Early processing of emotional faces in children with autism: An event-related potential study

Journal of Experimental Child Psychology

Volumn 109, Issue 4, 2011, Pages 430-444

  Batty, Magali ^a   Meaux, Emilie ^a   Wittemeyer, Kerstin ^b   Rogé, Bernadette ^c   Taylor, Margot J ^d  

^a UNIVERSITÉ DE TOURS   (France)

^b UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^c Université de Toulouse II Le Mirail   (France)

^d UNIVERSITY OF TORONTO   (Canada)

Author keywords

Autism; Autism spectrum disorders (ASDs); Development; Emotional faces; Event related potentials (ERPs); Visual processing

Indexed keywords

ADOLESCENT; ARTICLE; AUTISM; BRAIN; CASE CONTROL STUDY; CHILD; ELECTROENCEPHALOGRAPHY; EMOTION; EVOKED RESPONSE; FACIAL EXPRESSION; FEMALE; HUMAN; MALE; NEUROPSYCHOLOGICAL TEST; PATHOPHYSIOLOGY; PATTERN RECOGNITION; PSYCHOLOGICAL ASPECT; REACTION TIME;

ADOLESCENT; BRAIN; CASE-CONTROL STUDIES; CHILD; CHILD DEVELOPMENT DISORDERS, PERVASIVE; ELECTROENCEPHALOGRAPHY; EMOTIONS; EVOKED POTENTIALS; FACIAL EXPRESSION; FEMALE; HUMANS; MALE; NEUROPSYCHOLOGICAL TESTS; PATTERN RECOGNITION, VISUAL; REACTION TIME;

EID: 79955472558     PISSN: 00220965     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jecp.2011.02.001     Document Type: Article

References (112)

