronization during social interaction // PLOS ONE. 2010. 5. № 8. P. e12166. DOI:10.1371/journal.pone.0012166
- Fallani F.D.V., Nicosia V., Sinatra R., Astolfi L., Cincotti F., Mattia D., Wilke C., Doud A., Latora V., He B., Babiloni F. Defecting or not defecting: how to “read” human behavior during cooperative games by EEG measurements // PLOS ONE. 2010. 5. № 12. P. e14187. DOI:10.1371/journal.pone.0014187
- Funane T., Kiguchi M., Atsumori H., Sato H., Kubota K., Koizumi H. Synchronous activity of two people’s prefrontal cortices during a cooperative task measured by simultaneous near-infrared spectroscopy // Journal of Biomedical Optics. Vol. 16. № 7. P. 077011. DOI:10.1117/1.3602853
- Gebauer L., Witek M.G., Hansen N.C., Thomas J., Konvalink, I., Vuust P. Oxytocin improves synchronisation in leader-follower interaction // Scientific Reports. Vol. 6. № 1. P. 38416. DOI:10.1038/srep38416
- Hari R., Kujala M. Brain basis of human social interaction: from concepts to brain imaging // Physiological reviews. Vol. 89. P. 453—79. DOI:10.1152/physrev.00041.2007
- Hasson U, Frith CD. Mirroring and beyond: coupled dynamics as a generalized framework for modelling social interactions // Philos Trans R Soc Lond B Biol Sci. 2016. 371. P. 1693. DOI:10.1098/rstb.2015.0366
- Hirsch J., Adam Noah J., Zhang X., Dravida S., Ono Y. A cross-brain neural mechanism for human-to-human verbal communication // Social Cognitive and Affective Neuroscience. Vol. 13. № 9. P. 907— 920. DOI:10.1093/scan/nsy070
- Hirsch J., Zhang X., Noah J.A., Ono Y. Frontal temporal and parietal systems synchronize within and across brains during live eye-to-eye contact // NeuroImage. Vol. 157. P. 314—330. DOI:10.1016/j. neuroimage.2017.06.018
- Hu Y., Hu Y., Li X., Pan Y., Cheng X. Brain-to-brain synchronization across two persons predicts mutual prosociality // Social Cognitive and Affective Neuroscience. 2017. Vol. 12. № 12. P. 1835—1844. DOI:10.1093/scan/nsx118
- Hu Y., Pan Y., Shi X., Cai Q., Li X., Cheng X. Inter-brain synchrony and cooperation context in interactive decision making // Biological Psychology. Vol. 133. P. 54—62. DOI:10.1016/j.biopsycho.2017.12.005
- Jiang J., Dai B., Peng D., Zhu C., Liu L., Lu C. Neural Synchronization during Face-to-Face Communication // Journal of Neuroscience. Vol. 32. № 45. P. 16064—16069. DOI:10.1016/j. neuroimage.2017.06.024
- Josef L., Goldstein P., Mayseless N., Ayalon L., Shamay-Tsoory S.G. The oxytocinergic system mediates synchronized interpersonal movement during dance // Scientific Reports. Vol. 9. № 1. P. 1894. DOI:10.1038/s41598-018-37141-1
- Kawasaki M., Yamada Y., Ushiku Y., Miyauchi E., Yamaguchi Y. Inter-brain synchronization during coordination of speech rhythm in human-to-human social interaction // Scientific Reports. Vol. 3. № 1. P. 1—8. DOI:10.1038/srep01692
