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Neuropsychology Review

, Volume 20, Issue 3, pp 290–322 | Cite as

Facial Emotion Recognition in Autism Spectrum Disorders: A Review of Behavioral and Neuroimaging Studies

  • Madeline B. Harms
  • Alex Martin
  • Gregory L. Wallace
Review

Abstract

Behavioral studies of facial emotion recognition (FER) in autism spectrum disorders (ASD) have yielded mixed results. Here we address demographic and experiment-related factors that may account for these inconsistent findings. We also discuss the possibility that compensatory mechanisms might enable some individuals with ASD to perform well on certain types of FER tasks in spite of atypical processing of the stimuli, and difficulties with real-life emotion recognition. Evidence for such mechanisms comes in part from eye-tracking, electrophysiological, and brain imaging studies, which often show abnormal eye gaze patterns, delayed event-related-potential components in response to face stimuli, and anomalous activity in emotion-processing circuitry in ASD, in spite of intact behavioral performance during FER tasks. We suggest that future studies of FER in ASD: 1) incorporate longitudinal (or cross-sectional) designs to examine the developmental trajectory of (or age-related changes in) FER in ASD and 2) employ behavioral and brain imaging paradigms that can identify and characterize compensatory mechanisms or atypical processing styles in these individuals.

Keywords

Autism Face perception Emotion Neuroimaging Eye-tracking Electrophysiology 

Notes

Acknowledgements

This research was supported by the Intramural Research Program of the NIH, National Institute of Mental Health.

Disclosures

The authors declare that no conflicts of interest are associated with the preparation of this article.

