EEG theta and Mu oscillations during perception of human and robot actions

Frontiers in Neurorobotics

Volumn 7, Issue NOV, 2013, Pages

  Urgen, Burcu A ^a,b   Plank, Markus ^c   Ishiguro, Hiroshi ^d,e   Poizner, Howard ^c,f   Saygin, Ayse P ^a,b,f  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^d OSAKA UNIVERSITY   (Japan)

^e Advanced Telecommunications Research   (Japan)

^f UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Action perception; EEG; Mirror neuron system; Mu rhythm; Social robotics; Theta rhythm

Indexed keywords

BIOLOGICAL PRODUCT;

ADULT; ARTICLE; COGNITION; ELECTROENCEPHALOGRAM; FEMALE; HUMAN; MALE; MEMORY; MIRROR NEURON; MOTION; MU OSCILLATION; NEUROSCIENCE; NEUROTRANSMISSION; NORMAL HUMAN; OSCILLATION; ROBOTICS; SENSORIMOTOR FUNCTION; SIMULATION; THETA RHYTHM;

EID: 84899682291     PISSN: None     EISSN: 16625218     Source Type: Journal    
DOI: 10.3389/fnbot.2013.00019     Document Type: Article

References (91)

1. Arnstein, D., Cui, F., Keysers, C., Maurits, N. M., and Gazzola, V. (2011). Mu suppression during action observation and execution correlates with BOLD in dorsal premotor, inferior parietal, and SI cortices. J. Neurosci. 31, 14243-14249. doi: 10.1523/JNEUROSCI.0963-11.2011
2. Atienza, M., Crespo-Garcia, M., and Cantero, J. L. (2011). Semantic congruence enhances memory of episodic associations: role of theta oscillations. J. Cogn. Neurosci. 23, 75-90. doi: 10.1162/jocn.2009.21358
3. Babiloni, C., Babiloni, F., Carducci, F., Cincotti, F., Cocozza, G., Del Percio, C., et al. (2002). Human cortical electroencephalography (EEG) rhythms during the observation of simple aimless movements: a high-resolution EEG study. Neuroimage 17, 559-572. doi: 10.1006/nimg.2002.1192
4. Barresi, J., and Moore, C. (1996). Intentional relations and social understanding. Behav. Brain Sci. 19, 107-154. doi: 10.1017/S0140525X00041790
5. Bastiaansen, M. C. M., Oostenveld, R., Jensen, O., and Hagoort, P. (2008). I see what you mean: theta power increases are involved in the retrieval of lexical semantic information. Brain Lang. 106, 15-28. doi: 10.1016/j.bandl.2007.10.006
6. Billard, A., Robins, B. Nadel, J., and Dautenhahn, K. (2007). Building Robota, a mini-humanoid robot for the rehabilitation of children with autism. Assist. Technol. 19, 37-49. doi: 10.1080/10400435.2007.10131864
7. Blakemore, S. J., and Decety, J. (2001). From the perception of action to the understanding of intention. Nat. Rev. Neurosci. 2, 561-566. doi: 10.1038/35086023
8. Braadbaart, L., Williams, J. H., and Waiter, G. D. (2013). Do mirror neuron areas mediate mu rhythm suppression during imitation and action observation? Int. J. Psychophysiol. 89, 99-105. doi: 10.1016/j.ijpsycho.2013.05.019
9. Buccino, G., Lui, F., Canessa, N., Patteri, I., Lagravinese, G., Benuzzi, F., et al. (2004). Neural circuits involved in the recognition of actions performed by nonconspecifics: an FMRI study. J. Cogn. Neurosci. 16, 114-126. doi: 10.1162/089892904322755601
10. Calvo-Merino, B., Grezes, J., Glaser, D. E., Passingham, R. E., and Haggard, P. (2006). Seeing or doing? Influence of visual and motor familiarity in action observation. Curr. Biol. 16, 1905-1910. doi: 10.1016/j.cub.2006.07.065
