Face processing regions are sensitive to distinct aspects of temporal sequence in facial dynamics

NeuroImage

Volumn 102, Issue P2, 2014, Pages 407-415

  Reinl, Maren ^a   Bartels, Andreas ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Emotion; Faces; FFA; Motion; Predictive coding; STS

Indexed keywords

ADULT; ARTICLE; BEHAVIOR; BRAIN FUNCTION; BRAIN REGION; CONTROLLED STUDY; EMOTION; EMOTION DIRECTION FACIAL DYNAMICS; FACE PROCESSING REGION; FACIAL EXPRESSION; FACTORIAL DESIGN; FEAR; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUSIFORM FACE AREA; HUMAN; HUMAN EXPERIMENT; MALE; MOVEMENT (PHYSIOLOGY); NORMAL HUMAN; OCCIPITAL FACE AREA; PRIORITY JOURNAL; SUPERIOR TEMPORAL SULCUS; TIME; TIMELINE FACIAL DYNAMICS; VISUAL STIMULATION; BRAIN MAPPING; FACE; NUCLEAR MAGNETIC RESONANCE IMAGING; OCCIPITAL LOBE; PHOTOSTIMULATION; PHYSIOLOGY; TEMPORAL LOBE; VISION; YOUNG ADULT; EMOTIONALITY; FACIAL DYNAMICS; FACIES; OCCIPITAL CORTEX; PREDICTION; SENSITIVITY ANALYSIS; STIMULUS RESPONSE; TASK PERFORMANCE; TEMPORAL ANALYSIS;

ADULT; BRAIN MAPPING; EMOTIONS; FACE; FACIAL EXPRESSION; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MOVEMENT; OCCIPITAL LOBE; PHOTIC STIMULATION; TEMPORAL LOBE; TIME FACTORS; VISUAL PERCEPTION; YOUNG ADULT;

EID: 84906345994     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2014.08.011     Document Type: Article

References (99)