1. Adolphs R., Damasio H., Tranel D., Cooper G., Damasio A.R. A role for somatosensory cortices in the visual recognition of emotion as revealed by three-dimensional lesion mapping. Journal of Neuroscience 2000, 20:2683-2690.
2. Adolphs R., Sears L., Piven J. Abnormal processing of social information from faces in autism. Journal of Cognitive Neuroscience 2001, 13:232-240.
3. Allison T., Puce A., McCarthy G. Social perception from visual cues: Role of the STS region. Trends in Cognitive Sciences 2000, 4:267-278.
4. Amaral D.G., Bauman M.D., Schumann C.M. The amygdala and autism: Implications from non-human primate studies. Genes, Brain, and Behavior 2003, 2:295-302.
5. American Psychological Association Diagnostic and statistical manual of mental disorders 1994, Author, Washington, DC. 4th ed.
6. Ashwin E., Ashwin C., Rhydderch D., Howells J., Baron-Cohen S. Eagle-eyed visual acuity: An experimental investigation of enhanced perception in autism. Biological Psychiatry 2009, 65:17-21.
7. Bachevalier J. An animal model for childhood autism: Memory loss and socioemotional disturbances following neonatal damage to the limbic system in monkeys. Advances in neuropsychiatry and psychopharmacology, Vol. 1: Schizophenia research 1991, 129-140. Raven, New York. C. Tamminga, S. Schulz (Eds.).
8. Balconi M., Pozzoli U. Face-selective processing and the effect of pleasant and unpleasant emotional expressions on ERP correlates. International Journal of Psychophysiology 2003, 49:67-74.
9. Baron-Cohen S. Mindblindness: An essay on autism and theory of mind 1995, MIT Press/Bradford Books, Cambridge, MA.
10. Baron-Cohen S., Wheelwright S., Hill J., Raste Y., Plumb I. The " Reading the Mind in the Eyes" test revised version: A study with normal adults, and adults with Asperger syndrome or high-functioning autism. Journal of Child Psychology and Psychiatry and Allied Disciplines 2001, 42:241-251.
11. Baron-Cohen S., Ring H.A., Bullmore E.T., Wheelwright S., Ashwin C., Williams S.C. The amygdala theory of autism. Neuroscience & Biobehavioral Reviews 2000, 24:355-364.
12. Understanding other minds: Perspectives from autism 1993, Oxford University Press, Oxford, UK. S. Baron-Cohen, H. Tager-Flusberg, D. Cohen (Eds.).
13. Batty M., Taylor M.J. Early processing of the six basic facial emotional expressions. Cognitive Brain Research 2003, 17:613-620.
14. Batty M., Taylor M.J. The development of emotional face processing during childhood. Developmental Science 2006, 9:207-220.
15. Behrmann M., Thomas C., Humphreys K. Seeing it differently: Visual processing in autism. Trends in Cognitive Sciences 2006, 10:258-264.
16. Bentin S., Allison T., Puce A., Perez E., McCarthy G. Electrophysiological studies of face perception in humans. Journal of Cognitive Neuroscience 1996, 8:551-565.
17. Bertone A., Mottron L., Jelenic P., Faubert J. Enhanced and diminished visuo-spatial information processing in autism depends on stimulus complexity. Brain 2005, 128:2430-2441.
18. Bonilha L., Cendes F., Rorden C., Eckert M., Dalgalarrondo P., Li L.M., et al. Gray and white matter imbalance--Typical structural abnormality underlying classic autism. Brain and Development 2008, 30:396-401.
19. Boraston Z., Blakemore S.J. The application of eye-tracking technology in the study of autism. Journal of Physiology 2007, 581:893-898.
20. Boucher J., Lewis V., Collis G. Familiar face and voice matching and recognition in children with autism. Journal of Child Psychology and Psychiatry and Allied Disciplines 1998, 39:171-181.
21. Breiter H.C., Etcoff N.L., Whalen P.J., Kennedy W.A., Rauch S.L., Buckner R.L., et al. Response and habituation of the human amygdala during visual processing of facial expression. Neuron 1996, 17:875-887.
22. Bruce V., Young A. Understanding face recognition. British Journal of Psychology 1986, 77:305-327.
23. Bruneau N., Bonnet-Brilhault F., Gomot M., Adrien J.L., Barthelemy C. Cortical auditory processing and communication in children with autism: Electrophysiological/behavioral relations. International Journal of Psychophysiology 2003, 51:17-25.
24. Bruneau N., Roux S., Adrien J.L., Barthelemy C. Auditory associative cortex dysfunction in children with autism: Evidence from late auditory evoked potentials (N1 wave-T complex). Clinical Neurophysiology 1999, 110:1927-1934.