11. Carmo, J. C., Rumiati, R. I., and Vallesi, A. (2012). Understanding and imitating unfamiliar actions: distinct underlying mechanisms. PLoS ONE 7:e46939. doi: 10.1371/journal.pone.0046939
12. Casile, A., and Giese, M. A. (2006). Nonvisual motor training influences biological motion perception. Curr. Biol. 16, 69-74. doi: 10.1016/j.cub.2005.10.071
13. Casile, A., Dayan, E., Caggiano, V., Hendler, T., Flash, T., and Giese, M. A. (2010). Neuronal encoding of human kinematic invariants during action observation. Cereb. Cortex 20, 1647-1655. doi: 10.1093/cercor/bhp229
14. Cattaneo, L., Sandrini, M., and Schwarzbach, J. (2010). State-dependent TMS reveals a hierarchical representation of observed acts in the temporal, parietal, and premotor cortices. Cereb. Cortex 20, 2252-2258. doi: 10.1093/cercor/bhp291
15. Chaminade, T., and Hodgins, J. K. (2006). Artificial agents in social cognitive sciences. Interact. Stud. 7, 347-353. doi: 10.1075/is.7.3.07cha
16. Chaminade, T., Hodgins, J., and Kawato, M. (2007). Anthropomorphism influences perception of computer-animated characters' actions. Soc. Cogn. Affect. Neurosci. 2, 206-216. doi: 10.1093/scan/nsm017
17. Chang, C., and Lin, C. (2011). LIBSVM: a library for support vector machines. ACM Trans. Intell. Syst. Technol. 2, 27:1-27:27. doi: 10.1145/1961189.1961199
18. Cheetham, M., Suter, P., and Jancke L. (2011). The human likeness dimension of the "uncanny valley hypothesis": behavioral and functional MRI findings. Front. Hum. Neurosci. 5:126. doi: 10.3389/fnhum.2011.00126
19. Cochin, S., Barthelemy, C., Roux, S., and Martineau, J. (1999). Observation and execution of movement: similarities demonstrated by quantified electroencephalography. Eur. J. Neurosci. 11, 1839-1842. doi: 10.1046/j.1460-9568.1999.00598.x
20. Cook, R., Bird, G., Catmur, C., Press, C., and Heyes, C. (in press). Mirror neurons: from origin to function. Behav. Brain Sci.
21. Coradeschi, S., Ishiguro, H., Asada, M., Shapiro, S. C., Thielscher, M., Breazeal, C., et al. (2006). Human-inspired robots. IEEE Intell. Syst. 21, 74-85. doi: 10.1109/MIS.2006.72
22. Cortes, C., and Vapnik, V. N. (1995). Support-vector networks. Mach. Learn. 20, 273-297. doi: 10.1007/BF00994018
23. Crespo-Garcia, M., Cantero, J. L., Pomyalov, A., Boccaletti, S., and Atienza, M. (2010). Functional neural networks underlying semantic encoding of associative memories. Neuroimage 50, 1258-1270. doi: 10.1016/j.neuroimage.2010.01.018
24. Cross, E., Liepelt, R., Hamilton, A., Parkinson, J., Remsey, R., Stadler, W., et al. (2012). Robotic movement preferentially engages the action observation network. Hum. Brain Mapp. 33, 2238-2254. doi: 10.1002/hbm.21361
25. Dautenhahn, K. (2007). Socially intelligent robots: dimensions of human-robot interaction. Philos. Trans. R. Soc. Lond. B Biol. Sci. 362, 679-704. doi: 10.1098/rstb.2006.2004
26. Davidson, D. J., and Indefrey, P. (2007). An inverse relation between event-related and time-frequency violation responses in sentence processing. Brain Res. 1158, 81-92. doi: 10.1016/j.brainres.2007.04.082
