Frontal alpha oscillations distinguish leaders from followers: Multivariate decoding of mutually interacting brains

NeuroImage

Volumn 94, Issue , 2014, Pages 79-88

  Konvalinka, Ivana ^a,b   Bauer, Markus ^c,d   Stahlhut, Carsten ^b   Hansen, Lars Kai ^b   Roepstorff, Andreas ^a   Frith, Chris D ^a,c  

^a AARHUS UNIVERSITY   (Denmark)

^b TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

Dual EEG; Interpersonal coordination; Leader follower dynamics; Multivariate decoding; Social interaction

Indexed keywords

ADAPTATION; ALPHA RHYTHM; ARTICLE; BETA RHYTHM; COMPUTER; CONTROLLED STUDY; COORDINATION; FEMALE; FINGER; FINGER TAPPING; FOLLOWER; FRONTAL CORTEX; HUMAN; HUMAN EXPERIMENT; LEADERSHIP; MALE; MISCELLANEOUS NAMED GROUPS; MULTIVARIATE ANALYSIS; NERVOUS SYSTEM FUNCTION; NORMAL HUMAN; PLANNING; PRIORITY JOURNAL; SOCIAL COGNITION; SOCIAL INTERACTION; SOCIAL ISOLATION; TASK PERFORMANCE; ADULT; BIOLOGICAL MODEL; BIOLOGICAL RHYTHM; BRAIN; BRAIN MAPPING; COMPUTER SIMULATION; FRONTAL LOBE; HUMAN RELATION; PHYSIOLOGY; PROCEDURES; REPRODUCIBILITY; SENSITIVITY AND SPECIFICITY; SOCIAL DOMINANCE; STATISTICAL ANALYSIS; STATISTICAL MODEL; YOUNG ADULT;

ADULT; ALPHA RHYTHM; BIOLOGICAL CLOCKS; BRAIN; BRAIN MAPPING; COMPUTER SIMULATION; DATA INTERPRETATION, STATISTICAL; FEMALE; FRONTAL LOBE; HUMANS; INTERPERSONAL RELATIONS; LEADERSHIP; MALE; MODELS, NEUROLOGICAL; MODELS, STATISTICAL; MULTIVARIATE ANALYSIS; REPRODUCIBILITY OF RESULTS; SENSITIVITY AND SPECIFICITY; SOCIAL DOMINANCE; YOUNG ADULT;

EID: 84898645311     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2014.03.003     Document Type: Article

References (74)