25. Caharel S., Bernard C., Thibaut F., Haouzir S., Di Maggio-Clozel C., Allio G., et al. The effects of familiarity and emotional expression on face processing examined by ERPs in patients with schizophrenia. Schizophrenia Research 2007, 95(1-3):186-196.
26. Caharel S., Courtay N., Bernard C., Lalonde R., Rebai M. Familiarity and emotional expression influence an early stage of face processing: An electrophysiological study. Brain and Cognition 2005, 59:96-100.
27. Campanella S., Quinet P., Bruyer R., Crommelinck M., Guerit J.M. Categorical perception of happiness and fear facial expressions: An ERP study. Journal of Cognitive Neuroscience 2002, 14:210-227.
28. Carper R.A., Moses P., Tigue Z.D., Courchesne E. Cerebral lobes in autism: Early hyperplasia and abnormal age effects. NeuroImage 2002, 16:1038-1051.
29. Celani G., Battacchi M.W., Arcidiacono L. The understanding of the emotional meaning of facial expressions in people with autism. Journal of Autism and Developmental Disorders 1999, 29:57-66.
30. Dalton K.M., Nacewicz B.M., Johnstone T., Schaefer H.S., Gernsbacher M.A., Goldsmith H.H., et al. Gaze fixation and the neural circuitry of face processing in autism. Nature Neuroscience 2005, 8:519-526.
31. Dapretto M., Davies M.S., Pfeifer J.H., Scott A.A., Sigman M., Bookheimer S.Y., et al. Understanding emotions in others: Mirror neuron dysfunction in children with autism spectrum disorders. Nature Neuroscience 2006, 9:28-30.
32. Dawson G., Carver L., Meltzoff A.N., Panagiotides H., McPartland J., Webb S.J. Neural correlates of face and object recognition in young children with autism spectrum disorder, developmental delay, and typical development. Child Development 2002, 73:700-717.
33. Dawson G., Meltzoff A.N., Osterling J., Rinaldi J., Brown E. Children with autism fail to orient to naturally occurring social stimuli. Journal of Autism and Developmental Disorders 1998, 28:479-485.
34. Dawson G., Webb S.J., Carver L., Panagiotides H., McPartland J. Young children with autism show atypical brain responses to fearful versus neutral facial expressions of emotion. Dev Sci 2004, 7:340-359.
35. Dennis T.A., Malone M.M., Chen C.C. Emotional face processing and emotion regulation in children: An ERP study. Developmental Neuropsychology 2009, 34:85-102.
36. Deruelle C., Monin M.A., Gepner B., Tardif C., Rondan C. March). Face processing in children with autism: The role of high spatial frequency information 2001, Paper presented at the eighth annual meeting of the Cognitive Neuroscience Society, New York.
37. Deruelle C., Rondan C., Gepner B., Tardif C. Spatial frequency and face processing in children with autism and Asperger syndrome. Journal of Autism and Developmental Disorders 2004, 34:199-210.
38. Eger E., Jedynak A., Iwaki T., Skrandies W. Rapid extraction of emotional expression: Evidence from evoked potential fields during brief presentation of face stimuli. Neuropsychologia 2003, 41:808-817.
39. Escalona A., Field T., Nadel J., Lundy B. Imitation effects on children with autism. Journal of Autism and Developmental Disorders 2002, 32:141-144.
40. Frith U. Autism: Explaining the enigma 1989, Blackwell, Oxford, UK.
41. Gao X., Maurer D. A happy story: Developmental changes in children's sensitivity to facial expressions of varying intensities. Journal of Experimental Child Psychology 2010, 107:67-86.
42. George N., Evans J., Fiori N., Davidoff J., Renault B. Brain events related to normal and moderately scrambled faces. Cognitive Brain Research 1996, 4:65-76.
43. Gepner B., Deruelle C., Grynfeltt S. Motion and emotion: A novel approach to the study of face processing by young autistic children. Journal of Autism and Developmental Disorders 2001, 31:37-45.
44. Grice S.J., Halit H., Farroni T., Baron-Cohen S., Bolton P., Johnson M.H. Neural correlates of eye-gaze detection in young children with autism. Cortex 2005, 41:342-353.
45. Grice S.J., Spratling M.W., Karmiloff-Smith A., Halit H., Csibra G., de Haan M., et al. Disordered visual processing and oscillatory brain activity in autism and Williams syndrome. NeuroReport 2001, 12:2697-2700.
