Brain response to a humanoid robot in areas implicated in the perception of human emotional gestures

PLoS ONE

Volumn 5, Issue 7, 2010, Pages

  Chaminade, Thierry ^a,b   Zecca, Massimiliano ^c,d   Blakemore, Sarah Jayne ^e   Takanishi, Atsuo ^c,d   Frith, Chris D ^a,f   Micera, Silvestro ^d,g,h   Dario, Paolo ^d,g   Rizzolatti, Giacomo ^i,j   Gallese, Vittorio ^i,j   Umiltà, Maria Alessandra ^i,j  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b AIX MARSEILLE UNIVERSITY   (France)

^c WASEDA UNIVERSITY   (Japan)

^d Italy Japan Joint Laboratory on Humanoid and Personal Robotics RoboCasa   (Japan)

^e UNIVERSITY COLLEGE LONDON   (United Kingdom)

^f AARHUS UNIVERSITY HOSPITAL   (Denmark)

^g SCUOLA SUPERIORE SANT ANNA   (Italy)

^h ETH ZURICH   (Switzerland)

ⁱ UNIVERSITY OF PARMA   (Italy)

^j ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ANGER; ARTICLE; BRAIN FUNCTION; CINGULATE GYRUS; CONTROLLED STUDY; DISGUST; EMOTION; FACIAL EXPRESSION; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GESTURE; HAPPINESS; HUMAN; HUMAN EXPERIMENT; INSULA; MALE; MOTOR PERFORMANCE; NORMAL HUMAN; ORBITAL CORTEX; PERCEPTION; ROBOTICS; SPEECH PERCEPTION; VISUAL STIMULATION; BRAIN; CLINICAL TRIAL; CONTROLLED CLINICAL TRIAL; METHODOLOGY; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; RANDOMIZED CONTROLLED TRIAL;

ADULT; ANGER; BRAIN; EMOTIONS; FACIAL EXPRESSION; FEMALE; GESTURES; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; ROBOTICS; YOUNG ADULT;

EID: 77955402750     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0011577     Document Type: Article

References (87)