References

  1. Adolphs, R., Sears, L., & Piven, J. (2001). Abnormal processing of social information from faces in autism. Journal of Cognitive Neuroscience, 13(2), 232–240.Google Scholar
  2. Akechi, H., Senju, A., Kikuchi, Y., Tojo, Y., Osanai, H., & Hasegawa, T. (2009). Does gaze direction modulate facial expression processing in children with autism spectrum disorder? Child Development, 80(4), 1134–1146.PubMedCrossRefGoogle Scholar
  3. Amaral, D. G., Schumann, C. M., & Nordahl, C. W. (2008). Neuroanatomy of autism. Trends in Neuroscience, 31, 37–45.CrossRefGoogle Scholar
  4. American Psychiatric Association. (2000). The Diagnostic and Statistical Manual of Mental Disorders, 4th Edition, Text Revision (DSM-IV-TR). Washington: Authors.CrossRefGoogle Scholar
  5. Ashwin, C., Chapman, E., Colle, L., & Baron-Cohen, S. (2006). Impaired recognition of negative basic emotions in autism: a test of the amygdala theory. Social Neuroscience, 1(3–4), 349–363.PubMedCrossRefGoogle Scholar
  6. Ashwin, C., Baron-Cohen, S., Wheelwright, S., O'Riordan, M., & Bullmore, E. T. (2007). Differential activation of the amygdala and the 'social brain' during fearful face-processing in Asperger Syndrome. Neuropsychologia, 45(1), 2–14.PubMedCrossRefGoogle Scholar
  7. Babiloni, C., Pizzella, V., Gratta, C. D., Ferretti, A., & Romani, G. L. (2009). Fundamentals of electroencephalography, magnetoencephalography, & functional magnetic resonance imaging. International Review of Neurobiology, 86, 67–80.PubMedCrossRefGoogle Scholar
  8. Bailey, A. J., Braetigam, S., Jousmaki, V., & Swithenby, S. J. (2005). Abnormal activation of face processing systems at early and intermediate latency in individuals with autism spectrum disorder: a magnetoencephalographic study. European Journal of Neuroscience, 21(9), 2575–2585.PubMedCrossRefGoogle Scholar
  9. Bal, E., Harden, E., Lamb, D., Van Hecke, A. V., Denver, J. W., & Porges, S. W. (2010). Emotion recognition in children with autism spectrum disorders: relations to eye gaze and autonomic state. Journal of Autism and Developmental Disorders, 40(3), 358–370.Google Scholar
  10. Baron-Cohen, S., Wheelwright, S., & Joliffe, T. (1997). Is there a “language of the eyes?” Evidence from normal adults, and adults with autism or Asperger syndrome. Visual Cognition, 4(3), 311–331.CrossRefGoogle Scholar
  11. Behrmann, M., Thomas, C., & Humphreys, K. (2006). Seeing it differently: visual processing in autism. Trends in Cognitive Sciences, 10(6), 258–264.PubMedCrossRefGoogle Scholar
  12. Bolte, S., Hubl, D., Feineis-Matthews, S., Prvulovic, D., Dierks, T., & Poustka, F. (2006). Facial affect recognition training in autism: can we animate the fusiform gyrus? Behavioral Neuroscience, 120(1), 211–216.PubMedCrossRefGoogle Scholar
  13. Bookheimer, S. Y., Ting Wang, A., Scott, A., Sigman, M., & Dapretto, M. (2008). Frontal contributions to face processing differences in autism: evidence from fMRI of inverted face processing. Journal of the International Neuropsychological Society, 14, 922–932.PubMedCrossRefGoogle Scholar
  14. Boraston, Z., Blakemore, S. J., Chilvers, R., & Skuse, D. (2007). Impaired sadness recognition is linked to social interaction deficit in autism. Neuropsychologia, 45(7), 1501–1510.PubMedCrossRefGoogle Scholar
  15. Bormann-Kischkel, C., Vilsmeier, M., & Baude, B. (1995). The development of emotional concepts in autism. Journal of Child Psychology and Psychiatry and Allied Disciplines, 36(7), 1243–1259.CrossRefGoogle Scholar
  16. Braverman, M., Fein, D., Lucci, D., & Waterhouse, L. (1989). Affect comprehension in children with pervasive developmental disorders. Journal of Autism and Developmental Disorders, 19(2), 301–316.PubMedCrossRefGoogle Scholar
  17. Buitelaar, J. K., Van der Wees, M., Swaab-Barneveld, H., & Van der Gaag, R. J. (1999). Theory of mind and emotion-recognition functioning in autistic spectrum disorders and in psychiatric control and normal children. Development and Psychopathology, 11(1), 39–58.PubMedCrossRefGoogle Scholar
  18. Burack, J. A., Iarocci, G., Flanagan, T. D., & Bowler, D. M. (2004). On mosaics and melting pots: conceptual considerations of comparison and matching strategies. Journal of Autism and Developmental Disorders, 34(1), 65–73.PubMedCrossRefGoogle Scholar