- Koike T., Tanabe H.C., Okazaki S., Nakagawa E., Sasaki A.T., Shimada K., Sugawara S.K., Takahashi H.K., Yoshihara K., Bosch-Bayard J., Sadato N. Neural substrates of shared attention as social memory: A hyperscanning functional magnetic resonance imaging study // NeuroImage. Vol. 125. P. 401—412. DOI:10.1016/j.neuroimage.2015.09.076
- Kuhlen A.K., Allefeld C., Haynes J.-D. Content-specific coordination of listeners’ to speakers’ EEG during communication // Frontiers in Human Neuroscience. Vol. 6. P. 266. DOI:10.3389/fnhum.2012.00266
- Lachat F., Hugeville L., Lemarechal J.-D., Conty L., George N. Oscillatory brain correlates of live joint attention: a dual-EEG study // Frontiers in Human Neuroscience. Vol. 6. P. 156. DOI:10.3389/ fnhum.2012.00156
- Lee R.F., Dai W., Jones J. Decoupled circular-polarized dual-head volume coil pair for studying two interacting human brains with dyadic fMRI // Magnetic Resonance in Medicine. Vol. 68. № 4. P. 1087—1096. DOI:10.1002/mrm.23313
- Lee S., Cho H., Kim K., Jun S.C. Simultaneous EEG acquisition system for multiple users: development and related issues // Sensors. Vol. 19. № 20. P. 4592. DOI:10.3390/s19204592
- Leong V., Schilbach L. The promise of two-person neuroscience for developmental psychiatry: using interaction-based sociometrics to identify disorders of social interaction // The British Journal of Psychiatry. Vol. 215. № 5. P. 636—638. DOI:10.1192/bjp.2019.73.
- Levy J., Goldstein A., Feldman R. Perception of social synchrony induces mother—child gamma coupling in the social brain // Social Cognitive and Affective Neuroscience. Vol. 12. № 7. P. 1036— 1046. DOI:10.1093/scan/nsx032
- Li T., Li G., Xue T., Zhang J. Analyzing brain connectivity in the mutual regulation of emotion— movement using bidirectional granger causality // Frontiers in Neuroscience. Vol. 14. P. 369. DOI:10.3389/fnins.2020.00369
- Liu D., Liu S., Liu X., Zhang C., Li A., Jin C., Chen Y., Wang H., Zhang X. Interactive brain activity: review and progress on EEG-based hyperscanning in social interactions // Frontiers in Psychology. Vol. 9. P. 1862. DOI:10.3389/fpsyg.2018.01862
- Mandel A., Bourguignon M., Parkkonen L., Hari R. Sensorimotor activation related to speaker vs. listener role during natural conversation // Neuroscience Letters. Vol. 614. P. 99—104. DOI:10.1016/j. neulet.2015.12.054
- Montague P.R., Berns G.S., Cohen J.D.,King R.D., Apple N., Fisher R.E. Hyperscanning: simultaneous fMRI during linked social interactions // NeuroImage. Vol. 16. № 4. P. 1159—1164. DOI:10.1006/ nimg.2002.1150
- Mu Y., Guo C., Han S. Oxytocin enhances inter-brain synchrony during social coordination in male adults // Social Cognitive and Affective Neuroscience. Vol. 11. № 12. P. 1882—1893. DOI:10.1093/ scan/nsw106
- Müller V., Lindenberger U. Hyper-brain networks support romantic kissing in humans // PLoS ONE. 2014. 9. № 11. DOI:10.1371/journal.pone.0112080.
