Duration matters: Dissociating neural correlates of detection and evaluation of social gaze

NeuroImage

Volumn 46, Issue 4, 2009, Pages 1154-1163

  Kuzmanovic, Bojana ^a   Georgescu, Alexandra L ^a   Eickhoff, Simon B ^b,c,e   Shah, Nadim J ^b,d   Bente, Gary ^a   Fink, Gereon R ^a,b,d   Vogeley, Kai ^a,d  

^a UNIVERSITY OF COLOGNE   (Germany)

^b FORSCHUNGSZENTRUM JÜLICH   (Germany)

^c RWTH AACHEN UNIVERSITY   (Germany)

^d Brain Imaging Center West   (Germany)

^e Jülich Aachen Research Alliance Section Fundamentals of Future Information Technology JARA FIT   (Germany)

Author keywords

fMRI; Gaze direction; Gaze duration; Mentalizing; Orbitofrontal cortex; Paracingulate cortex; Reward

Indexed keywords

ADULT; ARTICLE; BRAIN REGION; COGNITION; CONTROLLED STUDY; DURA MATER; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GAZE; HUMAN; HUMAN EXPERIMENT; MALE; NERVE CELL DIFFERENTIATION; PREFRONTAL CORTEX; PRIORITY JOURNAL; SOCIAL INTERACTION; VISION; VISUAL STIMULATION;

ADULT; BRAIN; BRAIN MAPPING; EMOTIONS; FEMALE; HUMANS; IMAGE INTERPRETATION, COMPUTER-ASSISTED; INTERPERSONAL RELATIONS; MAGNETIC RESONANCE IMAGING; MALE; SOCIAL PERCEPTION; TIME; VISION, OCULAR; VISUAL PERCEPTION;

EID: 67349147901     PISSN: 10538119     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2009.03.037     Document Type: Article

References (104)

