Journal of Autism and Developmental Disorders

, Volume 32, Issue 4, pp 249–261 | Cite as

Visual Scanning of Faces in Autism

  • Kevin A. Pelphrey
  • Noah J. Sasson
  • J. Steven Reznick
  • Gregory Paul
  • Barbara D. Goldman
  • Joseph Piven
Article

Abstract

The visual scanpaths of five high-functioning adult autistic males and five adult male controls were recorded using an infrared corneal reflection technique as they viewed photographs of human faces. Analyses of the scanpath data revealed marked differences in the scanpaths of the two groups. The autistic participants viewed nonfeature areas of the faces significantly more often and core feature areas of the faces (i.e., eyes, nose, and mouth) significantly less often than did control participants. Across both groups of participants, scanpaths generally did not differ as a function of the instructions given to the participants (i.e., “Please look at the faces in any manner you wish.” vs. “Please identify the emotions portrayed in these faces.”). Autistic participants showed a deficit in emotion recognition, but this effect was driven primarily by deficits in the recognition of fear. Collectively, these results indicate disorganized processing of face stimuli in autistic individuals and suggest a mechanism that may subserve the social information processing deficits that characterize autism spectrum disorders.

Face processing autism eye movements visual scanpaths social perception 

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REFERENCES

  1. Adolphs, R., Sears L., & Piven, J. (2001). Abnormal processing of social information from faces in autism. Journal of Cognitive Neuroscience, 3, (2), 232–240.Google Scholar
  2. American Psychiatric Association. (1994). Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition. Washington, DC: American Psychiatric Association.Google Scholar
  3. Baird, C., Charman, T., Baron-Cohen, S., Cox, A., Swettenham, J., Wheelwright, S., & Drew, A. (2000). A screening instrument for autism at 18 months of age: a 6-year follow-up study. Journal of the American Academy of Child and Adolescent Psychiatry, 39, 694–702.Google Scholar
  4. Baron-Cohen, S., Cox, A., Baird, G., Swettenham, J., Nightingale, N., Morgan, K., Drew, A., & Charman, T. (1996). Psychological markers in the detection of autism in infancy in a large population. British Journal of Psychiatry, 168, 158–163.Google Scholar
  5. Baron-Cohen, S., Spitz, A., & Cross, P. (1993). Can children with autism recognize surprise? Cognition and Emotion, 7, 507–516.Google Scholar
  6. Baron-Cohen, S., Wheelwright, S., & Jolliffe, T. (1997). Is there are a “language of the eyes”? Evidence from normal adults and adults with autism or Asperger Syndrome. Visual Cognition, 4, 311–332.Google Scholar
  7. Bentin, S., Allison, T., Puce, A., Purez, E., & McCarthy, G. (1996). Electrophysiological studies of face perception in humans. Journal of Cognitive Neuroscience, 8, 551–565.Google Scholar
  8. Boucher, J., & Lewis, V. (1992). Unfamiliar face recognition in relatively able autistic children. Journal of Child Psychology and Psychiatry, 33, 843–859.Google Scholar
  9. Braverman, M., Fein, D., Lucci, D., & Waterhouse, L. (1989). Affect comprehension in children with pervasive developmental disorders. Journal of Autism and Developmental Disorders, 19, 301–315.Google Scholar
  10. Briskman, J., Happé, F., & Frith, U. (2001). Exploring the cognitive phenotype of autism: weak “central coherence” in parents and siblings of children with autism: II. Real-life skills and preferences. Journal of Child Psychology and Psychiatry, 42, (3), 309–316.Google Scholar
  11. Capps, L., Yirmiya, N., & Sigman, M. D. (1992). Understanding of simple and complex emotions in non-retarded children with autism. Journal of Child Psychology and Psychiatry, 33, 1169–1182.Google Scholar