27. Delorme, A., and Makeig, S. (2004). EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J. Neurosci. Methods 134, 9-21. doi: 10.1016/j.jneumeth.2003.10.009
28. Di Pellegrino, G., Fadiga, L., Fogassi, L., Gallese, V., Rizzolatti, G. (1992). Understanding motor events: a neurophysiological study. Exp. Brain Res. 91, 176-180. doi: 10.1007/BF00230027
29. Dumas, G., Martinerie, J., Soussignan, R., and Nadel, J. (2012). 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
30. Fadiga, L., Fogassi, L., Pavesi, G., and Rizzolatti, G. (1995). Motor facilitation during action observation: a magnetic stimulation study. J. Neurophysiol. 73, 2608-2611.
31. Gallese, V., Fadiga, L., Fogassi, L., and Rizzolatti, G. (1996). Action recognition in the premotor cortex. Brain 119, 593-609. doi: 10.1093/brain/119.2.593
32. Gazzola, V., Rizzolatti, G., Wicker, B., and Keysers, C. (2007). The anthropomorphic brain: the mirror neuron system responds to human and robotic actions. Neuroimage 35, 1674-1684. doi: 10.1016/j.neuroimage.2007.02.003
33. Grafton, S. T., and Hamilton, A. F. (2007). Evidence for a distributed hierarchy of action representation in the brain. Hum. Mov. Sci. 26, 590-616. doi: 10.1016/j.humov.2007.05.009
34. Hald, L. A., Bastiaansen, M. C. M., and Hagoort, P. (2006). EEG theta and gamma responses to semantic violations in online sentence processing. Brain Lang. 96, 90-105. doi: 10.1016/j.bandl.2005.06.007
35. Hari, R. (2006). Action-perception connection and the cortical mu rhythm. Prog. Brain Res. 159, 253-260. doi: 10.1016/S0079-6123(06)59017-X
36. Hari, R., Forss, N., Avikainen, S., Kirveskari, E., Salenius, S., and Rizzolatti, G. (1998). Activation of human primary motor cortex during action observation: a neuromagnetic study. Proc. Natl. Acad. Sci. U.S.A. 95, 15061-15065. doi: 10.1073/pnas.95.25.15061
37. Haynes, J. D., and Rees, G. (2006). Decoding mental states from brain activity in humans. Nat. Rev. Neurosci. 7, 523-534. doi: 10.1038/nrn1931
38. Ho, C.-C., MacDorman, K. F., and Dwi Pramono, Z. A. D. (2008). "Human emotion and the uncanny valley: a GLM, MDS, and Isomap analysis of robot video ratings," in Proceedings of the 3rd ACM/IEEE International Conference on Human Robot Interaction (Amsterdam: Association for Computing Machinery).
39. Iacoboni, M., and Dapretto, M. (2006). The mirror neuron system and the consequences of its dysfunction. Nat. Rev. Neurosci. 7, 942-951. doi: 10.1038/nrn2024
40. Ishiguro, H. (2006). Android science: conscious and subconscious recognition. Conn. Sci. 18, 319-332. doi: 10.1080/09540090600873953
41. Kahana, M. J., Seelig, D., and Madsen, J. R. (2001). Theta returns. Curr. Opin. Neurobiol. 11, 739-744. doi: 10.1016/S0959-4388(01)00278-1
42. Kamitani, Y., and Tong, F. (2005). Decoding the visual and subjective contents of the human brain. Nat. Neurosci. 8, 679-685. doi: 10.1038/nn1444
43. Kanda, T., Ishiguro, H., Imai, M., and Ono, T. (2004). Development and evaluation of interactive humanoid robots. Proc. IEEE 92, 1839-1850. doi: 10.1109/JPROC.2004.835359
44. Kilner, J. M., Marchant, J. L., and Frith, C. D. (2009). Relationship between activity in human primary motor cortex during action observation and the mirror neuron system. PLoS ONE 4:e4925. doi: 10.1371/journal.pone.0004925