1. OECD (2004) Population statistics. Organisation for Economic Co-operation and Development. Available: http://www.oecd.org.
2. Goldstein RZ, Volkow ND, Wang GJ, Fowler JS, Rajaram S (2001) Addiction changes orbitofrontal gyrus function: involvement in response inhibition. Neuroreport 12: 2595-2599.
3. Kozima H, Nakagawa C, Yasuda Y (2007) Children-robot interaction: a pilot study in autism therapy. Prog Brain Res 164: 385-400.
4. Gates B (2007) A Robot in Every Home. Scientific American 1: 58-65.
5. DiSalvo C, Gemperle F, Forlizzi J, Kiesler S (2002) All robots are not created equal: the design and perception of humanoid robot heads. Proceedings of the conference on Designing interactive systems: processes, practices, methods, and techniques. Available: http://doi.acm.org/10.1145/778712.778756.
6. Wada K, Shibata T, Saito T, Sakamoto K, Tanie K Psychological and Social Effects of One Year Robot Assisted Activity on Elderly People at a Health Service Facility for the Aged. pp 2785-2790.
7. Fujita M (2004) On activating human communications with pet-type robot AIBO. Proceedings of the IEEE 92: 1804-1813.
8. Hirai K, Hirose M, Haikawa Y, Takenaka T (1998) The development of Honda humanoid robot. Leuven, Belgium. pp 1321-1326.
9. Kaneko K, Kanehiro F, Kajita S, Hirukawa H, Kawasaki T, et al. (2004) Humanoid robot HRP-2; 2004. pp 1083-1090.
10. Kokoro Company Ltd (2004) Actroid. Tokyo, Japan. Available: http://www.kokoro-dreams.co.jp/english/index.html.
11. Ishiguro H, Nishio S (2007) Building artificial humans for understanding humans. Journal of Artificial Organs 10: 133-142.
12. Itoh K, Miwa H, Matsumoto M, Zecca M, Takanobu H, et al. (2004) Various emotional expressions with emotion expression humanoid robot WE-4RII. pp 35-36.
13. Arbib MA, Fellous JM (2004) Emotions: from brain to robot. Trends Cogn Sci 8: 554-561.
14. Chaminade T (2006) Acquiring and probing self-other equivalencies - using artificial agents to study social cognition. Reading, UK.
15. Gallese V, Rochat M, Cossu G, Sinigaglia C (2009) Motor cognition and its role in the phylogeny and ontogeny of action understanding. Dev Psychol 45: 103-113.
16. Gallese V (2003) The manifold nature of interpersonal relations: the quest for a common mechanism. Philos Trans R Soc Lond B Biol Sci 358: 517-528.
17. James w (1890) Principles of Psychology. New York: Holt.
18. Gallese V, Fadiga L, Fogassi L, Rizzolatti G (1996) Action recognition in the premotor cortex. Brain 119(Pt 2): 593-609.
19. Rizzolatti G, Fadiga L, Gallese V, Fogassi L (1996) Premotor cortex and the recognition of motor actions. Cognitive Brain Research 3: 131-141.
20. Kohler E, Keysers C, Umiltà MA, Fogassi L, Gallese V, et al. (2002) Hearing sounds, understanding actions: action representation in mirror neurons. Science 297: 846-848.
21. Buccino G, Binkofski F, Fink GR, Fadiga L, Fogassi L, et al. (2001) Action observation activates premotor and parietal areas in a somatotopic manner: an fMRI study. European Journal of Neuroscience 13: 400-404.
22. Iacoboni M, Woods RP, Brass M, Bekkering H, Mazziotta JC, et al. (1999) Cortical mechanisms of human imitation. Science 286: 2526-2528.
23. Chaminade T, Decety J (2001) A common framework for perception and action: neuroimaging evidence. Behav Brain Sci 24: 879-882.
24. Rizzolatti G, Craighero L (2004) The mirror-neuron system. Annu Rev Neurosci 27: 169-192.
25. Blakemore SJ, Bristow D, Bird G, Frith C, Ward J (2005) Somatosensory activations during the observation of touch and a case of vision-touch synaesthesia. Brain 128: 1571-1583.
26. Keysers C, Wicker B, Gazzola V, Anton JL, Fogassi L, et al. (2004) A touching sight: SII/PV activation during the observation and experience of touch. Neuron 42: 335-346.
27. Ebisch SJ, Perrucci MG, Ferretti A, Del Gratta C, Romani GL, et al. (2008) The sense of touch: embodied simulation in a visuotactile mirroring mechanism for observed animate or inanimate touch. J Cogn Neurosci 20: 1611-1623.
28. Wicker B, Keysers C, Plailly J, Royet JP, Gallese V, et al. (2003) Both of us disgusted in My insula: the common neural basis of seeing and feeling disgust. Neuron 40: 655-664.
29. Rizzolatti G, Fogassi L, Gallese V (2006) Mirrors of the mind. Sci Am 295: 54-61.
30. Carr L, Iacoboni M, Dubeau M-C, Mazziotta JC, Lenzi GL (2003) Neural mechanisms of empathy in humans: A relay from neural systems for imitation to limbic areas. Proceedings of the National Academy of Sciences of the United States of America 100: 5497-5502.
31. Tai YF, Scherfler C, Brooks DJ, Sawamoto N, Castiello U (2004) The human premotor cortex is 'mirror' only for biological actions. Curr Biol 14: 117-120.