1. Aharon I., Etcoff N., Ariely D., Chabris C.F., O'Connor E., and Breiter H.C. Beautiful faces have variable reward value: fMRI and behavioral evidence. Neuron 32 (2001) 537-551
2. Akiyama T., Kato M., Muramatsu T., Saito F., Nakachi R., and Kashima H. A deficit in discriminating gaze direction in a case with right superior temporal gyrus lesion. Neuropsychologia 44 (2006) 161-170
3. Allison T., Puce A., and McCarthy G. Social perception from visual cues: role of the STS region. Trends Cogn. Sci. 4 (2000) 267-278
4. Amodio D.M., and Frith C.D. Meeting of minds: the medial frontal cortex and social cognition. Nat. Rev. Neurosci. 7 (2006) 268-277
5. Argyle M., and Cook M. Gaze and Mutual Gaze (1976), Cambridge University Press, Cambridge
6. Argyle M., and Dean J. Eye-contact, distance and affiliation. Sociometry 28 (1965) 289-304
7. Argyle M., Lefebvre L., and Cook M. The meaning of five patterns of gaze. Eur. J. Soc. Psychol. 4 (1974) 125-136
8. Ashburner J., and Friston K.J. Rigid body registration. In: Frackowiak R.S., Friston K.J., Frith C.D., Dolan R.J., Price C.J., Ashburner J., Penny W.D., and Zeki S. (Eds). Human Brain Function (2003), Academic Press, San Diego; London 635-655
9. Bailenson J.N., Blascovich J., Beall A.C., and Loomis J.M. Interpersonal distance in immersive virtual environments. Pers. Soc. Psychol. Bull. 29 (2003) 819-833
10. Baron-Cohen S. Mindblindness: An Essay on Autism and Theory Of Mind (1995), MIT Press, Cambridge, Mass.; London
11. Bente G. Facilities for the graphical computer simulation of head and body movements. Behav. Res. Meth. Instrum. Comput. 21 (1989) 455-462
12. Bente G., Feist A., and Elder S. Person perception effects of computer-simulated male and female head movement/Personwahrnehmungseffekte von computersimulierten männlichen und weiblichen Kopfbewegungen. J. Nonverbal Behav. 20 (1996) 213-228
13. Bente G., Kraemer N.C., Petersen A., and de Ruiter J.P. Computer animated movement and person perception: methodological advances in nonverbal behavior research. J. Nonverbal Behav. 25 (2001) 151-166
14. Bente G., Petersen A., Kraemer N.C., and de Ruiter J.P. Transcript-based computer animation of movement: evaluating a new tool for nonverbal behavior research. Behav. Res. Meth. Instrum. Comput. 33 (2001) 303-310
15. Blascovich J., Loomis J.M., Beall A.C., Swinth K.R., Hoyt C.L., and Bailenson J.N. Immersive virtual environment technology as a methodological tool for social psychology. Psychol. Inq. 13 (2002) 103-124
16. Blass E.M., Lumeng J., and Patil N. Influence of mutual gaze on human infant affect. In: Flom R., Lee K., and Muir D. (Eds). Gaze-following: Its Development and Significance (2007), Lawrence Erlbaum Associates, Mahwah, N.J.; London 113-143
17. Born R.T., and Bradley D.C. Structure and function of visual area MT. Annu. Rev. Neurosci. 28 (2005) 157-189
18. Bristow D., Rees G., and Frith C.D. Social interaction modifies neural response to gaze shifts. Soc. Cognitive Affect. Neurosci. 2 (2006) 52-61
19. Brooks C.I., Church M., A, and Fraser L. Effects of duration of eye contact on judgments of personality characteristics. J. Soc. Psychol. 126 (1986) 71-78
20. Bush G., Luu P., and Posner M.I. Cognitive and emotional influences in anterior cingulate cortex. Trends Cogn. Sci. 4 (2000) 215-222
21. Calder A.J., Lawrence A.D., Keane J., Scott S.K., Owen A.M., Christoffels I., and Young A.W. Reading the mind from eye gaze. Neuropsychologia 40 (2002) 1129-1138
22. Collins D.L., Neelin P., Peters T.M., and Evans A.C. Automatic 3D intersubject registration of MR volumetric data in standardized Talairach space. J. Comput. Assist. Tomogr. 18 (1994) 192-205
23. Conty L., N'Diaye K., Tijus C., and George N. When eye creates the contact! ERP evidence for early dissociation between direct and averted gaze motion processing. Neuropsychologia 45 (2007) 3024-3037
24. D'Argembeau A., Collette F., Van der Linden M., Laureys S., Del Fiore G., Degueldre C., Luxen A., and Salmon E. Self-referential reflective activity and its relationship with rest: a PET study. Neuroimage 25 (2005) 616-624
25. Dale A.M. Optimal experimental design for event-related fMRI. Hum. Brain Mapp. 8 (1999) 109-114
26. Devinsky O., Morrell M.J., and Vogt B.A. Contributions of anterior cingulate cortex to behaviour. Brain 118 Pt 1 (1995) 279-306
27. Droney J.M., and Brooks C.I. Attributions of self-esteem as a function of duration of eye contact. J. Soc. Psychol. 133 (1993) 715-722
28. Eickhoff S.B., Stephan K.E., Mohlberg H., Grefkes C., Fink G.R., Amunts K., and Zilles K. A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. Neuroimage 25 (2005) 1325-1335