46. Happe F., Ehlers S., Fletcher P., Frith U., Johansson M., Gillberg C., et al. " Theory of mind" in the brain: Evidence from a PET scan study of Asperger syndrome. NeuroReport 1996, 8:197-201.
47. Haxby J.V., Ungerleider L.G., Horwitz B., Maisog J.M., Rapoport S.I., Grady C.L. Face encoding and recognition in the human brain. Proceedings of the National Academy of Sciences of the United States of America 1996, 93:922-927.
48. Hobson R.P. The autistic child's appraisal of expressions of emotion: A further study. Journal of Child Psychology and Psychiatry and Allied Disciplines 1986, 27:671-680.
49. Hobson R.P. Methodological issues for experiments on autistic individuals' perception and understanding of emotion. Journal of Child Psychology and Psychiatry and Allied Disciplines 1991, 32:1135-1158.
50. Hobson R.P., Lee A. Hello and goodbye: A study of social engagement in autism. Journal of Autism and Developmental Disorders 1998, 28:117-127.
51. Hobson R.P., Ouston J., Lee A. What's in a face The case of autism. British Journal of Psychology 1988, 79:441-453.
52. Hyde K.L., Samson F., Evans A.C., Mottron L. Neuroanatomical differences in brain areas implicated in perceptual and other core features of autism revealed by cortical thickness analysis and voxel-based morphometry. Human Brain Mapping 2010, 31:556-566.
53. Itier R.J., Batty M. Neural bases of eye and gaze processing: The core of social cognition. Neuroscience & Biobehavioral Reviews 2009, 33:843-863.
54. Itier R.J., Taylor M.J. Inversion and contrast polarity reversal affect both encoding and recognition processes of unfamiliar faces: A repetition study using ERPs. NeuroImage 2002, 15:353-372.
55. Itier R.J., Taylor M.J. Face recognition memory and configural processing: A developmental ERP study using upright, inverted, and contrast-reversed faces. Journal of Cognitive Neuroscience 2004, 16:487-502.
56. Jambaque I., Mottron L., Ponsot G., Chiron C. Autism and visual agnosia in a child with right occipital lobectomy. Journal of Neurology, Neurosurgery, and Psychiatry 1998, 65:555-560.
57. Jarrold C., Brock J. To match or not to match? Methodological issues in autism-related research. Journal of Autism and Developmental Disorders 2004, 34:81-86.
58. Jemel B., Mottron L., Dawson M. Impaired face processing in autism: Fact or artifact Journal of Autism and Developmental Disorders 2006, 36:91-106.
59. Jeste S.S., Nelson C.A. Event related potentials in the understanding of autism spectrum disorders: An analytical review. Journal of Autism and Developmental Disorders 2009, 39:495-510.
60. Kanner L. Autistic disturbances of affective contact. The Nervous Child 1943, 2:217-250.
61. Kemper T.L., Bauman M.L. The contribution of neuropathologic studies to the understanding of autism. Neurologic Clinics 1993, 11:175-187.
62. Kleinhans N.M., Johnson L.C., Richards T., Mahurin R., Greenson J., Dawson G., et al. Reduced neural habituation in the amygdala and social impairments in autism spectrum disorders. American Journal of Psychiatry 2009, 166:467-475.
63. Klin A., Sparrow S.S., de Bildt A., Cicchetti D.V., Cohen D.J., Volkmar F.R. A normed study of face recognition in autism and related disorders. Journal of Autism and Developmental Disorders 1999, 29:499-508.
64. Koshino H., Kana R.K., Keller T.A., Cherkassky V.L., Minshew N.J., Just M.A. FMRI investigation of working memory for faces in autism: Visual coding and underconnectivity with frontal areas. Cerebral Cortex 2008, 18:289-300.
65. Lacroix A., Guidetti M., Rogé B., Reilly J. Recognition of emotional and nonemotional facial expressions: A comparison between Williams syndrome and autism. Research in Developmental Disabilities 2009, 30:976-985.
66. Langdell T. Recognition of faces: An approach to the study of autism. Journal of Child Psychology and Psychiatry and Allied Disciplines 1978, 19:255-268.
67. Légé Y., Dague P. Test de vocabulaire en Images 1974, Editions du centre de Psychologie Appliquée, Paris.
68. Linkenkaer-Hansen K., Palva J.M., Sams M., Hietanen J.K., Aronen H.J., Ilmoniemi R.J. Face-selective processing in human extrastriate cortex around 120 ms after stimulus onset revealed by magneto- and electroencephalography. Neuroscience Letters 1998, 253:147-150.