45. Kilner, J. M., Paulignan, Y., and Blakemore, S. J. (2003). An interference effect of observed biological movement on action. Curr. Biol. 13, 522-525. doi: 10.1016/S0960-9822(03)00165-9
46. Klimesch, W., Freunberger, R., and Sauseng, P. (2010). Oscillatory mechanisms of process binding in memory. Neurosci. Biobehav. Rev. 34, 1002-1014. doi: 10.1016/j.neubiorev.2009.10.004
47. Knoblich, G., Thornton, I. M., Grosjean, M., Shiffrar, M., eds. (2006). Human Body Perception from the Inside Out. New York: Oxford University Press.
48. Kutas, M., and Federmeier, K. D. (2011). Thirty Years and Counting: Finding Meaning in the N400 Component of the Event-Related Brain Potential (ERP). Annu. Rev. Psychol. 62, 621-647. doi: 10.1146/annurev.psych.093008.131123
49. Lewkowicz, D. J., and Ghazanfar, A. A. (2012). The development of the uncanny valley in infants. Dev. Psychobiol. 54, 124-132. doi: 10.1002/dev.20583
50. MacDorman, K. F., and Ishiguro, H. (2006). The uncanny advantage of using androids in cognitive and social science research. Interact. Stud. 7, 297-337. doi: 10.1075/is.7.3.03mac
51. MacDorman, K. F., Vasudevan, S. K., and Ho, C.-C. (2009). Does Japan really have robot mania? Comparing attitudes by implicit and explicit measures. AI Soc. 23, 485-510. doi: 10.1007/s00146-008-0181-2
52. Mataric, M., Tapus, A., Winstein, C., and Eriksson, J. (2009). Socially assistive robotics for stroke and mild TBI rehabilitation. Stud. Health Technol. Inform. 145, 249-262.
53. Mizuhara, H., and Inui, T. (2011). "Is mu rhythm an index of the human mirror neuron system? A study of simultaneous fMRI and EEG," in Advances in Cognitive Neurodynamics (II) (Berlin: Springer), 123-127.
54. Mori, M. (1970). The uncanny valley. Energy 7, 33-35. doi: 10.1109/MRA.2012.2192811
55. Muller-Putz, G. R., Scherer, R., Brunner, C., Leeb, R., and Pfurtscheller, G. (2008). Better than random: A closer look on BCI results. Int. J. Biomagn. 10, 52-55.
56. Naeem, M., Prasad, G., Watson, D. R., and Kelso, J. A. (2012). Electrophysiological signatures of intentional social coordination in the 10-12Hz range. Neuroimage 59, 1795-1803. doi: 10.1016/j.neuroimage.2011.08.010
57. Norman, K. A., Polyn, S. M., Detre, G. J., and Haxby, J. V. (2006). Beyond mind-reading: multi-voxel pattern analysis of fMRI data. Trends Cogn. Sci. 10, 424-430. doi: 10.1016/j.tics.2006.07.005
58. Oberman, L. M., McCleery, J. P., Ramachandran, V. S., and Pineda, J. A. (2007). EEG evidence for mirror neuron activity during the observation of human and robot actions: Toward an analysis of the human qualities of interactive robots. Neurocomputing 70, 2194-2203. doi: 10.1016/j.neucom.2006.02.024
59. Orgs, G., Dombrowski, J., Heil, M., and Jansen-Osmann, P. (2008). Expertise in dance modulates alpha/beta event-related desynchronization during action observation. Eur. J. Neurosci. 27, 3380-3384. doi: 10.1111/j.1460-9568.2008.06271.x
60. Osipova, D., Takashima, A., Oostenveld, R., Fernández, G., Maris, E., and Jensen, O. (2006). Theta and gamma oscillations predict encoding and retrieval of declarative memory. J. Neurosci. 26, 7523-7531. doi: 10.1523/JNEUROSCI.1948-06.2006