- Müller V., Sänger J., Lindenberger U. Intra- and inter-brain synchronization during musical improvisation on the guitar // PloS One. 2013. 8. № 9. P. e73852. DOI:10.1093/scan/nsw106
- Naeem M., Prasad G., Watson D.R., Kelso J.A.S. Functional dissociation of brain rhythms in social coordination // Clinical Neurophysiology. 2012b. Vol. 123. № 9. P. 1789—1797. DOI:10.1016/j. clinph.2012.02.065
- Nastase S.A., Gazzola V., Hasson U., Keysers C. Measuring shared responses across subjects using intersubject correlation // Social Cognitive and Affective Neuroscience. Vol. 14. № 6. P. 667—685. DOI:10.1093/scan/nsz037
- Novembre G., Knoblich G., Dunne L., Keller P.E. Interpersonal synchrony enhanced through 20 Hz phase-coupled dual brain stimulation // Social Cognitive and Affective Neuroscience. Vol. 12. № 4. P. 662—670. DOI:10.1093/scan/nsw172
- Novembre G., Sammler D., Keller P.E. Neural alpha oscillations index the balance between self-other integration and segregation in real-time joint action // Neuropsychologia. Vol. 89. P. 414—425. DOI:10.1016/j.neuropsychologia.2016.07.027
- Nozawa T., Sasaki Y., Sakaki K., Yokoyama R., Kawashima R. Interpersonal frontopolar neural synchronization in group communication: An exploration toward fNIRS hyperscanning of natural interactions // NeuroImage. Vol. 133. P. 484—497. DOI:10.1016/j.neuroimage.2016.03.059
- Pan Y., Cheng X. Two-person approaches to studying social interaction in psychiatry: uses and clinical relevance // Frontiers in Psychiatry. Vol. 11. P. 301. DOI:10.3389/fpsyt.2020.00301
- Pan Y., Cheng X., Zhang Z., Li X., Hu Y. Cooperation in lovers: An fNIRS-based hyperscanning study. // Human Brain Mapping. Vol. 38. № 2. P. 831—841. DOI:10.1002/hbm.23421
- Pan Y., Dikker S., Goldstein P., Zhu Y., Yang C., Hu Y. Instructor-learner brain coupling discriminates between instructional approaches and predicts learning // NeuroImage. Vol. 211. P. 116657. DOI:10.1016/j.neuroimage.2020.116657
- Poulsen A.T., Kamronn S., Dmochowski J., Parra L.C., Hansen L.K. EEG in the classroom: synchronised neural recordings during video presentation // Scientific Reports. Vol. 7. № 1. P. 43916. DOI:10.1038/ srep43916
- Redcay E., Dodell-Feder D., Pearrow M.J., Mavros P.L., Kleiner M., Gabrieli J.D.E., Saxe R. Live face-to-face interaction during fMRI: a new tool for social cognitive neuroscience // NeuroImage. Vol. 50. № 4. P. 1639—1647. DOI:10.1016/j.neuroimage.2010.01.052
- Redcay E., Schilbach L. Using second-person neuroscience to elucidate the mechanisms of social interaction // Nature Reviews Neuroscience. Vol. 20. № 8. P. 495—505. DOI:10.1038/s41583-019-0179-4
- Renvall V., Kauramäki J., Malinen S., Hari R., Nummenmaa L. Imaging real-time tactile interaction with two-person dual-coil fMRI // Frontiers in Psychiatry. Vol. 11. P. 279. DOI:10.3389/fpsyt.2020.00279
- Saito D.N., Tanabe H.C., Izuma K., Hayashi M.J., Morito Y., Komeda H., Uchiyama H., Kosaka H., Okazawa H., Fujibayashi Y., Sadato N. “Stay tuned”: inter-individual neural synchronization during mutual gaze and joint attention // Frontiers in Integrative Neuroscience. Vol. 4. P. 127. DOI:10.3389/ fnint.2010.00127
- Sänger J., Müller V., Lindenberger U. Intra- and interbrain synchronization and network properties when playing guitar in duets // Frontiers in Human Neuroscience. Vol. 6. P. 312. DOI:10.3389/ fnhum.2012.00312
- Schilbach L., Timmermans B., Reddy V., Costall A., Bente G., Schlicht T., Vogeley K. Toward a second-person neuroscience // Behavioral and Brain Sciences. Vol. 36. № 4. P. 393—414. DOI:10.1017/ S0140525X12000660