  19. Capps, L., Yirmiya, N., & Sigman, M. (1992). Understanding of simple and complex emotions in nonretarted children with autism. Journal of Child Psychology and Psychiatry and Allied Disciplines, 33(7), 1169–1182.CrossRefGoogle Scholar
  20. Castelli, F. (2005). Understanding emotions from standardized facial expressions in autism and normal development. Autism, 9(4), 428–449.PubMedCrossRefGoogle Scholar
  21. Celani, G., Battacchi, M. W., & Arcidiacono, L. (1999). The understanding of the emotional meaning of facial expressions in people with autism. Journal of Autism and Developmental Disorders, 29(1), 57–66.PubMedCrossRefGoogle Scholar
  22. Clark, T. F., Winkielman, P., & McIntosh, D. N. (2008). Autism and the extraction of emotion from briefly presented facial expressions: stumbling at the first step of empathy. Emotion, 8(6), 803–809.PubMedCrossRefGoogle Scholar
  23. Clifford, S., Young, R., & Williamson, P. (2007). Assessing the early characteristics of autistic disorder using video analysis. Journal of Autism and Developmental Disorders, 37(2), 301–313.PubMedCrossRefGoogle Scholar
  24. Corbett, B. A., Carmean, V., Ravizza, S., Wendelken, C., Henry, M. L., Carter, C., et al. (2009). A functional and structural study of emotion and face processing in children with autism. Psychiatry Research, 173(3), 196–205.Google Scholar
  25. Corden, B., Chilvers, R., & Skuse, D. (2008). Avoidance of emotionally arousing stimuli predicts social-perceptual impairment in Asperger’s syndrome. Neuropsychologia, 46(1), 137–147.PubMedCrossRefGoogle Scholar
  26. Critchley, H. D., Daly, E. M., Bullmore, E. T., Williams, S. C. R., Van Amelsvoort, T., Robertson, D. M., et al. (2000). The functional neuroanatomy of social behaviour—Changes in cerebral blood flow when people with autistic disorder process facial expressions. Brain, 123, 2203–2212.PubMedCrossRefGoogle Scholar
  27. Dalton, K. M., Nacewicz, B. M., Johnstone, T., Schaefer, H. S., Gernsbacher, M. A., Goldsmith, H. H., et al. (2005). Gaze fixation and the neural circuitry of face processing in autism. Nature Neuroscience, 8, 519–526.PubMedGoogle Scholar
  28. Dapretto, M., Davies, M. S., Pfeifer, J. H., Scott, A. A., Sigman, M., Bookheimer, S. Y., et al. (2006). Understanding emotions in others: mirror neuron dysfunction in children with autism spectrum disorders. Nature Neuroscience, 9(1), 28–30.PubMedCrossRefGoogle Scholar
  29. Davies, S., Bishop, D., Manstead, A. S. R., & Tantam, D. (1994). Face perception in children with autism and Asperger’s syndrome. Journal of Child Psychology and Psychiatry and Allied Disciplines, 35(6), 1033–1057.CrossRefGoogle Scholar
  30. Dawson, G., Meltzoff, A. N., Osterling, J., Rinaldi, J., & Brown, E. (1998). Children with autism fail to orient to naturally occurring social stimuli. Journal of Autism and Developmental Disorders, 28(6), 479–485.PubMedCrossRefGoogle Scholar
  31. Dawson, G., Webb, S. J., Carver, L., Panagiotides, H., & McPartland, J. (2004). Young children with autism show atypical brain responses to fearful versus neutral facial expressions of emotion. Developmental Science, 7(3), 340–359.PubMedCrossRefGoogle Scholar
  32. Deeley, Q., Daly, E. M., Surguladze, S., Page, L., Toal, F., Robertson, D., et al. (2007). An event related functional magnetic resonance imaging study of facial emotion processing in Asperger syndrome. Biological Psychiatry, 62(3), 207–217.PubMedCrossRefGoogle Scholar
  33. Dehaene-Lambertz, G., Hertz-Pannier, L., Dubois, J., Meriaux, S., Roche, A., Sigman, M., et al. (2006). Functional organization of perisylvian activation during presentation of sentences in preverbal infants. Proceedings of the National Academy of Sciences of the United States of America, 103(38), 14240–14245.PubMedCrossRefGoogle Scholar
  34. Dyck, M. J., Piek, J. P., Hay, D., Smith, L., & Hallmayer, J. (2006). Are abilities abnormally interdependent in children with Autism? Journal of Clinical Child & Adolescent Psychology, 35, 20–33.CrossRefGoogle Scholar
  35. Dziobek, I., Fleck, S., Rogers, K., Wolf, O., & Convit, A. (2006). The ‘amygdala theory of autism’ revisited: linking structure to behavior. Neuropsychologia, 44, 1891–99.PubMedCrossRefGoogle Scholar