69. Lombardo M.V., Chakrabarti B., Baron-Cohen S. The amygdala in autism: Not adapting to faces?. American Journal of Psychiatry 2009, 166:395-397.
70. Machado C.J., Bachevalier J. Non-human primate models of childhood psychopathology: The promise and the limitations. Journal of Child Psychology and Psychiatry and Allied Disciplines 2003, 44:64-87.
71. McPartland J., Dawson G., Webb S.J., Panagiotides H., Carver L.J. Event-related brain potentials reveal anomalies in temporal processing of faces in autism spectrum disorder. Journal of Child Psychology and Psychiatry and Allied Disciplines 2004, 45:1235-1245.
72. Morris J.S., Frith C.D., Perrett D.I., Rowland D., Young A.W., Calder A.J., et al. A differential neural response in the human amygdala to fearful and happy facial expressions. Nature 1996, 383:812-815.
73. Mottron L., Burack J. Enhanced perceptual functioning in the development of autism. The development of autism: Perspectives from theory and research 2001, 131-148. Lawrence Erlbaum, Mahwah, NJ. J.A. Burack, T. Charman, N. Yirmiya, P.R. Zelazo (Eds.).
74. Munte T.F., Brack M., Grootheer O., Wieringa B.M., Matzke M., Johannes S. Brain potentials reveal the timing of face identity and expression judgments. Neuroscience Research 1998, 30:25-34.
75. O'Connor K., Hamm J.P., Kirk I.J. The neurophysiological correlates of face processing in adults and children with Asperger's syndrome. Brain and Cognition 2005, 59:82-95.
76. O'Connor K., Hamm J.P., Kirk I.J. Neurophysiological responses to face, facial regions, and objects in adults with Asperger's syndrome: An ERP investigation. International Journal of Psychophysiology 2007, 63:283-293.
77. Phillips M.L., Young A.W., Senior C., Brammer M., Andrew C., Calder A.J., et al. A specific neural substrate for perceiving facial expressions of disgust. Nature 1997, 389:495-498.
78. Pierce K., Muller R.A., Ambrose J., Allen G., Courchesne E. Face processing occurs outside the fusiform " face area" in autism: Evidence from functional MRI. Brain 2001, 124:2059-2073.
79. Pizzagalli D., Regard M., Lehmann D. Rapid emotional face processing in the human right and left brain hemispheres: An ERP study. NeuroReport 1999, 10:2691-2698.
80. Pourtois G., Grandjean D., Sander D., Vuilleumier P. Electrophysiological correlates of rapid spatial orienting towards fearful faces. Cerebral Cortex 2004, 14:619-633.
81. Pourtois G., Thut G., Grave de Peralta R., Michel C., Vuilleumier P. Two electrophysiological stages of spatial orienting towards fearful faces: Early temporo-parietal activation preceding gain control in extrastriate visual cortex. NeuroImage 2005, 26:149-163.
82. Puce A., Allison T., Asgari M., Gore J.C., McCarthy G. Differential sensitivity of human visual cortex to faces, letterstrings, and textures: A functional magnetic resonance imaging study. Journal of Neuroscience 1996, 16:5205-5215.
83. Raven J.C., Court J.H., Raven J. Raven's Coloured Progressive Matrices 1990, Oxford Psychologists Press, Oxford, UK.
84. Rossion B., Gauthier I., Tarr M.J., Despland P., Bruyer R., Linotte S., et al. The N170 occipito-temporal component is delayed and enhanced to inverted faces but not to inverted objects: An electrophysiological account of face-specific processes in the human brain. NeuroReport 2000, 11:69-74.
85. Scherf K.S., Luna B., Kimchi R., Minshew N., Behrmann M. Missing the big picture: Impaired development of global shape processing in autism. Autism Research 2008, 1:114-129.
86. Schopler E., Rechler R.J., Rochen Renner B.R. The Childhood Autism Rating Scale 1988, Western Psychological Services, Los Angeles.
87. Schultz R.T., Gauthier I., Klin A., Fulbright R.K., Anderson A.W., Volkmar F., et al. Abnormal ventral temporal cortical activity during face discrimination among individuals with autism and Asperger syndrome [comment]. Archives of General Psychiatry 2000, 57:331-340.
88. Senju A., Tojo Y., Yaguchi K., Hasegawa T. Deviant gaze processing in children with autism: An ERP study. Neuropsychologia 2005, 43:1297-1306.
89. Sergent J., Ohta S., MacDonald B. Functional neuroanatomy of face and object processing: A positron emission tomography study. Brain 1992, 115:15-36.
