On the interpretation of synchronization in EEG hyperscanning studies: A cautionary note

Frontiers in Human Neuroscience

Volumn 7, Issue DEC, 2013, Pages

  Burgess, Adrian P ^a  

^a ASTON UNIVERSITY   (United Kingdom)

Author keywords

Electroencephalography; Hyperscanning; Inter brain connectivity; Phase locking value; Phase synchronization; Social neuroscience

Indexed keywords

ADULT; ARTICLE; BRAIN DEPTH STIMULATION; COGNITIVE BIAS; CONNECTOME; CORRELATION COEFFICIENT; ELECTROENCEPHALOGRAPHY PHASE SYNCHRONIZATION; EVENT RELATED POTENTIAL; FEMALE; HUMAN; HUMAN EXPERIMENT; HYPERCONNECTIVITY ANALYSIS; KRASKOV MUTUAL INFORMATION; MALE; MOVEMENT PERCEPTION; NERVOUS SYSTEM PARAMETERS; NORMAL HUMAN; PARTIAL DIRECTED COHERENCE; PHASE LOCKING VALUE; RESTING STATE NETWORK; SENSE OF COHERENCE;

EID: 84891639852     PISSN: 16625161     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnhum.2013.00881     Document Type: Article

References (61)

1. Astolfi, L., Cincotti, F., Mattia, D., De Vico Fallani, F., Salinari, S., Marciani, M. G., et al.(2009). Estimation of the cortical activity from simultaneous multi-subject recordings during the prisoner's dilemma. Conf. Proc. IEEE Eng. Med. Biol. Soc. 2009, 1937-1939. doi: 10.1109/IEMBS.2009.5333456
2. Astolfi, L., Cincotti, F., Mattia, D., De Vico Fallani, F., Salinari, S., Vecchiato, G., et al. (2010a). Simultaneous estimation of cortical activity during social interactions by using EEG hyperscannings. Conf. Proc. IEEE Eng. Med. Biol. Soc. 2010, 2814-2817. doi: 10.1109/IEMBS.2010.5626555
3. Astolfi, L., Cincotti, F., Mattia, D., Fallani, F. D. V., Salinari, S., Vecchiato, G., et al. (2010b). Imaging the social brain: multi-subjects EEG recordings during the "Chicken's game" Conf. Proc. IEEE Eng. Med. Bhl Soc. 1734-1737. doi: 10.1109/IEMBS.2010.5626708
4. Astolfi, L., Toppi, J., De Vico Fallani, F., Vecchiato, G., Salinari, S., Mattia, D., et al. (2010c). Neuroelectrical hyperscanning measures simultaneous brain activity in humans. Brain Topogr. 23, 243-256. doi: 10.1007/s10548-010- 0147-9
5. Astolfi, L., Toppi, J., Borghini, G., Vecchiato, G., He, E. J., Roy, A., et al. (2012). Cortical activity and functional hyperconnectivity by simultaneous EEG recordings from interacting couples of professional pilots. Conf. Proc. IEEE Eng. Med. Biol. Soc. 2012, 4752-4755. doi: 10.1109/EMBC.2012.6347029
6. Astolfi, L., Toppi, J., Borghini, G., Vecchiato, G., Isabella, R., De Vico Fallani, F et al. (2011a). Study of the functional hyperconnectivity between couples of pilots during flight simulation: an EEG hyperscanning study. Conf. Proc. IEEE Eng. Med. Biol. Soc. 2011, 2338-2341. doi: 10.1109/IEMBS.2011.6090654
7. Astolfi, L., Toppi, J., De Vico Fallani, F., Vecchiato, G., Cincotti, F., Wilke, C. T., et al. (2011b). Imaging the social brain by simultaneous hyperscanning during subject interaction. IEEE Intell. Syst. 26, 38-45. doi: 10.1109/MIS.2011.61
8. Babiloni, C., Buffo, P., Vecchio, F., Marzano, N., Del Percio, C., Spada, D., et al. (2012). Brains "in concert": frontal oscillatory alpha rhythms and empathy in professional musicians. Neuroimage 60, 105-116. doi: 10.1016/j.neuroimage. 2011.12.008
9. Babiloni, C., Vecchio, F., Infarinato, F., Buffo, P., Marzano, N., Spada, D., et al. (2011). Simultaneous recording of electroencephalographic data in musicians playing in ensemble. Cortex 47, 1082-1090. doi: 10.1016/j.cortex.2011.05.006
10. Babiloni, F., and Astolfi, L. (2012). Social neuroscience and hyperscanning techniques: past, present and future. Neurosci. Biobehav. Rev. doi: 10.1016/j.neubiorev.2012.07.006. [Epub ahead of print].