  36. Dziobek, I., Bahnemann, M., Convit, A., & Heekeren, H. R. (2010). The role of the fusiform-amygdala system in the pathophysiology of autism. Archives of General Psychiatry, 67, 397–405.PubMedCrossRefGoogle Scholar
  37. Ekman, P., & Friesen, W. V. (1971). Constants across cultures in face and emotion. Journal of Personality and Social Psychology, 17(2), 124–129.PubMedCrossRefGoogle Scholar
  38. Fein, D., Lucci, D., Braverman, M., & Waterhouse, L. (1992). Comprehension of affect in context in children with pervasive developmental disorders. Journal of Child Psychology and Psychiatry and Allied Disciplines, 33(7), 1157–1167.CrossRefGoogle Scholar
  39. Feldman, R. S., McGee, G. G., Mann, L., & Strain, P. (1993). Nonverbal affective decoding ability in children with autism and in typical preschoolers. Journal of Early Intervention, 17(4), 341–350.CrossRefGoogle Scholar
  40. Gauthier, I., Klaiman, C., & Schultz, R. T. (2009). Face composite effects reveal abnormal face processing in Autism spectrum disorders. Vision Research, 49(4), 470–478.PubMedCrossRefGoogle Scholar
  41. Gepner, B., Deruelle, C., & Grynfeltt, S. (2001). Motion and emotion: a novel approach to the study of face processing by young autistic children. Journal of Autism and Developmental Disorders, 31(1), 37–45.PubMedCrossRefGoogle Scholar
  42. Golan, O., & Baron-Cohen, S. (2006). Systemizing empathy: teaching adults with Asperger syndrome or high-functioning autism to recognize complex emotions using interactive multimedia. Development and Psychopathology, 18(2), 591–617.PubMedCrossRefGoogle Scholar
  43. Golan, O., Ashwin, E., Granader, Y., McClintock, S., Day, K., Legget, V., et al. (2010). Enhancing emotion recognition in children with autism spectrum conditions: an intervention using animated vehicles with real emotional faces. Journal of Autism and Developmental Disorders, 40, 269–279.PubMedCrossRefGoogle Scholar
  44. Granpeesheh, D., Tarbox, J., & Dixon, D. R. (2009). Applied behavior analytic interventions for children with autism: a description and review of treatment research. Annals of Clinical Psychiatry, 21(3), 162–173.PubMedGoogle Scholar
  45. Greimel, E., Schulte-Ruether, M., Kircher, T., Kamp-Becker, I., Remschmidt, H., Fink, G. R., et al. (2010). Neural mechanisms of empathy in adolescents with autism spectrum disorder and their fathers. NeuroImage, 49(1), 1055–1065.PubMedCrossRefGoogle Scholar
  46. Grelotti, D. J., Gauthier, I., & Schultz, R. T. (2002). Social interest and the development of cortical face specialization: what autism teaches us about face processing. Developmental Psychobiology, 40(3), 213–225.PubMedCrossRefGoogle Scholar
  47. Gross, T. F. (2004). The perception of four basic emotions in human and nonhuman faces by children with autism and other developmental disabilities. Journal of Abnormal Child Psychology, 32(5), 469–480.PubMedCrossRefGoogle Scholar
  48. Gross, T. F. (2008). Recognition of immaturity and emotional expressions in blended faces by children with autism and other developmental disabilities. Journal of Autism and Developmental Disorders, 38(2), 297–311.PubMedCrossRefGoogle Scholar
  49. Grossman, R. B., & Tager-Flusberg, H. (2008). Reading faces for information about words and emotions in adolescents with autism. Research in Autism Spectrum Disorders, 2(4), 681–695.Google Scholar
  50. Grossman, J. B., Klin, A., Carter, A. S., & Volkmar, F. R. (2000). Verbal bias in recognition of facial emotions in children with Asperger syndrome. Journal of Child Psychology and Psychiatry and Allied Disciplines, 41(3), 369–379.CrossRefGoogle Scholar
  51. Hadjikhani, N., Joseph, R. M., Snyder, J., Chabris, C. F., Clark, J., Steele, S., et al. (2004). Activation of the fusiform gyrus when individuals with autism spectrum disorder view faces. Neuroimage, 22(3), 1141–1150.PubMedCrossRefGoogle Scholar
  52. Hadjikhani, N., Joseph, R. M., Snyder, J., & Tager-Flusber, H. (2007). Abnormal activation of the social brain during face perception in autism. Human Brain Mapping, 28(5), 441–449.PubMedCrossRefGoogle Scholar