  12. Celani, G., Battacchi, M. W., & Arcidiacono, L. (1999). The understanding of emotional meaning of facial expressions in people with autism. Journal of Autism and Developmental Disorders, 29, 57–66.Google Scholar
  13. Cicone, M., Wapner, W., & Gardner, H. (1980). Sensitivity to emotional expressions and situations in organic patients. Cortex, 16, 145–158.Google Scholar
  14. Cohen, D. J., & Volkmar, F. R. (1997). Handbook of Autism and Pervasive Developmental Disorders. 2nd Ed. New York, NY: John Wiley & Sons.Google Scholar
  15. 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, 35, 1033–1057.Google Scholar
  16. De Gelder, B., Vroomen, J., & van der Heide, L. (1991). Face recognition and lip reading in autism. European Journal of Cognitive Psychology, 3, 69–86.Google Scholar
  17. De Renzi, E., Perani, D., Carlesimo, G. A., Silveri, M. C., & Fazio, F. (1994). Prosopagnosia can be associated with damage confined to the right hemisphere: an MRI and PET study and a review of the literature. Neuropsychologia, 32, 893–902.Google Scholar
  18. Diamond, R., & Carey, S. (1986). Why faces are and are not special: an effect of expertise. Journal of Experimental Psychology, 115, 107–117.Google Scholar
  19. Dolan R. J., Fink G. R., Rolls E., Booth M., Holmes, A., Frackowiak, R. S., & Friston, K. J. (1997). How the brain learns to see objects and faces in an impoverished context. Nature, 389, 596–599.Google Scholar
  20. Ekman, P. (1989). The argument and evidence about universals in facial expressions of emotion. In H. Wagner and A. Manstead (Eds.), Handbook of social psychophysiology (pp. 143–164). Chichester: Wiley.Google Scholar
  21. Ekman, P., & Friesen, W. V. (1976). Pictures of facial affect. Palo Alto, CA: Consulting Psychologists Press.Google Scholar
  22. Ellis, H. D., & Shepard, J. W. (1975). Recognition of upright and inverted faces presented in the left and right visual fields. Cortex, 11, 3–7.Google Scholar
  23. Farah M. J., Wilson, K. D., Drain M., & Tanaka, J. N. (1998). What is special about face perception? Psychological Review, 105, 482–498.Google Scholar
  24. Farah, M. J., (1990). Visual agnosia. Cambridge, MA: MIT Press.Google Scholar
  25. Folstein, S. E., & Rutter, M. L. (1977). Infantile autism: a genetic study of 21 twin pairs. Journal of Child Psychology and Psychiatry, 18, 297–321.Google Scholar
  26. Frith, U. (1989). Autism: Explaining the enigma. Maiden, MA: Blackwell Publishers.Google Scholar
  27. Gauthier, I., & Tarr, M. J. (1997). Becoming a “Greeble” expert: exploring mechanisms for face recognition. Vision Research, 37, 1673–1681.Google Scholar
  28. Goren, C. C., Sarty, M., & Wu, P. Y. (1975). Visual following and pattern discrimination of face-like stimuli by newborn infants. Pediatrics, 56, 544–549.Google Scholar
  29. Happé, F., Briskman, J., & Frith, U. (2001). Exploring the cognitive phenotype of autism: weak “central coherence” in parents and siblings of children with autism: I. Experimental tests. Journal of Child Psychology and Psychiatry, 42, (3), 299–307.Google Scholar
  30. Happé, F. (1999). Autism: Cognitive deficit or cognitive style? Trends in Cognitive Sciences, 3, (6), 216–222.Google Scholar
  31. Happé, F. (1996). Studying weak central coherence at low levels: children with autism do not succumb to visual illusions. A research note. Journal of Child Psychology and Psychiatry and Allied Disciplines, 37, (7), 873–877.Google Scholar
  32. Hauck, M., Fein, D., Maltby, N., Waterhouse, L., & Feinstein, C. (1998). Memory for faces in children with autism. Child Neuropsychology, 4, 187–198.Google Scholar
  33. Haxby, J. V., Ungerleider, L. G., Clark, V. P., Schouten, J. L., Hoffman, E. A., & Martin, A. (1999). The effect of face inversion on activity in human neural systems for face and object perception. Neuron, 22, 189–199.Google Scholar
  34. Hobson, R. P. (1986a). The autistic child's appraisal of expressions of emotion. Journal of Child Psychology and Psychiatry, 27, 321–342.Google Scholar