11. Babiloni, F., Astolfi, L., Cincotti, F., Mattia, D., Tocci, A., Tarantino, A., et al. (2007a). Cortical activity and connectivity ofhuman brain during the prisoner's dilemma: an EEG hyperscanning study. Conf. Proc. IEEE Eng. Med. Biol. Soc. 2007, 4953-4956. doi: 10.1109/IEMBS.2007.4353452
12. Babiloni, F., Cincotti, F., Mattia, D., De Vico Fallani, F., Tocci, A., Bianchi, L., et al. (2007b). High resolution EEG hyperscanning during a card game. Conf. Proc. IEEE Eng. Med. Biol. Soc. 2007, 4957-4960. doi: 10.1109/IEMBS.2007.4353453
13. Babiloni, F., Cincotti, F., Mattia, D., Mattiocco, M., De Vico Fallani, F., Tocci, A., et al. (2006). Hypermethods for EEG hyperscanning. Conf. Proc. IEEE Eng. Med. Biol. Soc.1,3666-3669. doi: 10.1109/IEMBS.2006.260754
14. Baccala, L. A., and Sameshima, K. (2001). Partial directed coherence: a new concept in neural structure determination. Biol. Cybern. 84, 463-474. doi: 10.1007/ PL00007990
15. Baess, P., Zhdanov, A., Mandel, A., Parkkonen, L., Hirvenkari, L., Makela, J. P., et al. (2012). MEG dual scanning: a procedure to study real-time auditory interaction between two persons. Front. Hum. Neurosci. 6:83. doi: 10.3389/fnhum.2012.00083
16. Beirlant, J., Dudewicz, E. J., Gyorfi, L., and van der Meulen, J. C. (1997). Nonparametric entropy estimation: an overview. Int. J. Math. Stat. Sci. 6,17-39.
17. Berens, P. (2009). CircStat: a MATLAB TOOLBOX for circular statistics. J. Stat Sojtw. 31,1-21. Avilable online at: http://www.jstatsoft.org/v31/i10
18. Burgess, A. P. (2012). Towards a unified understanding of event-related changes in the EEG: the firefly model of synchronization through cross-frequency phase modulation. PLoS ONE 7:e45630. doi: 10.1371/journal.pone.0045630
19. Burgess, A. P., and Gruzelier, J. H. (1997). Localization of word and face recognition memory using topographical EEG. Psychophysiology 34, 7-16. doi: 10.1111/j.1469-8986.1997.tb02410.x
20. Chung, D., Yun, K., and Jeong, J. (2008). "Neural substrates of free-riding and cooperation during the standard public goods game," in International Conference of Cognitive Science, (Seoul).
21. Dodel, S., Cohn, J., Mersmann, J., Luu, P., Forsythe, C., and Jirsa, V. (2011). "Brain signatures of team performance," in Foundations of Augmented Cognition: Directing the Future ofAdaptive Systems, Vol. 6780, eds D. D. Schmorrow and C. M. Fidopiastis (Orlando, FL: Springer), 288-297. doi: 10.1007/978-3-64221852-1-35
22. Dumas, G. (2011). Towards a two-body neuroscience. Commun. Integr. Biol. 4, 349-352. doi: 10.4161/cib.4.3.15110
23. Dumas, G., Chavez, M., Nadel, J., and Martinerie, J. (2012a). Anatomical connectivity influences both intra- and inter-brain synchronizations. PLoS ONE 7:e36414. doi: 10.1371/journal.pone.0036414
24. Dumas, G., Martinerie, J., Soussignan, R., and Nadel, J. (2012b). Does the brain know who is at the origin of what in an imitative interaction? Front. Hum. Neurosci. 6:128. doi: 10.3389/fnhum.2012.00128
25. Dumas, G., Lachat, F., Martinerie, J., Nadel, J., and George, N. (2011). From social behaviour to brain synchronization: review and perspectives in hyperscanning. IRBM 32, 48-53. doi: 10.1016/j.irbm.2011.01.002
26. Dumas, G., Nadel, J., Soussignan, R., Martinerie, J., and Garnero, L. (2010). Inter-brain synchronization during social interaction. PLoS ONE 5:e12166. doi: 10.1371/journal.pone.0012166.
27. Faes, L., and Nollo, G. (2011). "Multivariate frequency domain analysis of causal interactions in physiological time series," in Biomedical Engineering, Trends in Electronics, Communications and Software, ed A. N. Laskovski (Rijeka: InTech), 403-428.