  53. Hall, G. B. C., Szechtman, H., & Nahmias, C. (2003). Enhanced salience and emotion recognition in autism: a PET study. American Journal of Psychiatry, 160(8), 1439–1441.PubMedCrossRefGoogle Scholar
  54. Haxby, J. V., Hoffman, E. A., & Gobbini, M. I. (2000). The distributed human neural system for face perception. Trends in Cognitive Sciences, 4(6), 223–233.PubMedCrossRefGoogle Scholar
  55. Herba, C., & Phillips, M. (2004). Annotation: development of facial expression recognition from childhood to adolescence: behavioural and neurological perspectives. Journal of Child Psychology and Psychiatry, 45(7), 1185–1198.PubMedCrossRefGoogle Scholar
  56. Hernandez, N., Metzger, A., Magne, R., Bonnet-Brilhault, F., Roux, S., Barthelemy, C., et al. (2009). Exploration of core features of a human face by healthy and autistic adults analyzed by visual scanning. Neuropsychologia, 47(4), 1004–1012.PubMedCrossRefGoogle Scholar
  57. Hobson, R. P. (1986). The autistic child's appraisal of expressions of emotion. Journal of Child Psychology and Psychiatry and Allied Disciplines, 27(3), 321–342.CrossRefGoogle Scholar
  58. Homer, M., & Rutherford, M. D. (2008). Individuals with autism can categorize facial expressions. Child Neuropsychology, 14(5), 419–437.PubMedCrossRefGoogle Scholar
  59. Howard, M. A., Cowell, P. E., Boucher, J., Broks, P., Mayes, A., Farrant, A., et al. (2000). Convergent neuroanatomical and behavioural evidence of an amygdala hypothesis of autism. Neuroreport, 11(13), 2931–2935.PubMedCrossRefGoogle Scholar
  60. Hubert, B. E., Wicker, B., Monfardini, E., & Deruelle, C. (2009). Electrodermal reactivity to emotion processing in adults with autistic spectrum disorders. Autism, 13(1), 9–19.PubMedCrossRefGoogle Scholar
  61. Hubl, D., Bolte, S., Feineis-Matthews, S., Lanfermann, H., Federspiel, A., Strik, W., et al. (2003). Functional imbalance of visual pathways indicates alternative face processing strategies in autism. Neurology, 61, 1232–37.PubMedGoogle Scholar
  62. Humphreys, K., Minshew, N., Leonard, G. L., & Behrmann, M. (2007). A fine-grained analysis of facial expression processing in high-functioning adults with autism. Neuropsychologia, 45(4), 685–695.PubMedCrossRefGoogle Scholar
  63. Kanner, L. (1943). Autistic disturbances of affective contact. Nervous Child, 2, 217–250.Google Scholar
  64. Katsyri, J., Saalasti, S., Tiippana, K., von Wendt, L., & Sams, M. (2008). Impaired recognition of facial emotions from low-spatial frequencies in Asperger syndrome. Neuropsychologia, 46(7), 1888–1897.PubMedCrossRefGoogle Scholar
  65. Keehn, B., Brenner, L. A., Ramos, A. I., Lincoln, A. J., Marshall, S. P., & Muller, R. A. (2009). Brief report: eye-movement patterns during an embedded figures test in children with ASD. Journal of Autism and Developmental Disorders, 39(2), 383–387.PubMedCrossRefGoogle Scholar
  66. Killgore, W. D., & Yurgelun-Todd, D. A. (2010). Cerebral correlates of amygdala responses during non-conscious perception of facial affect in adolescent and pre-adolescent children. Cognitive Neuroscience, 1(1), 33–43.PubMedCrossRefGoogle Scholar
  67. Kleinhans, N. M., Richards, T., Sterling, L., Stegbauer, K. C., Mahurin, R., Johnson, L. C., et al. (2008). Abnormal functional connectivity in autism spectrum disorders during face processing. Brain, 131, 1000–1012.PubMedCrossRefGoogle Scholar
  68. Kuusikko, S., Haapsamo, H., Jansson-Verkasalo, E., Hurtig, T., Mattila, M., Ebeling, H., et al. (2009). Emotion recognition in children and adolescents with autism spectrum disorders. Journal of Autism and Developmental Disorders, 39, 938–945.PubMedCrossRefGoogle Scholar
  69. Law Smith, M. J., Montagne, B., Perrett, M. G., & Gallagher, L. (2010). Detecting subtle facial emotion recognition deficits in high-functioning autism using dynamic stimuli of varying intensities. Neuropsychologia. In press.Google Scholar
  70. Leppanen, J. M., & Nelson, C. A. (2006). The development and neural bases of facial emotion recognition. Advances in Child Development and Behavior, 34, 207–246.PubMedGoogle Scholar
  71. Lindner, J. L., & Rosen, L. A. (2006). Decoding of emotion through facial expression, prosody and verbal content in children and adolescents with Asperger's syndrome. Journal of Autism and Developmental Disorders, 36(6), 769–777.PubMedCrossRefGoogle Scholar