1. Adolphs R. The social brain: neural basis of social knowledge. Annu. Rev. Psychol. 2009, 60:693-716.
2. Alink A., Schwiedrzik C.M., Kohler A., Singer W., Muckli L. Stimulus predictability reduces responses in primary visual cortex. J. Neurosci. Off. J. Soc. Neurosci. 2010, 30:2960-2966.
3. Ambadar Z., Schooler J.W., Cohn J.F. Deciphering the enigmatic face: the importance of facial dynamics in interpreting subtle facial expressions. Psychol. Sci. 2005, 16:403-410.
4. Apperly I.A., Samson D., Chiavarino C., Humphreys G.W. Frontal and temporo-parietal lobe contributions to theory of mind: neuropsychological evidence from a false-belief task with reduced language and executive demands. J. Cogn. Neurosci. 2004, 16:1773-1784.
5. Atkinson A.P., Adolphs R. The neuropsychology of face perception: beyond simple dissociations and functional selectivity. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 2011, 366:1726-1738.
6. Atkinson A.P., Vuong Q.C., Smithson H.E. Modulation of the face- and body-selective visual regions by the motion and emotion of point-light face and body stimuli. NeuroImage 2012, 59:1700-1712.
7. Bahnemann M., Dziobek I., Prehn K., Wolf I., Heekeren H.R. Sociotopy in the temporoparietal cortex: common versus distinct processes. Soc. Cogn. Affect. Neurosci. 2010, 5:48-58.
8. Baron-Cohen S., Ring H.A., Wheelwright S., Bullmore E.T., Brammer M.J., Simmons A., Williams S.C. Social intelligence in the normal and autistic brain: an fMRI study. Eur. J. Neurosci. 1999, 11:1891-1898.
9. Bartels A., Zeki S. Functional brain mapping during free viewing of natural scenes. Hum. Brain Mapp. 2004, 21:75-83.
10. Bartels A., Zeki S., Logothetis N.K. Natural vision reveals regional specialization to local motion and to contrast-invariant, global flow in the human brain. Cereb. Cortex 2008, 18:705-717.
11. Battelli L., Cavanagh P., Thornton I.M. Perception of biological motion in parietal patients. Neuropsychologia 2003, 41:1808-1816.
12. Blake R., Shiffrar M. Perception of human motion. Annu. Rev. Psychol. 2007, 58:47-73.
13. Bonda E., Petrides M., Ostry D., Evans A. Specific involvement of human parietal systems and the amygdala in the perception of biological motion. J. Neurosci. 1996, 16:3737-3744.
14. Bouvier S.E., Engel S.A. Behavioral deficits and cortical damage loci in cerebral achromatopsia. Cereb. Cortex 2006, 16:183-191.
15. Campbell R. The neuropsychology of lipreading. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 1992, 335:39-45.
16. Campbell R., MacSweeney M., Surguladze S., Calvert G., McGuire P., Suckling J., Brammer M.J., David A.S. Cortical substrates for the perception of face actions: an fMRI study of the specificity of activation for seen speech and for meaningless lower-face acts (gurning). Brain Res. Cogn. Brain Res. 2001, 12:233-243.
17. Decety J., Grezes J. Neural mechanisms subserving the perception of human actions. Trends Cogn. Sci. 1999, 3:172-178.
18. Desjardins A.E., Kiehl K.A., Liddle P.F. Removal of confounding effects of global signal in functional MRI analyses. NeuroImage 2001, 13:751-758.
19. Dolan R.J., Fletcher P., Morris J., Kapur N., Deakin J.F., Frith C.D. Neural activation during covert processing of positive emotional facial expressions. NeuroImage 1996, 4:194-200.
20. Dzhelyova M.P., Ellison A., Atkinson A.P. Event-related repetitive TMS reveals distinct, critical roles for right OFA and bilateral posterior STS in judging the sex and trustworthiness of faces. J. Cogn. Neurosci. 2011, 23:2782-2796.
21. Ekman P., Friesen W.V., Hager J.C. The Facial Action Coding System 2002, Research Nexus eBook, Salt Lace City, UT. 2nd ed.
22. Fletcher P.C., Happé F., Frith U., Baker S.C., Dolan R.J., Frackowiak R.S.J., Frith C.D. Other minds in the brain: a functional imaging study of "theory of mind" in story comprehension. Cognition 1995, 57:109-128.
23. Foley E., Rippon G., Thai N.J., Longe O., Senior C. Dynamic facial expressions evoke distinct activation in the face perception network: a connectivity analysis study. J. Cogn. Neurosci. 2012, 24:507-520.
24. Fox C.J., Iaria G., Barton J.J. Defining the face processing network: optimization of the functional localizer in fMRI. Hum. Brain Mapp. 2009, 30:1637-1651.
25. Friston K. A theory of cortical responses. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 2005, 360:815-836.