28. Fallani, F. D., Nicosia, V., Sinatra, R., Astolfi, L., Cincotti, F., Mattia, D., et al. Defecting or not defecting: howto "read" human behavior duringcoop- erative games by EEG measurements. PLoS ONE 5:e14187. doi: 10.1371/jour- nal.pone.0014187
29. Flexer, A., and Makeig, S. (2007). Independent component analysis of EEG recorded during two-person game playing. Appl. Artif. Intell. 21,883-894. doi: 10.1080/08839510701527127
30. Friston, K. J. (2011). Functional and effective connectivity: a review. Brain Connect. 1,13-36. doi: 10.1089/brain.2011.0008
31. Funane, T., Kiguchi, M., Atsumori, H., Sato, H., Kubota, K., and Koizumi, H. Synchronous activity of two people's prefrontal cortices during a cooperative task measured by simultaneous near-infrared spectroscopy. J. Biomed. Opt.16, 077011. doi: 10.1117/1.3602853
32. Gentle, J. E.(1998). Random Number Generation and Monte Carlo Methods. New York, NY: Springer. doi: 10.1007/978-1-4757-2960-3
33. Hasson, U., Furman, O., Clark, D., Dudai, Y., and Davachi, L. (2008). Enhanced intersubject correlations during movie viewing correlate with successful episodic encoding. Neuron 57, 452-462. doi: 10.1016/j.neuron.2007.12.009
34. Hnizdo, V., Tan, J., Killian, B. J., and Gilson, M. K. (2008). Efficient calculation of configurational entropy from molecular simulations by combining the mutual- information expansion and nearest-neighbor methods. J. Comput. Chem. 29, 1605-1614. doi: 10.1002/jcc.20919
35. Holmes, A. P., Blair, R. C., Watson, J. D., and Ford, I. (1996). Nonparametric analysis of statistic images from functional mapping experiments. J. Cereb. Blood FlowMetab.16, 7-22. doi: 10.1097/00004647-199601000-00002
36. Jammalamadaka, S. R., and Sengupta, A. (2001). Topics in Circular Statistics. River Edge, NJ: World Scientific.
37. Kawasaki, M., Yamada, Y., Ushiku, Y., Miyauchi, E., and Yamaguchi, Y. (2013). Inter-brain synchronization during coordination of speech rhythm in human- to-human social interaction. Sci. Rep. 3:1692. doi: 10.1038/srep01692
38. Klarreich, E. (2002). Huygens's clocks revisited. Am. Sci. 90, 322-323. Available online at: http://www.americanscientist.org/issues/pub/huygenss-clocks-revisited
39. Konvalinka, I., and Roepstorff, A. (2012). The two-brain approach: how can mutually interacting brains teach us something about social interaction? Front. Hum. Neurosci. 6:215. doi: 10.3389/fnhum.2012.00215
40. Kozachenko, L. F., and Leonenko, N. N.(1987). Sample estimate of entropy of a random vector. Probl. Inf. Trans. 23, 95-101.
41. Kraskov, A., Stogbauer, H., and Grassberger, P. (2004). Estimating mutual information. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 69, 066138. doi: 10.1103/Phys RevE.69.066138
42. Lachat, F., Hugueville, L., Lemarechal, J. D., Conty, L., and George, N. (2012). Oscillatory brain correlates of live joint attention: a dual-EEG study. Front. Hum. Neurosci. 6:156. doi: 10.3389/fnhum.2012.00156
43. Lachaux, J. P., Rodriguez, E., Martinerie, J., andVarela, F. J. (1999). Measuring phase synchrony in brain signals. Hum. Brain Mapp. 8, 194-208.
44. Lindenberger, U., Li, S. C., Gruber, W., and Muller, V. (2009). Brains swinging in concert: cortical phase synchronization while playing guitar. BMC Neurosci. 10:22. doi: 10.1186/1471-2202-10-22
45. Maris, E., Schoffelen, J. M., and Fries, P. (2007). Nonparametric statistical testing of coherence differences. J. Neurosci. Methods 163, 161-175. doi: 10.1016/j.jneu meth.2007.02.011