- Schilbach L., Wilms M., Eickhoff S.B., Romanzetti S., Tepest R., Bente G., Shah N.J., Fink G.R., Vogeley K. Minds made for sharing: initiating joint attention recruits reward-related neurocircuitry // Journal of Cognitive Neuroscience. Vol. 22. № 12. P. 2702—2715. DOI:10.1162/jocn.2009.21401
- Schirmer A, Fairhurst M, Hoehl S. Being ‘in sync’-is interactional synchrony the key to understanding the social brain? // Soc Cogn Affect Neurosci. 2021; Vol. 16. № 1-2. P. 1-4. DOI:10.1093/scan/nsaa148
- Stolk A., Noordzij M.L., Verhagen L., Volman I., Schoffelen J.-M., Oostenveld R., Hagoort P., Toni I. Cerebral coherence between communicators marks the emergence of meaning // Proceedings of the National Academy of Sciences. Vol. 111. № 51. P. 18183—18188. DOI:10.1073/pnas.1414886111
- Szymanski C., Müller V., Brick T.R., von Oertzen T., Lindenberger U. Hyper-transcranial alternating current stimulation: experimental manipulation of inter-brain synchrony // Frontiers in Human Neuroscience. Vol. 11. P. 539. DOI:10.3389/fnhum.2017.00539
- Szymanski C., Pesquita A., Brennan A.A., Perdikis D., Enns J.T., Brick T.R., Müller V., Lindenberger U. Teams on the same wavelength perform better: Inter-brain phase synchronization constitutes a neural substrate for social facilitation // NeuroImage. 2017. Vol. 152. P. 425—436. DOI:10.1016/j. neuroimage.2017.03.013
- Tomlin D., Kayali M.A., King-Casas B., Anen C., Camerer C.F., Quartz S.R., Montague P.R. Agent-specific responses in the cingulate cortex during economic exchanges // Science. Vol. 312. № 5776. P. 1047—1050. DOI:10.1126/science.1125596
- Toppi J., Borghini G., Petti M., He E.J., Giusti V.D., He B., Astolfi L., Babiloni F. Investigating cooperative behavior in ecological settings: an EEG hyperscanning study // PLOS ONE. 2016. 11. № 4. P. e0154236. DOI:10.1371/journal.pone.0154236
- Wang C., Zhang T., Shan Z., Liu J., Yuan D., Li X. Dynamic interpersonal neural synchronization underlying pain-induced cooperation in females // Human Brain Mapping. Vol. 40. № 11. P. 3222— 3232. DOI:10.1002/hbm.24592
- Xu J., Slagle J.M., Banerjee A., Bracken B., Weinger M.B. Use of a portable functional near-infrared spectroscopy (fNIRS) system to examine team experience during crisis event management in clinical simulations // Frontiers in Human Neuroscience. Vol. 13. P. 85. DOI:10.3389/fnhum.2019.00085
- Yun K., Chung D., Jeong J. Emotional interactions in human decision making using EEG hyperscanning // In Proceedings of the 6th International Conference on Cognitive Science. P. 327-330.
- Zhang M., Liu T., Pelowski M., Yu D. Gender difference in spontaneous deception: A hyperscanning study using functional near-infrared spectroscopy // Scientific Reports. Vol. 7. № 1. P. 7508. DOI:10.1038/s41598-017-06764-1
- Zhang Y., Meng T., Hou Y., Pan Y., Hu Y. Interpersonal brain synchronization associated with working alliance during psychological counseling // Psychiatry Research: Neuroimaging. V. 282. P. 103—109. DOI:10.1016/j.pscychresns.2018.09.007
- Zhdanov A., Nurminen J., Baess P., Hirvenkari L., Jousmäki V., Mäkelä P., Mandel A., Meronen L., Hari R., Parkkonen L. An internet-based real-time audiovisual link for dual MEG recordings // PLOS ONE. 2015. Vol. 10. № 6. P. e0128485. DOI:10.1371/journal.pone.0128485
- Zhou G., Bourguignon M., Parkkonen L., Hari R. Neural signatures of hand kinematics in leaders vs. followers: A dual-MEG study // NeuroImage. Vol. 125. P. 731—738. DOI:10.1016/j. neuroimage.2015.11.002
Information About the Authors
Metrics
Views
Total: 663
Previous month: 28
Current month: 7
Downloads
Total: 203
Previous month: 3
Current month: 1