26. Furl N., van Rijsbergen N.J., Kiebel S.J., Friston K.J., Treves A., Dolan R.J. Modulation of perception and brain activity by predictable trajectories of facial expressions. Cereb. Cortex 2010, 20:694-703.
27. Furl N., Garrido L., Dolan R.J., Driver J., Duchaine B. Fusiform gyrus face selectivity relates to individual differences in facial recognition ability. J. Cogn. Neurosci. 2011, 23:1723-1740.
28. Furl N., Hadj-Bouziane F., Liu N., Averbeck B.B., Ungerleider L.G. Dynamic and static facial expressions decoded from motion-sensitive areas in the macaque monkey. J. Neurosci. Off. J. Soc. Neurosci. 2012, 32:15952-15962.
29. Gallagher H.L., Happe F., Brunswick N., Fletcher P.C., Frith U., Frith C.D. Reading the mind in cartoons and stories: an fMRI study of 'theory of mind' in verbal and nonverbal tasks. Neuropsychologia 2000, 38:11-21.
30. Gauthier I., Tarr M.J., Moylan J., Skudlarski P., Gore J.C., Anderson A.W. The fusiform "face area"" is part of a network that processes faces at the individual level. J. Cogn. Neurosci. 2000, 12:495-504.
31. Gerber A.J., Posner J., Gorman D., Colibazzi T., Yu S., Wang Z., Kangarlu A., Zhu H., Russell J., Peterson B.S. An affective circumplex model of neural systems subserving valence, arousal, and cognitive overlay during the appraisal of emotional faces. Neuropsychologia 2008, 46:2129-2139.
32. Giese M.A., Poggio T. Neural mechanisms for the recognition of biological movements. Nat. Rev. Neurosci. 2003, 4:179-192.
33. Grossman E., Donnelly M., Price R., Pickens D., Morgan V., Neighbor G., Blake R. Brain areas involved in perception of biological motion. J. Cogn. Neurosci. 2000, 12:711-720.
34. Grossman E.D., Battelli L., Pascual-Leone A. Repetitive TMS over posterior STS disrupts perception of biological motion. Vis. Res. 2005, 45:2847-2853.
35. Gschwind M., Pourtois G., Schwartz S., Van De Ville D., Vuilleumier P. White-matter connectivity between face-responsive regions in the human brain. Cereb. Cortex 2012, 22:1564-1576.
36. Haxby J.V., Hoffman E.A., Gobbini M.I. The distributed human neural system for face perception. Trends Cogn. Sci. 2000, 4:223-233.
37. Hill H., Johnston A. Categorizing sex and identity from the biological motion of faces. Curr. Biol. 2001, 11:880-885.
38. Hoffman E.A., Haxby J.V. Distinct representations of eye gaze and identity in the distributed human neural system for face perception. Nat. Neurosci. 2000, 3:80-84.
39. Ishai A., Pessoa L., Bikle P.C., Ungerleider L.G. Repetition suppression of faces is modulated by emotion. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:9827-9832.
40. Ishai A., Schmidt C.F., Boesiger P. Face perception is mediated by a distributed cortical network. Brain Res. Bull. 2005, 67:87-93.
41. Jastorff J., Kourtzi Z., Giese M.A. Visual learning shapes the processing of complex movement stimuli in the human brain. J. Neurosci. Off. J. Soc. Neurosci. 2009, 29:14026-14038.
42. Jiang X., Rosen E., Zeffiro T., Vanmeter J., Blanz V., Riesenhuber M. Evaluation of a shape-based model of human face discrimination using FMRI and behavioral techniques. Neuron 2006, 50:159-172.
43. Kadosh K.C., Walsh V., Kadosh R.C. Investigating face-property specific processing in the right OFA. Soc. Cogn. Affect. Neurosci. 2011, 6:58-65.
44. Kanai R., Carmel D., Bahrami B., Rees G. Structural and functional fractionation of right superior parietal cortex in bistable perception. Curr. Biol. 2011, 21:R106-R107.
45. Kanwisher N., McDermott J., Chun M.M. The fusiform face area: a module in human extrastriate cortex specialized for face perception. J. Neurosci. 1997, 17:4302-4311.
46. Kaul C., Rees G., Ishai A. The gender of face stimuli is represented in multiple regions in the human brain. Front. Hum. Neurosci. 2011, 4:238.
47. Kaulard K., Cunningham D.W., Bulthoff H.H., Wallraven C. The MPI facial expression database - a validated database of emotional and conversational facial expressions. PLoS One 2012, 7:e32321.
48. Kilts C.D., Egan G., Gideon D.A., Ely T.D., Hoffman J.M. Dissociable neural pathways are involved in the recognition of emotion in static and dynamic facial expressions. NeuroImage 2003, 18:156-168.
49. Kriegeskorte N., Formisano E., Sorger B., Goebel R. Individual faces elicit distinct response patterns in human anterior temporal cortex. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:20600-20605.
50. LaBar K.S., Crupain M.J., Voyvodic J.T., McCarthy G. Dynamic perception of facial affect and identity in the human brain. Cereb. Cortex 2003, 13:1023-1033.