29. Eickhoff S.B., Heim S., Zilles K., and Amunts K. Testing anatomically specified hypotheses in functional imaging using cytoarchitectonic maps. Neuroimage 32 (2006) 570-582
30. Eickhoff S.B., Paus T., Caspers S., Grosbras M.H., Evans A.C., Zilles K., and Amunts K. Assignment of functional activations to probabilistic cytoarchitectonic areas revisited. Neuroimage 36 (2007) 511-521
31. Einav S., and Hood B.M. Children's use of the temporal dimension of gaze for inferring preference. Dev. Psychol. 42 (2006) 142-152
32. Eskritt M., and Lee K. Preschoolers' use of eye gaze for "mind reading". In: Flom R., Lee K., and Muir D. (Eds). Gaze-following: Its Development and Significance (2007), Lawrence Erlbaum Associates, Mahwah, N.J.; London 243-263
33. Evans A.C., Marrett S., Neelin P., Collins L., Worsley K., Dai W., Milot S., Meyer E., and Bub D. Anatomical mapping of functional activation in stereotactic coordinate space. Neuroimage 1 (1992) 43-53
34. Farroni T., Csibra G., Simion F., and Johnson M.H. Eye contact detection in humans from birth. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 9602-9605
35. Friston K.J., Holmes A., Poline J.B., Price C.J., and Frith C.D. Detecting activations in PET and fMRI: levels of inference and power. Neuroimage 4 (1996) 223-235
36. Frith U. Mind blindness and the brain in autism. Neuron 32 (2001) 969-979
37. Gallagher H.L., Jack A.I., Roepstorff A., and Frith C.D. Imaging the intentional stance in a competitive game. Neuroimage 16 (2002) 814-821
38. George N., Driver J., and Dolan R.J. Seen gaze-direction modulates fusiform activity and its coupling with other brain areas during face processing. Neuroimage 13 (2001) 1102-1112
39. Gibson J.J., and Pick A.D. Perception of another person's looking behavior. Am. J. Psychol. 76 (1963) 386-394
40. Gobbini M.I., Koralek A.C., Bryan R.E., Montgomery K.J., and Haxby J.V. Two takes on the social brain: a comparison of theory of mind tasks. J. Cogn. Neurosci. 19 (2007) 1803-1814
41. Gopnik A., Slaughter V., and Meltzoff A. Changing your views: how understanding visual perception can lead to a new theory of mind. In: Lewis C., and Mitchell P. (Eds). Children's Early Understanding Of Mind (1994), Lawrence Erlbaum Associates, UK 157-183
42. Grossman E.D., and Blake R. Brain areas active during visual perception of biological motion. Neuron 35 (2002) 1167-1175
43. Gueguen N., and Jacob C. Direct look versus evasive glance and compliance with a request. J. Soc. Psychol. 142 (2002) 393-396
44. Gusnard D.A., Akbudak E., Shulman G.L., and Raichle M.E. Medial prefrontal cortex and self-referential mental activity: relation to a default mode of brain function. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 4259-4264
45. Gusnard D.A., Raichle M.E., and Raichle M.E. Searching for a baseline: functional imaging and the resting human brain. Nat. Rev. Neurosci. 2 (2001) 685-694
46. Hains S.M., and Muir D.W. Infant sensitivity to adult eye direction. Child Dev. 67 (1996) 1940-1951
47. Heinzel A., Bermpohl F., Niese R., Pfennig A., Pascual-Leone A., Schlaug G., and Northoff G. How do we modulate our emotions? Parametric fMRI reveals cortical midline structures as regions specifically involved in the processing of emotional valences. Brain Res. Cogn. Brain Res. 25 (2005) 348-358
48. Hoffman E.A., and Haxby J.V. Distinct representations of eye gaze and identity in the distributed human neural system for face perception. Nat. Neurosci. 3 (2000) 80-84
49. Holmes C.J., Hoge R., Collins L., Woods R., Toga A.W., and Evans A.C. Enhancement of MR images using registration for signal averaging. J. Comput. Assist. Tomogr. 22 (1998) 324-333
50. Hood B.M., and Macrae C.N. Look into my eyes: the effect of direct gaze on face processing in children and adults. In: Flom R., Lee K., and Muir D. (Eds). Gaze-following: Its Development and Significance (2007), Lawrence Erlbaum Associates, Mahwah, N.J.; London 297-383
51. Hooker C.I., Paller K.A., Gitelman D.R., Parrish T.B., Mesulam M.M., and Reber P.J. Brain networks for analyzing eye gaze. Brain Res. Cogn. Brain Res. 17 (2003) 406-418
52. Iacoboni M., Lieberman M.D., Knowlton B.J., Molnar-Szakacs I., Moritz M., Throop C.J., and Fiske A.P. Watching social interactions produces dorsomedial prefrontal and medial parietal BOLD fMRI signal increases compared to a resting baseline. Neuroimage 21 (2004) 1167-1173