  35. Hobson, R. P. (1986b). The autistic child's appraisal of expressions of emotion: a further study. Journal of Child Psychology and Psychiatry, 27, 671–680.Google Scholar
  36. Hobson, R. P., Ouston, J., & Lee, A. (1988). Emotion recognition in autism: coordinating faces and voices. Psychological Medicine, 18, 911–923.Google Scholar
  37. Hobson, R. P., Ouston, J., & Lee, A. (1989). Naming emotion in faces and voices: abilities and disabilities in autism and mental retardation. British Journal of Developmental Psychology, 7, 237–250.Google Scholar
  38. Johnson, M. H., & Morton, J. (1991). Biology and cognitive development: The case of face recognition. Oxford: Basil Blackwell.Google Scholar
  39. Johnson, M. S., Dziurawic, H., Ellis, M., & Morton, J. (1991). Newborns’ preferential tracking of face-like stimuli and its subsequent decline. Cognition, 40, 1–19.Google Scholar
  40. Kanner, L. (1943). Autistic disturbances of affective contact. Nervous Child, 2, 217–250.Google Scholar
  41. Kanwisher, N., McDermott, J., & Chun, M. M. (1997). The fusiform face area: a module in human extrastriate cortex specialized for face perception. Journal of Neuroscience, 17, 4302–4311.Google Scholar
  42. Klin, A., Sparrow, S., de Bildt, A., Cicchetti, D., Cohen, D., & Volkmar, F. (1999). A normed study of face recognition in autism and related disorders. Journal of Autism and Developmental Disorders, 29, 499–508.Google Scholar
  43. Langdell, T. (1978). Recognition of faces: an approach to the study of autism. Journal of Child Psychology and Psychiatry, 19, 255–268.Google Scholar
  44. Lord, C., Rutter, M., & Le Couteur, A. (1994). Autism Diagnostic Interview-Revised: a revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders. Journal of Autism and Developmental Disorders, 24, 659–685.Google Scholar
  45. Lord, C., Rutter, M., DiLavore, P., & Risi, S. (1999). Autism Diagnostic Observation Schedule (ADOS). Los Angeles, CA: Western Psychological Services.Google Scholar
  46. Loveland, K., Tunali-Kotoski, B., Chen Y., Ortegon J., Pearson, D., Brelsford, K., & Gibbs, M. (1997). Emotion recognition in autism: verbal and nonverbal information. Development and Psychopathology, 9, 579–593.Google Scholar
  47. Luria, S. M., & Strauss, M. S. (1978). Comparison of eye movements over faces in photographic positives and negatives. Perception and Psychophysics, 2, 547–552.Google Scholar
  48. Mackworth, N. H., & Bruner, J. S. (1970). How adults and children search and recognize pictures. Human Development, 13, 149–177.Google Scholar
  49. Manor, B. R., Gordon, E., Williams, L. M., Rennie, C. J., Bahramali, H., Latimer, C. R., Barry, R. J., & Meares, R. A. (1999). Eye movements reflect impaired face processing in patients with schizophrenia. Biological Psychiatry, 46, 963–969.Google Scholar
  50. Mertens, I., Siegmund, H., & Grusser, O. (1993). Gaze motor asymmetries in the perception of faces during a memory task. Neuropsychologia,31, 989–998.Google Scholar
  51. Morton, J., & Johnson, M. H. (1991). CONSPEC and CONLERN: a two-process theory of infant face recognition. Psychological Review, 98, 164–181.Google Scholar
  52. Mottron, L., Belleville, S., & Menard, E. (1999). Local bias in autistic subjects as evidenced by graphic tasks: perceptual hierarchization or working memory deficit? Journal of Child Psychology and Psychiatry and Allied Disciplines, 40, (5), 743–755.Google Scholar
  53. Mottron L., Burack, J. A., Stauder, J. E. A., & Robaey, P. (1999). Perceptual processing among high-functioning persons with autism. Journal of Child Psychology and Psychiatry and Allied Disciplines Volume 40, (2), 203–211.Google Scholar
  54. Mottron, L., Peretz, I., & Menard, E. (2000). Local and global processing of music in high-functioning persons with autism: beyond central coherence? Journal of Child Psychology and Psychiatry and Allied Disciplines, 41, (8), 1057–1065.Google Scholar