51. Lee L.C., Andrews T.J., Johnson S.J., Woods W., Gouws A., Green G.G., Young A.W. Neural responses to rigidly moving faces displaying shifts in social attention investigated with fMRI and MEG. Neuropsychologia 2010, 48:477-490.
52. Liu T.T. Efficiency, power, and entropy in event-related fMRI with multiple trial types. Part II: design of experiments. NeuroImage 2004, 21:401-413.
53. McCarthy G., Puce A., Gore J.C., Allison T. Face-specific processing in the human fusiforrn gyms. J. Cogn. Neurosci. 1997, 9:605-610.
54. Muckli L., Kohler A., Kriegeskorte N., Singer W. Primary visual cortex activity along the apparent-motion trace reflects illusory perception. PLoS Biol. 2005, 3:e265.
55. Murray S.O., Wojciulik E. Attention increases neural selectivity in the human lateral occipital complex. Nat. Neurosci. 2004, 7:70-74.
56. Murray S.O., Kersten D., Olshausen B.A., Schrater P., Woods D.L. Shape perception reduces activity in human primary visual cortex. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:15164-15169.
57. Natu V., Raboy D., O'Toole A.J. Neural correlates of own- and other-race face perception: spatial and temporal response differences. NeuroImage 2011, 54:2547-2555.
58. Nestor A., Plaut D.C., Behrmann M. Unraveling the distributed neural code of facial identity through spatiotemporal pattern analysis. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:9998-10003.
59. Nummenmaa L., Calder A.J. Neural mechanisms of social attention. Trends Cogn. Sci. 2009, 13:135-143.
60. O'Toole A.J., Roark D.A., Abdi H. Recognizing moving faces: a psychological and neural synthesis. Trends Cogn. Sci. 2002, 6:261-266.
61. Pavlova M., Staudt M., Sokolov A., Birbaumer N., Krageloh-Mann I. Perception and production of biological movement in patients with early periventricular brain lesions. Brain 2003, 126:692-701.
62. Peelen M.V., Wiggett A.J., Downing P.E. Patterns of fMRI activity dissociate overlapping functional brain areas that respond to biological motion. Neuron 2006, 49:815-822.
63. Pessoa L., McKenna M., Gutierrez E., Ungerleider L.G. Neural processing of emotional faces requires attention. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:11458-11463.
64. Pitcher D., Garrido L., Walsh V., Duchaine B.C. Transcranial magnetic stimulation disrupts the perception and embodiment of facial expressions. J. Neurosci. Off. J. Soc. Neurosci. 2008, 28:8929-8933.
65. Pitcher D., Dilks D.D., Saxe R.R., Triantafyllou C., Kanwisher N. Differential selectivity for dynamic versus static information in face-selective cortical regions. NeuroImage 2011, 56:2356-2363.
66. Puce A., Perrett D. Electrophysiology and brain imaging of biological motion. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 2003, 358:435-445.
67. Puce A., Allison T., Gore J.C., McCarthy G. Face-sensitive regions in human extrastriate cortex studied by functional MRI. J. Neurophysiol. 1995, 74:1192-1199.
68. Puce A., Allison T., Bentin S., Gore J.C., McCarthy G. Temporal cortex activation in humans viewing eye and mouth movements. J. Neurosci. Off. J. Soc. Neurosci. 1998, 18:2188-2199.
69. Rao R.P., Ballard D.H. Predictive coding in the visual cortex: a functional interpretation of some extra-classical receptive-field effects. Nat. Neurosci. 1999, 2:79-87.
70. Rilling J.K., Sanfey A.G., Aronson J.A., Nystrom L.E., Cohen J.D. The neural correlates of theory of mind within interpersonal interactions. NeuroImage 2004, 22:1694-1703.
71. Rossion B., Caldara R., Seghier M., Schuller A.M., Lazeyras F., Mayer E. A network of occipito-temporal face-sensitive areas besides the right middle fusiform gyrus is necessary for normal face processing. Brain 2003, 126:2381-2395.
72. Said C.P., Moore C.D., Engell A.D., Todorov A., Haxby J.V. Distributed representations of dynamic facial expressions in the superior temporal sulcus. J. Vis. 2010, 10. (11-11).
73. Said C.P., Haxby J.V., Todorov A. Brain systems for assessing the affective value of faces. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 2011, 366:1660-1670.
74. Sato W., Kochiyama T., Yoshikawa S., Naito E., Matsumura M. Enhanced neural activity in response to dynamic facial expressions of emotion: an fMRI study. Brain Res. Cogn. Brain Res. 2004, 20:81-91.
75. Sato W., Kochiyama T., Yoshikawa S. Amygdala activity in response to forward versus backward dynamic facial expressions. Brain Res. 2010, 1315:92-99.