61. Pelphrey, K. A., Mitchell, T. V., McKeown, M. J., Goldstein, J., Allison, T., and McCarthy, G. (2003). Brain activity evoked by the perception of human walking: controlling for meaningful coherent motion. J. Neurosci. 23, 6819-25.
62. Pereira, F., Mitchell, T., and Botvinick, M. (2009). Machine learning classifiers and fMRI: A tutorial overview. Neuroimage 45, 199-209. doi: 10.1016/j.neuroimage.2008.11.007
63. Perry, A., and Bentin, S (2009). Mirror activity in the human brain while observing hand movements: a comparison between EEG desynchronization in the mu-range and previous fMRI results. Brain Res. 1282, 126-132. doi: 10.1016/j.brainres.2009.05.059
64. Pineda, J. (2005). The functional significance of mu rhythms: Translating "seeing" and "hearing" into "doing." Brain Res. Rev. 50, 57-68. doi: 10.1016/j.brainresrev.2005.04.005
65. Press, C., Cook, J., Blakemore, S. J., and Kilner, J. M. (2011). Dynamic modulation of human motor activity when observing actions. J. Neurosci. 31, 2792-2800. doi: 10.1523/JNEUROSCI.1595-10.2011
66. Press, C., Gillmeister, H., and Heyes, C. (2007). Sensorimotor experience enhances automatic imitation of robotic action. Proc. Biol. Sci. 274, 2509-2514. doi: 10.1098/rspb.2007.0774
67. Rizzolatti, G., Fadiga, L., Gallese, V., and Fogassi, L. (1996). Premotor cortex and the recognition of motor actions. Brain Res. Cogn. Brain Res. 3, 131-141. doi: 10.1016/0926-6410(95)00038-0
68. Rizzolatti, G., Fogassi, L., and Gallese, V. (2001). Neurophysiological mechanisms underlying the understanding and imitation of action. Nat. Rev. Neurosci. 2, 661-670. doi: 10.1038/35090060
69. Saygin, A. P. (2007). Superior temporal and premotor areas are necessary for biological motion perception. Brain 130, 2452-2461. doi: 10.1093/brain/awm162
70. Saygin, A. P., Chaminade, T., Ishiguro, H., Driver, J., and Frith, C. (2012). The thing that should not be: predictive coding and the uncanny valley in perceiving human and humanoid robot actions. Soc. Cogn. Affect. Neurosci. 7, 413-422. doi: 10.1093/scan/nsr025
71. Saygin, A. P., Chaminade, T., Urgen, B. A., and Ishiguro, H. (2011). "Cognitive neuroscience and robotics: a mutually beneficial joining of forces," in Robotics: Systems and Science, ed. L. Takayama (Los Angeles: MIT Press).
72. Saygin, A. P., and Cicekli, I. (2002). Pragmatics in human-computer conversations. J. Pragmat. 34, 227-258. doi: 10.1016/S0378-2166(02)80001-7
73. Saygin, A. P., and Stadler, W. (2012). The role of appearance and motion in action prediction. Psychol. Res. 76, 388-394. doi: 10.1007/s00426-012-0426-z
74. Saygin, A. P., Wilson, S. M., Hagler, D. J. Jr., Bates, E., and Sereno, M. I. (2004). Point-light biological motion perception activates human premotor cortex. J. Neurosci. 24, 6181-6188. doi: 10.1523/JNEUROSCI.0504-04.2004
75. Shahin, A. J., Picton, T. W., and Miller, L. M. (2009). Brain oscillations during semantic evaluation of speech. Brain Cogn. 70, 259-66. doi: 10.1016/j.bandc.2009.02.008
76. Silas, J., Levy, J. P., and Holmes, A. (2012). Sensitivity of 'mu' rhythm modulation to the relevance of an observed movement but not to goal congruency. Int. J. Psychophysiol. 85, 168-173. doi: 10.1016/j.ijpsycho.2012.05.008