90. Sigman M.D., Kasari C., Kwon J.H., Yirmiya N. Responses to the negative emotions of others by autistic, mentally retarded, and normal children. Child Development 1992, 63:796-807.
91. Snow M.E., Hertzig M.E., Shapiro T. Expression of emotion in young autistic children. Journal of the American Academy of Child and Adolescent Psychiatry 1987, 26:836-838.
92. Spezio M.L., Adolphs R., Hurley R.S., Piven J. Abnormal use of facial information in high-functioning autism. Journal of Autism and Developmental Disorders 2007, 37:929-939.
93. Sprengelmeyer R., Jentzsch I. Event related potentials and the perception of intensity in facial expressions. Neuropsychologia 2006, 44:2899-2906.
94. Sutherland A., Crewther D.P. Magnocellular visual evoked potential delay with high autism spectrum quotient yields a neural mechanism for altered perception. Brain 2010, 133:2089-2097.
95. Tantam D., Monaghan L., Nicholson H., Stirling J. Autistic children's ability to interpret faces: A research note. Journal of Child Psychology and Psychiatry and Allied Disciplines 1989, 30:623-630.
96. Taylor M.J. Non-spatial attentional effects on P1. Clinical Neurophysiology 2002, 113:1903-1908.
97. Taylor M.J., Batty M., Itier R.J. The faces of development: A review of early face processing over childhood. Journal of Cognitive Neuroscience 2004, 16:1426-1442.
98. Taylor M.J., Edmonds G.E., McCarthy G., Allison T. Eyes first! Eye processing develops before face processing in children. NeuroReport 2001, 12:1671-1676.
99. Taylor M.J., Itier R.J., Allison T., Edmonds G.E. Direction of gaze effects on early face processing: Eyes-only versus full faces. Cognitive Brain Research 2001, 10:333-340.
100. Teunisse J.P., De Gelder B. Do autistics have a generalized face processing deficit. International Journal of Neuroscience 1994, 77:1-10.
101. Utama N.P., Takemoto A., Koike Y., Nakamura K. Phased processing of facial emotion: An ERP study. Neuroscience Research 2009, 64:30-40.
102. Vandenbroucke M.W.G., Scholte H.S., van Engeland H., Lamme V.A.F., Kemner C. A neural substrate for atypical low-level visual processing in autism spectrum disorder. Brain 2008, 131:1013-1024.
103. Webb S.J., Dawson G., Bernier R., Panagiotides H. ERP evidence of atypical face processing in young children with autism. Journal of Autism and Developmental Disorders 2006, 36:881-890.
104. Webb S.J., Jones E.J., Merkle K., Murias M., Greenson J., Richards T., et al. Response to familiar faces, newly familiar faces, and novel faces as assessed by ERPs is intact in adults with autism spectrum disorders. International Journal of Psychophysiology 2010, 77:106-117.
105. Webb, S. J., Merkle, K., Murias, M., Richards, T., Aylward, E., & Dawson, G. (2009). ERP responses differentiate inverted but not upright face processing in adults with ASD. Social Cognitive and Affective Neuroscience, doi: 10.1093/scan/nsp002.
106. Weeks S.J., Hobson R.P. The salience of facial expression for autistic children. Journal of Child Psychology and Psychiatry and Allied Disciplines 1987, 28:137-151.
107. Williams L.M., Liddell B.J., Rathjen J., Brown K.J., Gray J., Phillips M., et al. Mapping the time course of nonconscious and conscious perception of fear: An integration of central and peripheral measures. Human Brain Mapping 2004, 21:64-74.
108. Wong T.K., Fung P.C., Chua S.E., McAlonan G.M. Abnormal spatiotemporal processing of emotional facial expressions in childhood autism: Dipole source analysis of event-related potentials. European Journal of Neuroscience 2008, 28:407-416.
109. Wright B., Clarke N., Jordan J., Young A.W., Clarke P., Miles J., et al. Emotion recognition in faces and the use of visual context in young people with high-functioning autism spectrum disorders. Autism 2008, 12:607-626.
110. Young A.W., Hellawell D.J., Van De Wal C., Johnson M. Facial expression processing after amygdalotomy. Neuropsychologia 1996, 34:31-39.
111. Zilbovicius M., Boddaert N., Belin P., Poline J.B., Remy P., Mangin J.F., et al. Temporal lobe dysfunction in childhood autism: A PET study. American Journal of Psychiatry 2000, 157:1988-1993.
112. Zilbovicius M., Meresse I., Chabane N., Brunelle F., Samson Y., Boddaert N. Autism, the superior temporal sulcus, and social perception. Trends in Neurosciences 2006, 29:359-366.