32. Gazzola V, Rizzolatti G, Wicker B, Keysers C (2007) The anthropomorphic brain: the mirror neuron system responds to human and robotic actions. Neuroimage 35: 1674-1684.
33. Chaminade T, Hodgins J, Kawato M (2007) Anthropomorphism influences perception of computer-animated characters' actions. Soc Cogn Affect Neurosci 2: 206-216.
34. Itoh K, Miwa H, Matsumoto M, Zecca M, Takanobu H, et al. (2005) Behavior model of humanoid robots based on operant conditioning. pp 220-225.
35. Ekman P, Friesen W (1978) Facial Action Coding System: A Technique for the Measurement of Facial Movement. Palo Alto, CA, USA: Consulting Psychologists Press, Inc.
36. Weiskopf N, Hutton C, Josephs O, Deichmann R (2006) Optimal EPI parameters for reduction of susceptibility-induced BOLD sensitivity losses: a whole-brain analysis at 3 T and 1.5 T. Neuroimage 33: 493-504.
37. Hutton C, Bork A, Josephs O, Deichmann R, Ashburner J, et al. (2002) Image distortion correction in fMRI: A quantitative evaluation. Neuroimage 16: 217-240.
38. Andersson JL, Hutton C, Ashburner J, Turner R, Friston K (2001) Modeling geometric deformations in EPI time series. Neuroimage 13: 903-919.
39. Friston KJ, Ashburner JT, Kiebel S, Nichols TE, Penny WD, eds. Statistical Parametric Mapping: The Analysis of Functional Brain Images. London, UK: Elsevier.
40. Friston KJ, Holmes AP, Worsley KJ, Poline JP, Frith CD, et al. (1994) Statistical parametric maps in functional imaging: a general linear approach. Hum Brain Mapp 2: 189-210.
41. Duvernoy HM (1999) The human brain: surface, blood supply, and threedimensional anatomy, 2nd edn, completely revised. Wien New York: Springer-Verlag.
42. Eickhoff SB, Stephan KE, Mohlberg H, Grefkes C, Fink GR, et al. (2005) A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. Neuroimage 25: 1325-1335.
43. Zecca M, Chaminade T, Umiltà MA, Itoh K, Saito M, et al. (2007) Emotional Expression Humanoid Robot WE-4RII - Evaluation of the perception of facial emotional expressions by using fMRI. May 10/12, 2007; Akita, Japan. pp 2A1-O10.
44. Caspers S, Eickhoff SB, Geyer S, Scheperjans F, Mohlberg H, et al. (2008) The human inferior parietal lobule in stereotaxic space. Brain Struct Funct 212: 481-495.
45. Malikovic A, Amunts K, Schleicher A, Mohlberg H, Eickhoff SB, et al. (2007) Cytoarchitectonic analysis of the human extrastriate cortex in the region of V5/ MT+: a probabilistic, stereotaxic map of area hOc5. Cereb Cortex 17: 562-574.
46. Puce A, Allison T, Asgari M, Gore JC, McCarthy G (1996) Differential sensitivity of human visual cortex to faces, letterstrings, and textures: a functional magnetic resonance imaging study. J Neurosci 16: 5205-5215.
47. Steeves JK, Culham JC, Duchaine BC, Pratesi CC, Valyear KF, et al. (2006) The fusiform face area is not sufficient for face recognition: evidence from a patient with dense prosopagnosia and no occipital face area. Neuropsychologia 44: 594-609.
48. Kanwisher N, McDermott J, Chun MM (1997) The Fusiform Face Area: A Module in Human Extrastriate Cortex Specialized for Face Perception. J Neurosci 17: 4302-4311.
49. Grossman ED, Blake R (2002) Brain Areas Active during Visual Perception of Biological Motion. Neuron 35: 1167-1175.
50. Barnikol UB, Amunts K, Dammers J, Mohlberg H, Fieseler T, et al. (2006) Pattern reversal visual evoked responses of V1/V2 and V5/MT as revealed by MEG combined with probabilistic cytoarchitectonic maps. Neuroimage 31: 86-108.
51. Amunts K, Schleicher A, Burgel U, Mohlberg H, Uylings HB, et al. (1999) Broca's region revisited: cytoarchitecture and intersubject variability. J Comp Neurol 412: 319-341.
52. Hagoort P (2005) On Broca, brain, and binding: a new framework. Trends Cogn Sci 9: 416-423.
53. Higuchi S, Chaminade T, Imamizu H, Kawato M (2009) Shared neural correlates for language and tool use in Broca's area. Neuroreport.
54. Frith CD, Frith U (2008) Implicit and explicit processes in social cognition. Neuron 60: 503-510.
55. Kanwisher N (2000) Domain specificity in face perception. Nat Neurosci 3: 759-763.
56. Buccino G, Lui F, Canessa N, Patteri I, Lagravinese G, et al. (2004) Neural circuits involved in the recognition of actions performed by nonconspecifics: an FMRI study. J Cogn Neurosci 16: 114-126.
57. Chao LL, Martin A, Haxby JV (1999) Are face-responsive regions selective only for faces? Neuroreport 10: 2945-2950.
58. Farah MJ, Wilson KD, Drain M, Tanaka JN (1998) What is "special" about face perception? Psychol Rev 105: 482-498.
59. Duchaine B, Yovel G (2008) Face Recognition. In: Basbaum AI, Kaneko A, Shepherd GM, Westheimer G, eds. The Senses: A Comprehensive Reference. San Diego: Academic Press. pp 329-358.