46. Montague, P. R., Berns, G. S., Cohen, J. D., McClure, S. M., Pagnoni, G., Dhamala, M., et al. (2002). Hyperscanning: simultaneous fMRI during linked social interactions. Neuroimage 16, 1159-1164. doi: 10.1006/nimg.2002.1150
47. Naeem, M., Prasad, G., Watson, D. R., and Kelso, J. A. (2012a). Electrophysiological signatures of intentional social coordination in the 10-12 Hz range. Neuroimage 59,1795-1803. doi: 10.1016/j.neuroimage.2011.08.010
48. Naeem, M., Prasad, G., Watson, D. R., and Kelso, J. A. (2012b). Functional dissociation of brain rhythms in social coordination. Clin. Neurophysiol. 123, 1789-1797. doi: 10.1016/j.clinph.2012.02.065
49. Pikovsky, A., Rosenblum, M., and Kurths, J. (2001). Synchronization: A Universal Concept in Nonlinear Sciences. Cambridge: Cambridge University Press. doi: 10.1017/CBO9780511755743
50. Sanger, J., Lindenberger, U., and Muller, V. (2011). Interactive brains, social minds. Commun. Integr. Biol. 4, 655-663. doi: 10.4161/cib.4.6.17934
51. Sanger, J., Muller, V., and Lindenberger, U. (2012). Intra- and interbrain synchronization and network properties when playing guitar in duets. Front. Hum. Neurosci. 6:312. doi: 10.3389/fnhum.2012.00312
52. Sanger, J., Muller, V., and Lindenberger, U. (2013). Directionality in hyperbrain networks discriminates between leaders and followers in guitar duets. Front. Hum. Neurosci. 7:234. doi: 10.3389/fnhum.2013.00234
53. Singh, H., Hnizdo, V., and Demchuk, E. (2002). Probabilistic model for two dependent circular variables. Biometrika 89, 719-723. doi: 10.1093/biomet/89. 3.719
54. Tass, P., Rosenblum, M. G., Weule, J., Kurths, J., Pikovsky, A., Volkmann, J., et al. (1998). Detection of n: m phase locking from noisy data: application to mag- netoencephalography. Phys. Rev. Lett. 81,3291-3294. doi: 10.1103/PhysRevLett. 81.3291
55. Tognoli, E. (2008). "EEG coordination dynamics: neuromarkers of social coordination," in Coordination: Neural, Behavioral and Social Dynamics, eds A. Fuchs and V. K. Jirsa (Boca Raton, FL: Springer), 309-323. doi: 10.1007/978-3-54074479-5-15
56. Tognoli, E., Kovacs, A. J., Suutari, B., Afergan, D., Coyne, J., Gibson, G., et al. (2011a). "Behavioral and brain dynamics of team coordination part I: task design," in Foundations of Augmented Cognition: Directing the Future of Adaptive Systems, Vol. 6780, eds D. D. Schmorrow and C. M. Fidopiastis (Orlando, FL: Springer), 257-264. doi: 10.1007/978-3-64221852-1-32
57. Tognoli, E., Kovacs, A. J., Suutari, B., Afergan, D., Coyne, J., Gibson, G., et al. (2011b). "Behavioral and brain dynamics of team coordination part II: neu- robehavioral performance," in Foundations of Augmented Cognition: Directing the Future of Adaptive Systems, Vol. 6780, eds D. D. Schmorrow and C. M. Fidopiastis (Orlando, FL: Springer), 376-382. doi: 10.1007/978-3-64221852-1-44
58. Tognoli, E., Lagarde, J., Deguzman, G. C., and Kelso, J. A. (2007). The phi complex as a neuromarker of human social coordination. Proc. Natl. Acad. Sci. U.S.A. 104, 8190-8195. doi: 10.1073/pnas.0611453104
59. Vinck, M., Battaglia, F. P., Womelsdorf, T., and Pennartz, C. (2012). Improved measures of phase-coupling between spikes and the local field potential. J. Comput. Neurosci. 33, 53-75. doi: 10.1007/s10827-011-0374-4
60. Yun, K., Chung, D., and Jeong, J. (2008). "Emotional interactions in human decision making using EEG hyperscanning, in International Conference of Cognitive Science. (Seoul).
61. Yun, K., Watanabe, K., and Shimojo, S. (2012). Interpersonal body and neural synchronization as a marker of implicit social interaction. Sci. Rep. 2, 959. doi: 10.1038/srep00959