53. Johnson M.H., and Farroni T. The neurodevelopmental origins of eye gaze perception. In: Flom R., Lee K., and Muir D. (Eds). Gaze-following: Its Development and Significance (2007), Lawrence Erlbaum Associates, Mahwah, N.J.; London 1-17
54. Kampe K.K., Frith C.D., and Frith U. "Hey John": signals conveying communicative intention toward the self activate brain regions associated with "mentalizing", regardless of modality. J. Neurosci. 23 (2003) 5258-5263
55. Kawashima R., Sugiura M., Kato T., Nakamura A., Hatano K., Ito K., Fukuda H., Kojima S., and Nakamura K. The human amygdala plays an important role in gaze monitoring. A PET study. Brain 122 Pt 4 (1999) 779-783
56. Kim H., Adolphs R., O'Doherty J.P., and Shimojo S. Temporal isolation of neural processes underlying face preference decisions. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 18253-18258
57. Kleinke C.L. Gaze and eye contact: a research review. Psychol. Bull. 100 (1986) 78-100
58. Knackstedt G., and Kleinke C.L. Eye contact, gender, and personality judgments. J. Soc. Psychol. 131 (1991) 303-304
59. Kranz F., and Ishai A. Face perception is modulated by sexual preference. Curr. Biol. 16 (2006) 63-68
60. Kringelbach M.L. The human orbitofrontal cortex: linking reward to hedonic experience. Nat. Rev., Neurosci. 6 (2005) 691-702
61. Kringelbach M.L., and Rolls E.T. The functional neuroanatomy of the human orbitofrontal cortex: evidence from neuroimaging and neuropsychology. Prog. Neurobiol. 72 (2004) 341-372
62. Ku J., Jang H.J., Kim K.U., Kim J.H., Park S.H., Lee J.H., Kim J.J., Kim I.Y., and Kim S.I. Experimental results of affective valence and arousal to avatar's facial expressions. Cyberpsychol. Behav. 8 (2005) 493-503
63. Lancaster J.L., Woldorff M.G., Parsons L.M., Liotti M., Freitas C.S., Rainey L., Kochunov P.V., Nickerson D., Mikiten S.A., and Fox P.T. Automated Talairach atlas labels for functional brain mapping. Hum. Brain Mapp. 10 (2000) 120-131
64. Liu X., Powell D.K., Wang H., Gold B.T., Corbly C.R., and Joseph J.E. Functional dissociation in frontal and striatal areas for processing of positive and negative reward information. J. Neurosci. 27 (2007) 4587-4597
65. Mah L., Arnold M.C., and Grafman J. Lesions of prefrontal cortex impair social perception. Am. J. Psychiatr. 161 (2004) 1247-1255
66. Maldjian J.A., Laurienti P.J., Kraft R.A., and Burdette J.H. An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 19 (2003) 1233-1239
67. Malikovic A., Amunts K., Schleicher A., Mohlberg H., Eickhoff S.B., Wilms M., Palomero-Gallagher N., Armstrong E., and Zilles K. Cytoarchitectonic analysis of the human extrastriate cortex in the region of V5/MT+: a probabilistic, stereotaxic map of area hOc5. Cereb. Cortex 17 (2007) 562-574
68. Mason M.F., Tatkow E.P., and Macrae C.N. The look of love: gaze shifts and person perception. Psychol. Sci. 16 (2005) 236-239
69. Mazoyer B., Zago L., Mellet E., Bricogne S., Etard O., Houde O., Crivello F., Joliot M., Petit L., and Tzourio-Mazoyer N. Cortical networks for working memory and executive functions sustain the conscious resting state in man. Brain Res. Bull. 54 (2001) 287-298
70. Mirenda P.L., Donnellan A.M., and Yoder D.E. Gaze behavior: a new look at an old problem. J. Autism. Dev. Disord. 13 (1983) 397-409
71. Mitchell J.P., Banaji M.R., and Macrae C.N. The link between social cognition and self-referential thought in the medial prefrontal cortex. J. Cogn. Neurosci. 17 (2005) 1306-1315
72. Montgomery D.E., Bach L.M., and Moran C. Children's use of looking behavior as a cue to detect another's goal. Child Dev. 69 (1998) 692-705
73. Moser E., Derntl B., Robinson S., Fink B., Gur R.C., and Grammer K. Amygdala activation at 3 T in response to human and avatar facial expressions of emotions. J. Neurosci. Methods 161 (2007) 126-133
74. Nichols K.A., and Champness B.G. Eye gaze and the GSR. J. Exp. Soc. Psychol. 7 (1971) 623-626
75. Northoff G., Heinzel A., Bermpohl F., Niese R., Pfennig A., Pascual-Leone A., and Schlaug G. Reciprocal modulation and attenuation in the prefrontal cortex: an fMRI study on emotional-cognitive interaction. Hum. Brain Mapp. 21 (2004) 202-212
76. O'Doherty J.P. Reward representations and reward-related learning in the human brain: insights from neuroimaging. Curr. Opin. Neurobiol. 14 (2004) 769-776
77. O'Doherty J., Winston J., Critchley H., Perrett D., Burt D.M., and Dolan R.J. Beauty in a smile: the role of medial orbitofrontal cortex in facial attractiveness. Neuropsychologia 41 (2003) 147-155
78. Ochsner K.N., Beer J.S., Robertson E.R., Cooper J.C., Gabrieli J.D., Kihsltrom J.F., and D'Esposito M. The neural correlates of direct and reflected self-knowledge. Neuroimage 28 (2005) 797-814