  55. Noton, D., & Stark, L. (1971). Eye movements and visual perception. Scientific American, 224, 35–43.Google Scholar
  56. Osterling, J., & Dawson, G. (1994). Early recognition of children with autism: a study of first birthday home videotapes. Journal of Autism and Developmental Disorders, 24, 247–257.Google Scholar
  57. Ozonoff, S., Pennington, B. F., & Rogers, S. J. (1990). Are there emotional perception deficits in young autistic children? Journal of Child Psychology and Psychiatry, 31, 343–361.Google Scholar
  58. Phillips, M. L., & David, A. S. (1997). Visual scanpaths are abnormal in deluded schizophrenia. Neuropsychologia, 35, 99–105.Google Scholar
  59. Piven, J., & Palmer, P. (1997). Cognitive deficits in parents from multiple-incidence autism families. Journal of Child Psychology and Psychiatry, 38, 1011–1021.Google Scholar
  60. Piven, J., Palmer, P., Landa, R., Santangelo, S., Jacobi, D., & Childress, D. (1997). Personality and language characteristics in parents from multiple-incidence autism families. American Journal of Medical Genetics (Neuropsychiatric Genetics), 74, 398–411.Google Scholar
  61. Piven, J. (2001). The broad autism phenotype: a complementary strategy for molecular genetic studies of autism. American Journal of Medical Genetics (Neuropsychiatric Genetics), 106, 34–35.Google Scholar
  62. Ropar, D., & Mitchell, P. (1999). Are individuals with autism and Asperger's syndrome susceptible to visual illusions? Journal of Child Psychology and Psychiatry and Allied Disciplines 40, (8), 1283–1293.Google Scholar
  63. Sams, M., Hietanen, J. K., Hari, R., Ilmoniemi, J. H., & Lounasmaa, O. V. (1997). Face-specific response from the human inferior occipito-temporal cortex. Neuroscience, 77, 49–55.Google Scholar
  64. Schultz, R. T., Gauthier, I., Klin, A., Fulbright, R., Anderson, A., Volkmar, F., Skudlarski, P., Lacadie, C., Cohen, D. J., & Gore, J. C. (2000). Abnormal ventral temporal cortical activity during face discrimination among individuals with autism and Asperger syndrome. Archives of General Psychiatry, 57, (4) 1–23.Google Scholar
  65. Sergent, J., Ohta, S., & MacDonald, B. (1992). Functional neuroanatomy of face and object processing: a positron emission tomography study. Brain, 115, 15–36.Google Scholar
  66. Streit, M., Wölwer, W., & Gabel, W. (1996). Facial-affect recognition and visual scanning behavior in the course of schizophrenia. Schizophrenia Research, 24, 311–317.Google Scholar
  67. 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, 30, 623–630.Google Scholar
  68. Tarr, M. J., & Bulthoff, H. H. (1998). Image-based object recognition in man, monkey, and machine. Cognition, 67, 1–20.Google Scholar
  69. Valentine, T. (1988). Upside-down faces: a review of the effect of inversion upon face recognition. British Journal of Psychology,79, 471–491.Google Scholar
  70. Volkmar, F. R., Sparrow, S. S., Rende, R. C., & Cohen, D. J. (1989). Facial perception in autism. Journal of Psychological Psychiatry, 30, 591–598.Google Scholar
  71. Walker-Smith, G. J., Gale, A. G., & Findlay, J. M. (1977). Eye movement strategies in face perception. Perception, 6, 313–326.Google Scholar
  72. Wechsler, D. (1981). Wechsler Adult Intelligence Scale-Revised. New York: Harcourt Brace Jovanovich.Google Scholar
  73. Yarbus, A. L. (1967). Eye movements and vision. New York: Plenum Press.Google Scholar

Copyright information

© Plenum Publishing Corporation 2002

Authors and Affiliations

  • Kevin A. Pelphrey
    • 1
    • 2
  • Noah J. Sasson
    • 1
  • J. Steven Reznick
    • 1
  • Gregory Paul
    • 1
  • Barbara D. Goldman
    • 1
  • Joseph Piven
    • 2
  1. 1.Department of PsychologyUniversity of North Carolina atChapel Hill
  2. 2.UNC Neurodevelopmental Disorders Research CenterUniversity of North Carolina atChapel Hill

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