77. Sitnikova, T., Holcomb, P. J., Kiyonaga, K. A., and Kuperberg, G. R. (2008). Two neurocognitive mechanisms of semantic integration during the comprehension of visual real-world events. J. Cogn. Neurosci. 20, 2037-2057. doi: 10.1162/jocn.2008.20143
78. Steckenfinger, S. A., and Ghazanfar, A. A. (2009). Monkey visual behavior falls into the uncanny valley. Proc. Natl. Acad. Sci. U.S.A. 106, 18362-18366. doi: 10.1073/pnas.0910063106
79. Steele, V. R., Bernat, E. M., van den Broek, P., Collins, P., Patrick, C. J., and Marsolek, C. J. (2013). Separable processes before, during, and after the N400 elicited by previously inferred and new information: Evidence from time-frequency decompositions. Brain Res. 1492, 92-107. doi: 10.1016/j.brainres.2012.11.016
80. Stefan, K., Cohen, L. G., Duque, J., Mazzocchio, R., Celnik, P., Sawaki, L., et al. (2005). Formation of a motor memory by action observation. J. Neurosci. 25, 9339-46. doi: 10.1523/JNEUROSCI.2282-05.2005
81. Tai, Y. F., Scherfler, C., Brooks, D. J., Sawamoto, N., and Castiello, U. (2004). The human premotor cortex is 'mirror' only for biological actions. Curr. Biol. 14, 117-120. doi: 10.1016/j.cub.2004.01.005
82. Thompson, J. C., Trafton, J. G., and McKnight, P. (2011). The perception of humanness from the movements of synthetic agents. Perception 40, 695-704. doi: 10.1068/p6900
83. Tinwell, A., Grimshaw, M., Abdel-Nabi, D., and Williams, A. (2011). Facial expression of emotion and perception of the uncanny valley in virtual characters. Comput. Hum. Behav. 27, 741-749. doi: 10.1016/j.chb.2010.10.018
84. Tognoli, E., Lagarde, J., DeGuzman, G. C., and Kelso, J. S. (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
85. Ugur, E., and Erol, S. (2011). "Unsupervised learning of object affordances for planning in a mobile manipulation platform," in Robotics and Automation (ICRA) IEEE International Conference, Shanghai.
86. Umiltà, M. A., Kohler, E., Gallese, V., Fogassi, L., Fadiga, L., Keysers, C., et al. (2001). I know what you are doing: a neurophysiological study. Neuron 31, 155-165. doi: 10.1016/S0896-6273(01)00337-3
87. Urgen, B. A., Plank, M., Ishiguro, H., Poizner, H., and Saygin, A. P. (2012). "Temporal dynamics of action perception: the role of biological appearance and motion kinematics," in 34thAnnual Conference of Cognitive Science Society, Sapporo.
88. van Kemenade, B. M., Muggleton, N., Walsh, V., and Saygin, A. P. (2012). Effects of TMS over premotor and superior temporal cortices on biological motion perception. J. Cogn. Neurosci. 24, 896-904. doi: 10.1162/jocn_a_00194
89. Wermter, S., and Elshaw, M. (2003). Learning robot actions based on self-organising language memory. Neural Netw. 16, 691-699. doi: 10.1016/S0893-6080(03)00100-X
90. Wu, Y. C., and Coulson, S. (2011). Are depictive gestures like pictures? Commonalities and differences in semantic processing. Brain Lang. 119, 184-195. doi: 10.1016/j.bandl.2011.07.002
91. Zion-Golumbic, E., Kutas, M., and Bentin, S. (2010). Neural dynamics associated with semantic and episodic memory for faces: evidence from multiple frequency bands. J. Cogn. Neurosci. 22, 263-277. doi: 10.1162/jocn.2009.21251