  72. Loveland, K. A., TunaliKotoski, B., Chen, Y. R., Ortegon, J., Pearson, D. A., Brelsford, K. A., et al. (1997). Emotion recognition in autism: verbal and nonverbal information. Development and Psychopathology, 9(3), 579–593.PubMedCrossRefGoogle Scholar
  73. Loveland, K. A., Steinberg, J. L., Pearson, D. A., Mansour, R., & Reddoch, S. (2008). Judgments of auditory-visual affective congruence in adolescents with and without autism: a pilot study of a new task using fMRI. Perceptual and Motor Skills, 107(2), 557–575.PubMedCrossRefGoogle Scholar
  74. Macdonald, H., Rutter, M., Howlin, P., Rios, P., Leconteur, A., Evered, C., et al. (1989). Recognition and expression of emotional cues by autistic and normal adults. Journal of Child Psychology and Psychiatry and Allied Disciplines, 30(6), 865–877.CrossRefGoogle Scholar
  75. Mazefsky, C. A., & Oswald, D. P. (2007). Emotion perception in Asperger’s syndrome and high-functioning autism: the importance of diagnostic criteria and cue intensity. Journal of Autism and Developmental Disorders, 37, 1086–1095.PubMedCrossRefGoogle Scholar
  76. Miller, G. A., & Chapman, J. P. (2001). Misunderstanding analysis of covariance. Journal of Abnormal Psychology, 110(1), 40–48.PubMedCrossRefGoogle Scholar
  77. Monk, C. S., Weng, S., Wiggins, J. L., Kurapati, N., Louro, H. M. C., Carrasco, M., et al. (2010). Neural circuitry of emotional face processing in autism spectrum disorders. Journal of Psychiatry and Neuroscience, 35(2), 105–14.PubMedCrossRefGoogle Scholar
  78. Morris, J. S., Ohman, A., & Dolan, R. J. (1998). Conscious and unconscious emotional learning in the human amygdala. Nature, 393(6684), 467–470.PubMedCrossRefGoogle Scholar
  79. Mundy, P., Sigman, M., & Kasari, C. (1994). Joint attention, developmental level, and symptom presentation in autism. Development and Psychopathology, 6(3), 389–401.CrossRefGoogle Scholar
  80. Munson, J., Dawson, G., Abbott, R., Faja, S., Webb, S. J., Friedman, S. D., et al. (2006). Amygdalar volume and behavioral development in autism. Archives of General Psychiatry, 63(6), 686–693.PubMedCrossRefGoogle Scholar
  81. Neumann, D., Spezio, M. L., Piven, J., & Adolphs, R. (2006). Looking you in the mouth: abnormal gaze in autism resulting from impaired top-down modulation of visual attention. Social Cognitive and Affective Neuroscience, 1, 194–202.PubMedCrossRefGoogle Scholar
  82. O'Connor, K., Hamm, J. P., & Kirk, I. J. (2005). The neurophysiological correlates of face processing in adults and children with Asperger's syndrome. Brain and Cognition, 59(1), 82–95.PubMedCrossRefGoogle Scholar
  83. Ogai, M., Matsumoto, H., Suzuki, K., Ozawa, F., Fukuda, R., Uchiyama, I., et al. (2003). fMRI study of recognition of facial expressions in high-functioning autistic patients. Neuroreport, 14(4), 559–563.PubMedCrossRefGoogle Scholar
  84. Ozonoff, S., Pennington, B. F., & Rogers, S. J. (1990). Are there emotion perception deficits in young autistic children. Journal of Child Psychology and Psychiatry and Allied Disciplines, 31(3), 343–361.CrossRefGoogle Scholar
  85. Pelphrey, K. A., Sasson, N. J., Reznick, J. S., Paul, G., Goldman, B. D., & Piven, J. (2002). Visual scanning of faces in autism. Journal of Autism and Developmental Disorders, 32(4), 249–261.PubMedCrossRefGoogle Scholar
  86. Pelphrey, K. A., Morris, J. P., McCarthy, G., & Labar, K. S. (2007). Perception of dynamic changes in facial affect and identity in autism. Social Cognitive and Affective Neuroscience, 2(2), 140–149.PubMedCrossRefGoogle Scholar
  87. Philip, R. C. M., Whalley, H. C., Stanfield, A. C., Sprengelmeyer, R., Santos, I. M., Young, A. W., et al. (2010). Deficits in facial, body movement, and vocal emotional processing in autism spectrum disorders. Psychological Medicine.Google Scholar
  88. Pierce, K., & Redcay, E. (2008). Fusiform function in children with an autism spectrum disorder is a matter of “who.”. Biological Psychiatry, 64, 552–560.PubMedCrossRefGoogle Scholar
  89. Pierce, K., Muller, R. A., Ambrose, J., Allen, G., & Courchesne, E. (2001). Face processing occurs outside the fusiform ‘face area’ in autism: evidence from functional MRI. Brain, 124, 2059–2073.PubMedCrossRefGoogle Scholar