79. Oldfield R.C. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9 (1971) 97-113
80. Omori Y., and Miyata Y. Estimates of impressions based on frequency of blinking. Soc. Behav. Personal. 29 (2001) 159-168
81. Pelphrey K.A., Mitchell T.V., McKeown M.J., Goldstein J., Allison T., and McCarthy G. Brain activity evoked by the perception of human walking: controlling for meaningful coherent motion. J. Neurosci. 23 (2003) 6819-6825
82. Pelphrey K.A., Singerman J.D., Allison T., and McCarthy G. Brain activation evoked by perception of gaze shifts: the influence of context. Neuropsychologia 41 (2003) 156-170
83. Pelphrey K.A., Morris J.P., and McCarthy G. Grasping the intentions of others: the perceived intentionality of an action influences activity in the superior temporal sulcus during social perception. J. Cogn. Neurosci. 16 (2004) 1706-1716
84. Pelphrey K.A., Viola R.J., and McCarthy G. When strangers pass: processing of mutual and averted social gaze in the superior temporal sulcus. Psychol Sci 15 (2004) 598-603
85. Penny W.D., and Holmes A.P. Random effects analysis. In: Frackowiak R.S., Friston K.J., Frith C.D., Dolan R.J., Price C.J., Ashburner J., Penny W.D., and Zeki S. (Eds). Human Brain Function (2003), Academic Press, San Diego; London 843-850
86. Premack D., and Woodruff G. Does the chimpanzee have a theory of mind?. Behav. Brain Sci. 1 (1978) 515-526
87. Puce A., Allison T., Bentin S., Gore J.C., and McCarthy G. Temporal cortex activation in humans viewing eye and mouth movements. J. Neurosci. 18 (1998) 2188-2199
88. Raichle M.E., MacLeod A.M., Snyder A.Z., Powers W.J., Gusnard D.A., and Shulman G.L. A default mode of brain function. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 676-682
89. Schilbach L., Wohlschlaeger A.M., Kraemer N.C., Newen A., Shah N.J., Fink G.R., and Vogeley K. Being with virtual others: neural correlates of social interaction. Neuropsychologia 44 (2006) 718-730
90. Schilbach L., Eickhoff S.B., Rotarska-Jagiela A., Fink G.R., and Vogeley K. Minds at rest? Social cognition as the default mode of cognizing and its putative relationship to the "default system" of the brain. Conscious. Cogn. 17 (2008) 457-467
91. Serences J.T. A comparison of methods for characterizing the event-related BOLD timeseries in rapid fMRI. Neuroimage 21 (2004) 1690-1700
92. Symons L.A., Hains S.M.J., and Muir D.W. Look at me: five-month-old infants' sensitivity to very small deviations in eye-gaze during social interactions. Infant Behavi. Dev. 21 (1998) 531-536
93. Valentine M.E., and Ehrlichman H. Interpersonal gaze and helping behavior. J. Soc. Psychol. 107 (1979) 193-198
94. Vogeley K., Bussfeld P., Newen A., Herrmann S., Happe F., Falkai P., Maier W., Shah N.J., Fink G.R., and Zilles K. Mind reading: neural mechanisms of theory of mind and self-perspective. Neuroimage 14 (2001) 170-181
95. von Grunau M., and Anston C. The detection of gaze direction: a stare-in-the-crowd effect. Perception 24 (1995) 1297-1313
96. Vuilleumier P., and Pourtois G. Distributed and interactive brain mechanisms during emotion face perception: evidence from functional neuroimaging. Neuropsychologia 45 (2007) 174-194
97. Vuilleumier P., George N., Lister V., Armony J., and Driver J. Effects of perceived mutual gaze and gender on face processing and recognition memory. Vis. Cogn. 12 (2005) 85-101
98. Walter H., Adenzato M., Ciaramidaro A., Enrici I., Pia L., and Bara B.G. Understanding intentions in social interaction: the role of the anterior paracingulate cortex. J. Cogn. Neurosci. 16 (2004) 1854-1863
99. Watanabe S., Kakigi R., and Puce A. Occipitotemporal activity elicited by viewing eye movements: a magnetoencephalographic study. Neuroimage 13 (2001) 351-363
100. Watanabe S., Kakigi R., Miki K., and Puce A. Human MT/V5 activity on viewing eye gaze changes in others: a magnetoencephalographic study. Brain Res. 1092 (2006) 152-160
101. Wicker B., Michel F., Henaff M.A., and Decety J. Brain regions involved in the perception of gaze: a PET study. Neuroimage 8 (1998) 221-227
102. Wicker B., Perrett D.I., Baron-Cohen S., and Decety J. Being the target of another's emotion: a PET study. Neuropsychologia 41 (2003) 139-146
103. Wilms M., Eickhoff S.B., Specht K., Amunts K., Shah N.J., Malikovic A., and Fink G.R. Human V5/MT+: comparison of functional and cytoarchitectonic data. Anat. Embryol. (Berl) 210 (2005) 485-495
104. Zysset S., Huber O., Ferstl E., and von Cramon D.Y. The anterior frontomedian cortex and evaluative judgment: an fMRI study. Neuroimage 15 (2002) 983-991