76. Saxe R., Kanwisher N. People thinking about thinking people. The role of the temporo-parietal junction in "theory of mind". NeuroImage 2003, 19:1835-1842.
77. Saygin A.P. Superior temporal and premotor brain areas necessary for biological motion perception. Brain 2007, 130:2452-2461.
78. Schultz J., Pilz K.S. Natural facial motion enhances cortical responses to faces. Exp. Brain Res. 2009, 194:465-475.
79. Schultz J., Friston K.J., O'Doherty J., Wolpert D.M., Frith C.D. Activation in posterior superior temporal sulcus parallels parameter inducing the percept of animacy. Neuron 2005, 45:625-635.
80. Schultz J., Brockhaus M., Bulthoff H.H., Pilz K.S. What the human brain likes about facial motion. Cereb. Cortex 2012, 12:1167-1178.
81. Sergent J., Ohta S., Macdonald B. Functional anatomy of face and object processing. Brain 1992, 115:15-36.
82. Smith F.W., Muckli L. Nonstimulated early visual areas carry information about surrounding context. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:20099-20103.
83. Steeves J.K., Culham J.C., Duchaine B.C., Pratesi C.C., Valyear K.F., Schindler I., Humphrey G.K., Milner A.D., Goodale M.A. The fusiform face area is not sufficient for face recognition: evidence from a patient with dense prosopagnosia and no occipital face area. Neuropsychologia 2006, 44:594-609.
84. Steeves J., Dricot L., Goltz H.C., Sorger B., Peters J., Milner A.D., Goodale M.A., Goebel R., Rossion B. Abnormal face identity coding in the middle fusiform gyrus of two brain-damaged prosopagnosic patients. Neuropsychologia 2009, 47:2584-2592.
85. Surguladze S.A., Brammer M.J., Young A.W., Andrew C., Travis M.J., Williams S.C., Phillips M.L. A preferential increase in the extrastriate response to signals of danger. NeuroImage 2003, 19:1317-1328.
86. Thornton I.M., Kourtzi Z. A matching advantage for dynamic human faces. Perception 2002, 31:113-132.
87. Trautmann S.A., Fehr T., Herrmann M. Emotions in motion: dynamic compared to static facial expressions of disgust and happiness reveal more widespread emotion-specific activations. Brain Res. 2009, 1284:100-115.
88. Vaina L.M., Gross C.G. Perceptual deficits in patients with impaired recognition of biological motion after temporal lobe lesions. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:16947-16951.
89. van der Gaag C., Minderaa R.B., Keysers C. The BOLD signal in the amygdala does not differentiate between dynamic facial expressions. Soc. Cogn. Affect. Neurosci. 2007, 2:93-103.
90. Van Dijk K.R., Hedden T., Venkataraman A., Evans K.C., Lazar S.W., Buckner R.L. Intrinsic functional connectivity as a tool for human connectomics: theory, properties, and optimization. J. Neurophysiol. 2010, 103:297-321.
91. van Kemenade B.M., Muggleton N., Walsh V., Saygin A.P. Effects of TMS over premotor and superior temporal cortices on biological motion perception. J. Cogn. Neurosci. 2012, 24:896-904.
92. Vangeneugden J., Pollick F., Vogels R. Functional differentiation of macaque visual temporal cortical neurons using a parametric action space. Cereb. Cortex 2009, 19:593-611.
93. Vollm B.A., Taylor A.N., Richardson P., Corcoran R., Stirling J., McKie S., Deakin J.F., Elliott R. Neuronal correlates of theory of mind and empathy: a functional magnetic resonance imaging study in a nonverbal task. NeuroImage 2006, 29:90-98.
94. Vuilleumier P., Pourtois G. Distributed and interactive brain mechanisms during emotion face perception: evidence from functional neuroimaging. Neuropsychologia 2007, 45:174-194.
95. Vuilleumier P., Armony J.L., Driver J., Dolan R.J. Effects of attention and emotion on face processing in the human brain: an event-related fMRI study. Neuron 2001, 30:829-841.
96. Wehrle T., Kaiser S., Schmidt S., Scherer K.R. Studying the dynamics of emotional expression using synthesized facial muscle movements. J. Pers. Soc. Psychol. 2000, 78:105-119.
97. Winston J.S., O'Doherty J., Dolan R.J. Common and distinct neural responses during direct and incidental processing of multiple facial emotions. NeuroImage 2003, 20:84-97.
98. Winston J.S., Henson R.N., Fine-Goulden M.R., Dolan R.J. fMRI-adaptation reveals dissociable neural representations of identity and expression in face perception. J. Neurophysiol. 2004, 92:1830-1839.
99. Zaretskaya N., Anstis S., Bartels A. Parietal cortex mediates conscious perception of illusory gestalt. J. Neurosci. Off. J. Soc. Neurosci. 2013, 33:523-531.