  90. Pierce, K., Haist, F., Sedaghat, F., & Courchesne, E. (2004). The brain response to personally familiar faces in autism: findings of fusiform activity and beyond. Brain, 127, 2703–2716.PubMedCrossRefGoogle Scholar
  91. Piggot, J., Kwon, H., Mobbs, D., Blasey, C., Lotspeich, L., Menon, V., et al. (2004). Emotional attribution in high-functioning individuals with autistic spectrum disorder: a functional imaging study. Journal of the American Academy of Child and Adolescent Psychiatry, 43(4), 473–480.PubMedCrossRefGoogle Scholar
  92. Prior, M., Dahlstrom, B., & Squires, T. L. (1990). Autistic children's knowledge of thinking and feeling states in other people. Journal of Child Psychology and Psychiatry and Allied Disciplines, 31(4), 587–601.CrossRefGoogle Scholar
  93. Proposed revision: APA DSM-5. 299.00 (2010). Autistic Disorder. Retrieved from http://www.dsm5.org/ProposedRevisions/Pages/proposedrevision.aspx?rid=94#.
  94. Riby, D. M., Doherty-Sneddon, G., & Bruce, V. (2008). Exploring face perception in disorders of development: Evidence from Williams syndrome and autism. Journal of Neuropsychology, 2, 47–64.PubMedCrossRefGoogle Scholar
  95. Robel, L., Ennouri, K., Piana, H. N., Vaivre-Douret, L., Perier, A., Flament, M. F., et al. (2004). Discrimination of face identities and expressions in children with autism: Same or different? European Child & Adolescent Psychiatry, 13(4), 227–233.CrossRefGoogle Scholar
  96. Rosset, D. B., Rondan, C., Da Fonseca, D., Santos, A., Assouline, B., & Deruelle, C. (2008). Typical emotion processing for cartoon but not for real faces in children with autistic spectrum disorders. Journal of Autism and Developmental Disorders, 38(5), 919–925.PubMedCrossRefGoogle Scholar
  97. Rump, K. M., Giovannelli, J. L., Minshew, N. J., & Strauss, M. S. (2009). The development of emotion recognition in individuals with autism. Child Development, 80(5), 1434–1447.PubMedCrossRefGoogle Scholar
  98. Russell, J. A., & Widen, S. C. (2002). A label superiority effect in children's categorization of facial expressions. Social Development, 11(1), 30–52.CrossRefGoogle Scholar
  99. Rutherford, M. D., & McIntosh, D. N. (2007). Rules versus prototype matching: Strategies of perception of emotional facial expressions in the autism spectrum. Journal of Autism and Developmental Disorders, 37(2), 187–196.PubMedCrossRefGoogle Scholar
  100. Rutherford, M. D., & Towns, A. M. (2008). Scan path differences and similarities during emotion perception in those with and without autism spectrum disorders. Journal of Autism and Developmental Disorders, 38(7), 1371–1381.PubMedCrossRefGoogle Scholar
  101. Schultz, R. T. (2005). Developmental deficits in social perception in autism: the role of the amygdala and fusiform face area. International Journal of Developmental Neuroscience, 23, 125–141.PubMedCrossRefGoogle Scholar
  102. Schultz, R. T., Gauthier, I., Klin, A., Fulbright, R. K., Anderson, A. W., Volkmar, F., et al. (2000). Abnormal ventral temporal cortical activity during face discrimination among individuals with autism and asperger syndrome. Archives of General Psychiatry, 57(4), 331–40.PubMedCrossRefGoogle Scholar
  103. Schumann, C. M., Hamstra, J., Goodlin-Jones, B. L., Lotspeich, L. J., Kwon, H., Buonocore, M. H., et al. (2004). The amygdala is enlarged in children but not adolescents with autism; The hippocampus is enlarged at all ages. Journal of Neuroscience, 24(28), 6392–6401.PubMedCrossRefGoogle Scholar
  104. Schumann, C. M., Barnes, C. C., Lord, C., & Courchesne, E. (2009). Amygdala enlargement in toddlers with autism related to severity of social and communication impairments. Biological Psychiatry, 66(10), 942–949.PubMedCrossRefGoogle Scholar
  105. Senju, A., Southgate, V., White, S., & Frith, U. (2009). Mindblind eyes: An absence of spontaneous theory of mind in Asperger syndrome. Science, 325(5942), 883–885.PubMedCrossRefGoogle Scholar
  106. Shah, A., & Frith, U. (1993). Why do autistic individuals show superior performance on the block design task. Journal of Child Psychology and Psychiatry and Allied Disciplines, 34(8), 1351–1364.CrossRefGoogle Scholar
