Looking But Not Seeing: Atypical Visual Scanning and Recognition of Faces in 2 and 4-Year-Old Children with Autism Spectrum Disorder

Original Paper

Abstract

This study used eye-tracking to examine visual scanning and recognition of faces by 2- and 4-year-old children with autism spectrum disorder (ASD) (N = 44) and typically developing (TD) controls (N = 30). TD toddlers at both age levels scanned and recognized faces similarly. Toddlers with ASD looked increasingly away from faces with age, atypically attended to key features of faces, and were impaired in face recognition. Deficits in recognition were associated with imbalanced attention between key facial features. This study illustrates that face processing in ASD may be affected early and become further compromised with age. We propose that deficits in face processing likely impact the effectiveness of toddlers with ASD as social partners and thus should be targeted for intervention.

Keywords

Autism ASD Face scanning Face recognition Toddlers 

References

  1. American Psychiatric Association. (1994). Diagnostic and statistical manual of mental disorders (4th ed.). Washington DC: American Psychiatric Association.Google Scholar
  2. Blair, R. J. R., Frith, U., Smith, N., Abell, F., & Cipolotti, L. (2002). Fractionation of visual memory: agency detection and its impairment in autism. Neuropsychologia, 40(1), 108–118.CrossRefPubMedGoogle Scholar
  3. Boraston, Z., Corden, B., Miles, L., Skuse, D., & Blakemore, S. (2008). Brief report: Perception of genuine and posed smiles by individuals with autism. Journal of Autism and Developmental Disorders, 38(3), 574–580.CrossRefPubMedGoogle Scholar
  4. Boucher, J., & Lewis, V. (1992). Unfamiliar face recognition in relatively able autistic children. Journal of Child Psychology and Psychiatry and Allied Disciplines, 33(5), 843–859.CrossRefGoogle Scholar
  5. Chawarska, K., & Volkmar, F. R. (2005). Autism in Infancy and Early Childhood. In: F. Volkmar, R. Paul, A. Klin, D. Cohen (Eds), Handbook of autism and pervasive developmental disorders, Vol. 1: Diagnosis, development, neurobiology, and behavior (3rd ed.).Google Scholar
  6. Chawarska, K., & Volkmar, F. (2007). Impairments in monkey and human face recognition in 2-year-old toddlers with autism spectrum disorder and developmental delay. Developmental Science, 10(2), 266–279.CrossRefPubMedGoogle Scholar
  7. Chawarska, K., Paul, R., Klin, A., Hannigen, S., Dichtel, L. E., & Volkmar, F. (2007). Parental recognition of developmental problems in toddlers with autism spectrum disorders. Journal of Autism and Developmental Disorders, 37(1), 62–73.CrossRefPubMedGoogle Scholar
  8. Chawarska, K., Klin, A., Paul, R., Macari, S., & Volkmar, F. R. (in press). A prospective study of toddlers with ASD: Short-term diagnostic and cognitive outcomes. Journal of Child Psychology and Psychiatry.Google Scholar
  9. Chawarska, K., Shic, F., Bradshaw, J., Macari, S., & Klin, A. (2009a). Atypical face scanning in high-risk infants. Presentation at the international conference of infancy studies, Chicago, IL.Google Scholar
  10. Chawarska, K., Shic, F., & Macari, S. (2009b). Context matters: Development of face scanning strategies infancy, (manuscript in preparation).Google Scholar
  11. Dalton, K. M., Nacewicz, B. M., Johnstone, T., Schaefer, H. S., Gernsbacher, M. A., Goldsmith, H., et al. (2005). Gaze fixation and the neural circuitry of face processing in autism. Nature Neuroscience, 8(4), 519–526.PubMedGoogle Scholar
  12. 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.CrossRefPubMedGoogle Scholar
  13. De Giacomo, A., & Fombonne, E. (1998). Parental recognition of developmental abnormalities in autism. European Child and Adolescent Psychiatry, 7(3), 131–136.CrossRefPubMedGoogle Scholar
  14. Duchowski, A. T. (2003). Eye tracking methodology: Theory and practice (1st ed.). Heidelberg: Springer.Google Scholar
  15. Fantz, R. (1964). Visual experience in infants: Decreased attention familiar patterns relative to novel ones. Science, 146(3644), 668–670.CrossRefPubMedGoogle Scholar
  16. Gallay, M., Baudouin, J.-Y., Durand, K., Lemoine, C., & Lecuyer, R. (2006). Qualitative differences in the exploration of upright and upside-down faces in four-month-old infants: An eye-movement study. Child Development, 77(4), 984–996.CrossRefPubMedGoogle Scholar
  17. Gepner, B., de Gelder, B., & de Schonen, S. (1996). Face processing in autistics: Evidence for a generalized deficit? Child Neuropsychology, 2(2), 123–139.CrossRefGoogle Scholar
  18. Golarai, G., Grill-Spector, K., & Rice, A. L. (2006). Autism and the development of face processing. Clinical Neuroscience Research, 6, 145–160.CrossRefPubMedGoogle Scholar
  19. Gotham, K., Risi, S., Pickles, A., & Lord, C. (2007). The autism diagnostic observation schedule: Revised algorithms for improved diagnostic validity. Journal of Autism and Developmental Disorders, 37(4), 613–627.CrossRefPubMedGoogle Scholar
  20. Hainline, L. (1978). Developmental changes in visual scanning of face and nonface patterns by infants. Journal of Experimental Child Psychology, 25(1), 90–115. Feb 1978.CrossRefPubMedGoogle Scholar