60. Pinker S (1997) How the mind works. New York: Norton. xii, 660 p.
61. Morton J, Johnson MH (1991) CONSPEC and CONLERN: a two-process theory of infant face recognition. Psychol Rev 98: 164-181.
62. Rhodes G, McLean IG (1990) Distinctiveness and expertise effects with homogeneous stimuli: towards a model of configural coding. Perception 19: 773-794.
63. Jovicich J, Peters R, Koch K, Chang L, Ernst T (2000) Human perception of faces and face cartoons: an fMRI study. Denver, CO.
64. Cohen L, Dehaene S, Vinckier F, Jobert A, Montavont A (2008) Reading normal and degraded words: contribution of the dorsal and ventral visual pathways. Neuroimage 40: 353-366.
65. Allison T, Puce A, McCarthy G (2000) Social perception from visual cues: Role of the STS region. Trends in Cognitive Sciences 4: 267-278.
66. Grossman E, Donnelly M, Price R, Pickens D, Morgan V, et al. (2000) Brain areas involved in perception of biological motion. J Cogn Neurosci 12: 711-720.
67. Castelli F, Happe F, Frith U, Frith C (2000) Movement and mind: a functional imaging study of perception and interpretation of complex intentional movement patterns. Neuroimage 12: 314-325.
68. Phan KL, Wager T, Taylor SF, Liberzon I (2002) Functional Neuroanatomy of Emotion: A Meta-Analysis of Emotion Activation Studies in PET and fMRI. Neuroimage 16: 331-348.
69. Phillips ML, Drevets WC, Rauch SL, Lane R (2003) Neurobiology of emotion perception I: The neural basis of normal emotion perception. Biol Psychiatry 54: 504-514.
70. Drevets WC, Gautier C, Price JC, Kupfer DJ, Kinahan PE, et al. (2001) Amphetamine-induced dopamine release in human ventral striatum correlates with euphoria. Biol Psychiatry 49: 81-96.
71. Blair RJ, Cipolotti L (2000) Impaired social response reversal. A case of 'acquired sociopathy'. Brain 123(Pt 6): 1122-1141.
72. Blair RJ, Morris JS, Frith CD, Perrett DI, Dolan RJ (1999) Dissociable neural responses to facial expressions of sadness and anger. Brain 122(Pt 5): 883-893.
73. Wright P, Albarracin D, Brown RD, Li H, He G, et al. (2008) Dissociated responses in the amygdala and orbitofrontal cortex to bottom-up and top-down components of emotional evaluation. Neuroimage 39: 894-902.
74. Anderson SW, Bechara A, Damasio H, Tranel D, Damasio AR (1999) Impairment of social and moral behavior related to early damage in human prefrontal cortex. Nat Neurosci 2: 1032-1037.
75. Epley N, Waytz A, Cacioppo JT (2007) On seeing human: a three-factor theory of anthropomorphism. Psychol Rev 114: 864-886.
76. Santi A, Servos P, Vatikiotis-Bateson E, Kuratate T, Munhall K (2003) Perceiving biological motion: dissociating visible speech from walking. J Cogn Neurosci 15: 800-809.
77. Skipper JI, Nusbaum HC, Small SL (2005) Listening to talking faces: motor cortical activation during speech perception. Neuroimage 25: 76-89.
78. Liberman AM, Mattingly IG (1985) The motor theory of speech perception revised. Cognition 21: 1-36.
79. Schulte-Ruther M, Markowitsch HJ, Fink GR, Piefke M (2007) Mirror Neuron and Theory of Mind Mechanisms Involved in Face-to-Face Interactions: A Functional Magnetic Resonance Imaging Approach to Empathy. Journal of Cognitive Neuroscience 19: 1354-1372.
80. de Gelder B, Snyder J, Greve D, Gerard G, Hadjikhani N (2004) Fear fosters flight: a mechanism for fear contagion when perceiving emotion expressed by a whole body. Proc Natl Acad Sci U S A 101: 16701-16706.
81. Koski L, Wohlschlager A, Bekkering H, Woods RP, Dubeau MC, et al. (2002) Modulation of Motor and Premotor Activity during Imitation of Targetdirected Actions. Cereb Cortex 12: 847-855.
82. Nelissen K, Luppino G, Vanduffel W, Rizzolatti G, Orban GA (2005) Observing Others: Multiple Action Representation in the Frontal Lobe. Science 310: 332-336.
83. Peeters R, Simone L, Nelissen K, Fabbri-Destro M, Vanduffel W, et al. (2009) The Representation of Tool Use in Humans and Monkeys: Common and Uniquely Human Features. J Neurosci 29: 11523-11539.
84. Saygin AP, Wilson SM, Hagler DJ, Jr., Bates E, Sereno MI (2004) Point-light biological motion perception activates human premotor cortex. J Neurosci 24: 6181-6188.
85. Kilner JM, Paulignan Y, Blakemore SJ (2003) An interference effect of observed biological movement on action. Current Biology 13: 522-525.
86. Oztop E, Franklin D, Chaminade T, Gordon C (2005) Human-humanoid interaction: is a humanoid robot perceived as a human. Internation Journal of Humanoid Robotics 2: 537-559.
87. Press C, Bird G, Flach R, Heyes C (2005) Robotic movement elicits automatic imitation. Brain Res Cogn Brain Res 25: 632-640.