  107. Smith, C. D., Lori, N. F., Akbudak, E., Sorar, E., Gultepe, E., Shimony, J. S., et al. (2009). MRI diffusion tensor tracking of a new amygdalo-fusiform and hippocampo-fusiform pathway system in humans. Journal of Magnetic Resonance Imaging, 29(6), 1248–1261.PubMedCrossRefGoogle Scholar
  108. Spezio, M. L., Adolphs, R., Hurley, R. S. E., & Piven, J. (2007a). Abnormal use of facial information in high-functioning autism. Journal of Autism and Developmental Disorders, 37, 929–939.PubMedCrossRefGoogle Scholar
  109. Spezio, M. L., Adolphs, R., Hurley, R. S. E., & Piven, J. (2007b). Analysis of face gaze in autism using “Bubbles. Neuropsychologia, 45, 144–151.PubMedCrossRefGoogle Scholar
  110. Tantam, D., Monaghan, L., Nicholson, H., & Stirling, J. (1989). Autistic children's ability to interpret faces-a research note. Journal of Child Psychology and Psychiatry and Allied Disciplines, 30(4), 623–630.CrossRefGoogle Scholar
  111. Tardif, C., Laine, F., Rodriguez, M., & Gepner, B. (2007). Slowing down presentation of facial movements and vocal sounds enhances facial expression recognition and induces facial-vocal imitation in children with autism. Journal of Autism and Developmental Disorders, 37(8), 1469–84.PubMedCrossRefGoogle Scholar
  112. Teunisse, J. P., & de Gelder, B. (2001). Impaired categorical perception of facial expressions in high-functioning adolescents with autism. Child Neuropsychology, 7(1), 1–14.PubMedGoogle Scholar
  113. Thomas, L. A., De Bellis, M. D., Graham, R., & LaBar, K. S. (2007). Development of emotional facial recognition in late childhood and adolescence. Developmental Science, 10(5), 547–558.PubMedCrossRefGoogle Scholar
  114. Vicari, S., Reilly, J. S., Pasqualetti, P., Vizzotto, A., & Caltagirone, C. (2000). Recognition of facial expressions of emotions in school-age children: the intersection of perceptual and semantic categories. Acta Paediatrica, 89(7), 836–845.PubMedCrossRefGoogle Scholar
  115. Wallace, S., Coleman, M., & Bailey, A. (2008). An investigation of basic facial expression recognition in autism spectrum disorders. Cognition & Emotion, 22(7), 1353–1380.CrossRefGoogle Scholar
  116. Wang, A. T., Dapretto, M., Hariri, A. R., Sigman, M., & Bookheimer, S. Y. (2004). Neural correlates of facial affect processing in children and adolescents with autism spectrum disorder. Journal of the American Academy of Child and Adolescent Psychiatry, 43(4), 481–490.PubMedCrossRefGoogle Scholar
  117. Whalen, R. J., Rauch, S. L., Etcoff, N. L., McInerney, S. C., Lee, M. B., & Jenide, M. A. (1998). Masked presentations of emotional facial expressions modulate amygdala activity without explicit knowledge. Journal of Neuroscience, 18(1), 411–418.PubMedGoogle Scholar
  118. Wicker, B., Fonlupt, P., Hubert, B., Tardif, C., Gepner, B., & Deruelle, C. (2008). Abnormal cerebral effective connectivity during explicit emotional processing in adults with autism spectrum disorder. Social Cognitive and Affective Neuroscience, 3(2), 135–143.PubMedCrossRefGoogle Scholar
  119. Wishart, J. G., Cebula, K. R., Willis, D. S., & Pitcairn, T. K. (2007). Understanding of facial expressions of emotion by children with intellectual disabilities of differing aetiology. Journal of Intellectual Disability Research, 51, 551–563.PubMedCrossRefGoogle Scholar
  120. Wong, T. K. W., Fung, P. C. W., Chua, S. E., & McAlonan, G. M. (2008). Abnormal spatiotemporal processing of emotional facial expressions in childhood autism: dipole source analysis of event-related potentials. European Journal of Neuroscience, 28(2), 407–416.PubMedCrossRefGoogle Scholar
  121. Wright, B., Clarke, N., Jordan, J., Young, A. W., Clarke, P., Miles, J., et al. (2008). Emotion recognition in faces and the use of visual context in young people with high-functioning autism spectrum disorders. Autism, 12(6), 607–626.PubMedCrossRefGoogle Scholar

Copyright information

© US Government 2010

Authors and Affiliations

  • Madeline B. Harms
    • 1
  • Alex Martin
    • 1
  • Gregory L. Wallace
    • 1
  1. 1.Laboratory of Brain & CognitionNational Institute of Mental HealthBethesdaUSA

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