1. Anders S., Heinzle J., Weiskopf N., Ethofer T., Haynes J.D. Flow of affective information between communicating brains. Neuroimage 2011, 54:439-446.
2. Astolfi L., Toppi J., De Vico Fallani F., Vecchiato G., Salinari S., Mattia D., Cincotti F., Babiloni F. Neuroelectrical hyperscanning measures simultaneous brain activity in humans. Brain Topogr. 2010, 23:243-256.
3. Babiloni F., Astolfi L. Social neuroscience and hyperscanning techniques: past, present and future. Neurosci. Biobehav. Rev 2012, (in press). 10.1016/j.neubiorev.2012.07.006.
4. Babiloni F., Cincotti F., Mattia D., De Vico Fallani F., Tocci A., Bianchi L., Salinari S., Marciani M., Colosimo A., Astolfi L. High resolution EEG hyperscanning during a card game. Conf. Proc. IEEE Eng. Med. Biol. Soc. 2007, 2007:4957-4960.
5. Bauer M., Kennett S., Driver J. Attentional selection of location and modality in vision and touch modulates low-frequency activity in associated sensory cortices. J. Neurophysiol. 2012, 107:2342-2351.
6. Caetano G., Jousmaki V., Hari R. Actor's and observer's primary motor cortices stabilize similarly after seen or heard motor actions. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:9058-9062.
7. Cochin S., Barthelemy C., Roux S., Martineau J. Observation and execution of movement: similarities demonstrated by quantified electroencephalography. Eur. J. Neurosci. 1999, 11:1839-1842.
8. Cui X., Bryant D.M., Reiss A.L. NIRS-based hyperscanning reveals increased interpersonal coherence in superior frontal cortex during cooperation. Neuroimage 2012, 59:2430-2437.
9. De Jaegher H. Social understanding through direct perception? Yes, by interacting. Conscious. Cogn. 2009, 18:535-542. (discussion 543-550).
10. de Lange F.P., Jensen O., Bauer M., Toni I. Interactions between posterior gamma and frontal alpha/beta oscillations during imagined actions. Front. Hum. Neurosci. 2008, 2:7.
11. De Vico Fallani F., 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:e14187.
12. Decety J., Chaminade T., Grezes J., Meltzoff A.N. A PET exploration of the neural mechanisms involved in reciprocal imitation. Neuroimage 2002, 15:265-272.
13. Dodel S., Cohn J., Mersmann J., Luu P., Forsythe C., Jirsa V. Brain signatures of team performance. Lecture Notes in Computer Science 2011, 6780:288-297.
14. Dumas G., Nadel J., Soussignan R., Martinerie J., Garnero L. Inter-brain synchronization during social interaction. PLoS One 2010, 5:e12166.
15. Dumas G., Lachat F., Martinerie J., Nadel J., George N. From social behaviour to brain synchronization: review and perspectives in hyperscanning. IRBM 2011, 32:48-53.
16. Dumas G., Martinerie J., Soussignan R., Nadel J. Does the brain know who is at the origin of what in an imitative interaction?. Front. Hum. Neurosci. 2012, 6:128.
17. Fairhurst M.T., Janata P., Keller P.E. Leading the follower: an fMRI investigation of dynamic cooperativity and leader-follower strategies in synchronization with an adaptive virtual partner. Neuroimage 2013, 84C:688-697.
18. Gastaut H. Etude electrocorticographique de la reactivite des rythmes rolandiques. Rev. Neurol. 1952, 87:176-182.
19. Gastaut H., Bert J. EEG changes during cinematographic presentation. Electroencephalogr. Clin. Neurophysiol. 1954, 6:433-444.
20. Guionnet S., Nadel J., Bertasi E., Sperduti M., Delaveau P., Fossati P. Reciprocal imitation: toward a neural basis of social interaction. Cereb. Cortex 2012, 22:971-978.
21. Guyon I., Elisseeff A. An introduction to variable and feature selection. J. Mach. Learn. Res. 2003, 3:1157-1182.
22. Hari R. Action-perception connection and the cortical mu rhythm. Prog. Brain Res. 2006, 159:253-260.
23. Hari R., Kujala M.V. Brain basis of human social interaction: from concepts to brain imaging. Physiol. Rev. 2009, 89:453-479.
24. Hari R., Forss N., Avikainen S., Kirveskari E., Salenius S., Rizzolatti G. Activation of human primary motor cortex during action observation: a neuromagnetic study. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:15061-15065.
25. Hari R., Himberg T., Nummenmaa L., Hamalainen M., Parkkonen L. Synchrony of brains and bodies during implicit interpersonal interaction. Trends Cogn. Sci. 2013, 17:105-106.
26. Hasson U., Ghazanfar A.A., Galantucci B., Garrod S., Keysers C. Brain-to-brain coupling: a mechanism for creating and sharing a social world. Trends Cogn. Sci. 2012, 16:114-121.
27. Haynes J., Rees G. Decoding mental states from brain activity in humans. Nat. Neurosci. 2006, 7:523-534.
28. Holper L., Scholkmann F., Wolf M. Between-brain connectivity during imitation measured by fNIRS. Neuroimage 2012, 63:212-222.
29. Jensen O., Mazaheri A. Shaping functional architecture by oscillatory alpha activity: gating by inhibition. Front. Hum. Neurosci. 2010, 4:186.
30. Jiang J., Dai B., Peng D., Zhu C., Liu L., Lu C. Neural synchronization during face-to-face communication. J. Neurosci. 2012, 32:16064-16069.
31. Jung T.P., Makeig S., Humphries C., Lee T.W., McKeown M.J., Iragui V., Sejnowski T.J. Removing electroencephalographic artifacts by blind source separation. Psychophysiology 2000, 37:163-178.
32. Kilner J.M., Marchant J.L., Frith C.D. Relationship between activity in human primary motor cortex during action observation and the mirror neuron system. PLoS One 2009, 4:e4925.
33. King-Casas B., Tomlin D., Anen C., Camerer C.F., Quartz S.R., Montague P.R. Getting to know you: reputation and trust in a two-person economic exchange. Science 2005, 308:78-83.
34. Klimesch W., Sauseng P., Hanslmayr S. EEG alpha oscillations: the inhibition-timing hypothesis. Brain Res. Rev. 2007, 53:63-88.
35. Knoblich G., Jordan J.S. Action coordination in groups and individuals: learning anticipatory control. J. Exp. Psychol. Learn. Mem. Cogn. 2003, 29:1006-1016.
36. Kokal I., Gazzola V., Keysers C. Acting together in and beyond the mirror neuron system. Neuroimage 2009, 47:2046-2056.
37. Konvalinka I., Roepstorff A. The two-brain approach: how can mutually interacting brains teach us something about social interaction?. Front. Hum. Neurosci. 2012, 6:215.
38. Konvalinka I., Vuust P., Roepstorff A., Frith C.D. A coupled oscillator model of interactive tapping. Proceedings of the 7th Triennial Conference of European Society for the Cognitive Sciences of Music (ESCOM) 2009, University of Jyväskylä, Finland. J. Louhivuori, T. Eerola, S. Saarikallio, T. Himberg, P.-S. Eerola (Eds.).
39. Konvalinka I., Vuust P., Roepstorff A., Frith C.D. Follow you, follow me: continuous mutual prediction and adaptation in joint tapping. Q. J. Exp. Psychol. (Colch.) 2010, 63:2220-2230.
40. Kourtis D., Sebanz N., Knoblich G. Predictive representation of other people's actions in joint action planning: an EEG study. Soc. Neurosci. 2012, 8:31-42.
41. Kuhlen A.K., Allefeld C., Haynes J.D. Content-specific coordination of listeners' to speakers' EEG during communication. Front. Hum. Neurosci. 2012, 6:266.
42. Kuhlman W.N. Functional topography of the human mu rhythm. Electroencephalogr. Clin. Neurophysiol. 1978, 44:83-93.
43. Lachat F., Hugueville L., Lemarechal J.D., Conty L., George N. Oscillatory brain correlates of live joint attention: a dual-EEG study. Front. Hum. Neurosci. 2012, 6:156.
44. Lemm S., Blankertz B., Dickhaus T., Muller K.R. Introduction to machine learning for brain imaging. Neuroimage 2011, 56:387-399.
45. Lindenberger U., Li S.C., Gruber W., Muller V. Brains swinging in concert: cortical phase synchronization while playing guitar. BMC Neurosci. 2009, 10:22.
46. Mardia K.V., Jupp P.E. Directional Statistics 2000, Wiley, Chichester, UK.
47. Maris E., Oostenveld R. Nonparametric statistical testing of EEG- and MEG-data. J. Neurosci. Methods 2007, 164:177-190.
48. Masumoto J., Inui N. Two heads are better than one: both complementary and synchronous strategies facilitate joint action. J. Neurophysiol. 2013, 109:1307-1314.
49. Miller E.K., Cohen J.D. An integrative theory of prefrontal cortex function. Annu. Rev. Neurosci. 2001, 24:167-202.
50. Mitchell J.P., Macrae C.N., Banaji M.R. Dissociable medial prefrontal contributions to judgments of similar and dissimilar others. Neuron 2006, 50:655-663.
51. Montague P.R., Berns G.S., Cohen J.D., McClure S.M., Pagnoni G., Dhamala M., Wiest M.C., Karpov I., King R.D., Apple N., Fisher R.E. Hyperscanning: simultaneous fMRI during linked social interactions. Neuroimage 2002, 16:1159-1164.
52. Naeem M., Prasad G., Watson D.R., Kelso J.A. Electrophysiological signatures of intentional social coordination in the 10-12Hz range. Neuroimage 2012, 59:1795-1803.
53. Naeem M., Prasad G., Watson D.R., Kelso J.A. Functional dissociation of brain rhythms in social coordination. Clin. Neurophysiol. 2012, 123:1789-1797.
54. Noy L., Dekel E., Alon U. The mirror game as a paradigm for studying the dynamics of two people improvising motion together. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:20947-20952.
55. Oostenveld R., Fries P., Maris E., Schoffelen J.M. FieldTrip: open source software for advanced analysis of MEG, EEG, and invasive electrophysiological data. Comput. Intell. Neurosci. 2011, 2011:156869.
56. Pecenka N., Keller P.E. The role of temporal prediction abilities in interpersonal sensorimotor synchronization. Exp. Brain Res. 2011, 211:505-515.
57. Pfurtscheller G., Lopes da Silva F.H. Event-related EEG/MEG synchronization and desynchronization: basic principles. Clin. Neurophysiol. 1999, 110:1842-1857.
58. Sacheli L.M., Tidoni E., Pavone E.F., Aglioti S.M., Candidi M. Kinematics fingerprints of leader and follower role-taking during cooperative joint actions. Exp. Brain Res. 2013, 226:473-486.
59. 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. Front. Integr. Neurosci. 2010, 4:127.
60. Sanger J., Muller V., Lindenberger U. Intra- and interbrain synchronization and network properties when playing guitar in duets. Front. Hum. Neurosci. 2012, 6:312.
61. Sanger J., Muller V., Lindenberger U. Directionality in hyperbrain networks discriminates between leaders and followers in guitar duets. Front. Hum. Neurosci. 2013, 7:234.
62. Schilbach L., Timmermans B., Reddy V., Costall A., Bente G., Schlicht T., Vogeley K. Toward a second-person neuroscience. Behav. Brain Sci. 2013, 36:393-414.
63. Schippers M.B., Roebroeck A., Renken R., Nanetti L., Keysers C. Mapping the information flow from one brain to another during gestural communication. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:9388-9393.
64. Sebanz N., Bekkering H., Knoblich G. Joint action: bodies and minds moving together. Trends Cogn. Sci. 2006, 10:70-76.
65. Stauffer H.B. An introduction to generalized linear models: logistic regression models. Contemporary Bayesian and Frequentist Statistical Research Methods for Natural Resource Scientists 2008, 155-190.
66. Stephens G.J., Silbert L.J., Hasson U. Speaker-listener neural coupling underlies successful communication. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:14425-14430.
67. Sui J., Rotshtein P., Humphreys G.W. Coupling social attention to the self forms a network for personal significance. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:7607-7612.
68. Tognoli E., Lagarde J., DeGuzman G.C., Kelso J.A. The phi complex as a neuromarker of human social coordination. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:8190-8195.
69. Verhagen L., Dijkerman H.C., Medendorp W.P., Toni I. Cortical dynamics of sensorimotor integration during grasp planning. J. Neurosci. 2012, 32:4508-4519.
70. Verhagen L., Dijkerman H.C., Medendorp W.P., Toni I. Hierarchical organization of parietofrontal circuits during goal-directed action. J. Neurosci. 2013, 33:6492-6503.
71. Vesper C., RP van der Wel, Knoblich G., Sebanz N. Are you ready to jump? Predictive mechanisms in interpersonal coordination. J. Exp. Psychol. Hum. Percept. Perform. 2013, 39:48-61.
72. Wallstrom G.L., Kass R.E., Miller A., Cohn J.F., Fox N.A. Automatic correction of ocular artifacts in the EEG: a comparison of regression-based and component-based methods. Int. J. Psychophysiol. 2004, 53:105-119.
73. Wing A.M., Endo S., Bradbury A., Vorberg D. Optimal feedback correction in string quartet synchronization. J. R. Soc. Interface 2014, 11:20131125.
74. Yun K., Watanabe K., Shimojo S. Interpersonal body and neural synchronization as a marker of implicit social interaction. Sci. Rep. 2012, 2:959.