  21. Haith, M. M., Bergman, T., & Moore, M. (1977). Eye contact and face scanning in early infancy. Science, 218, 179–181.Google Scholar
  22. Hayhoe, M., & Ballard, D. (2005). Eye movements in natural behavior. Trends in Cognitive Sciences, 9(4), 188–194.CrossRefPubMedGoogle Scholar
  23. Heisz, J. J., & Shore, D. I. (2008). More efficient scanning for familiar faces. Journal of Vision, 8(1), 1–10.CrossRefPubMedGoogle Scholar
  24. Henderson, J. M. (2003). Human gaze control during real-world scene perception. Trends in Cognitive Sciences, 7(11), 498–504.CrossRefPubMedGoogle Scholar
  25. Henderson, J. M., Williams, C. C., & Falk, R. J. (2005). Eye movements are functional during face learning. Memory & Cognition, 33(1), 98–106.Google Scholar
  26. Jones, W., Carr, K., & Klin, A. (2008). Absence of preferential looking to the eyes of approaching adults predicts level of social disability in 2-year-olds with autism spectrum disorder. Archives of General Psychiatry, 65(8), 946–954.CrossRefPubMedGoogle Scholar
  27. Joseph, R. M., & Tanaka, J. (2003). Holistic and part-based face recognition in children with autism. Journal of Child Psychology and Psychiatry, 44(4), 529–542.CrossRefPubMedGoogle Scholar
  28. Kaplan, P., Werner, J., & Rudy, J. (1990). Habituation, sensitization, and infant visual attention. Advances in infancy research, 6, 61–109.Google Scholar
  29. Klin, A., Sparrow, S. S., de Bildt, A., Cicchetti, D. V., Cohen, D. J., & Volkmar, F. R. (1999). A normed study of face recognition in autism and related disorders. Journal of Autism and Developmental Disorders, 29(6), 499–508.CrossRefPubMedGoogle Scholar
  30. Klin, A., Jones, W., Schultz, R., Volkmar, F., & Cohen, D. (2002). Visual fixation patterns during viewing of naturalistic social situations as predictors of social competence in individuals with autism. Archives of General Psychiatry, 59(9), 809–816.CrossRefPubMedGoogle Scholar
  31. Klin, A., Lin, D., Gorrindo, P., Ramsay, G., & Jones, W. (2009). Two-year-olds with autism orient to non-social contingencies rather than biological motion. Nature, 459(7244), 257–261. doi: 10.1038/nature07868.CrossRefPubMedGoogle Scholar
  32. Langdell, T. (1978). Recognition of faces: An approach to the study of autism. Journal of Child Psychology and Psychiatry, 19, 255–268.CrossRefPubMedGoogle Scholar
  33. López, B., Donnelly, N., Hadwin, J. A., & Leekam, S. R. (2004). Face processing in high-functioning adolescents with autism: Evidence for weak central coherence. Visual Cognition, 11(6), 673–688.CrossRefGoogle Scholar
  34. Lord, C., Risi, S., Lambrecht, L., Cook, E. H., Leventhal, B. L., DiLavore, P. C., et al. (2000). The autism diagnostic observation schedule-generic: A standard measure of social and communication deficits associated with the spectrum of autism. Journal of Autism and Developmental Disorders, 30(3), 205–223.CrossRefPubMedGoogle Scholar
  35. Lundqvist, D., Flykt, A., & Öhman, A. (1998). The Karolinska Directed Emotional Faces—KDEF, CD ROM from Department of Clinical Neuroscience, Psychology section, Karolinska Institutet, ISBN 91-630-7164-9.Google Scholar
  36. Mathworks, Inc. (2004). MATLAB 7.0 (Release 14).Google Scholar
  37. Maurer, D., & Salapatek, P. (1976). Developmental changes in the scanning of faces by young infants. Child Development, 47(2), 523–527.CrossRefPubMedGoogle Scholar
  38. Morgan, K., & Hayne, H. (2006). The effect of encoding time on retention by infants and young children. Infant behavior & development, 29, 599–602.CrossRefGoogle Scholar
  39. Mullen, E. (1995). Mullen scales of early learning (AGS Edition ed.). Circle Pines, MN: American Guidance Serivce, Inc.Google Scholar
  40. 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(3), 194–202.CrossRefPubMedGoogle Scholar
  41. Neurobehavioral Systems. (2005). Presentation. Version 10.1. www.neurobs.com.
  42. Pascalis, O., & de Haan, M. (2003). Recognition memory and novelty preference: What model? Progress in Infancy Research, 3, 95–120.Google Scholar
  43. Paul, R. (2008). Communication development and assessment. In K. Chawarska, A. Klin, & F. Volkmar (Eds.), Autism in infants and toddlers: Diagnosis, assessment and treatment. New York, NY: Guilford Press.Google Scholar
  44. Paul, R., Chawarska, K., Fowler, C., Cicchetti, D., & Volkmar, F. (2007). “Listen my children and you shall hear”: Auditory preferences in toddlers with autism spectrum disorders. Journal of Speech, Language and Hearing Research, 50(5), 1350–1364.CrossRefGoogle Scholar
  45. Pelphrey, K. A., Sasson, N. J., Reznick, J., Paul, G., Goldman, B. D., & Piven, J. (2002). Visual scanning of faces in autism. Journal of Autism and Developmental Disorders, 32(4), 249–261.CrossRefPubMedGoogle Scholar
  46. Pierce, G. L., & Henderson, J. M. (2007). The control of fixation duration during scene perception. Visual Cognition, 15(1), 108–112.Google Scholar
  47. Richards, J. E. (1997). Effects of attention in infants’ preference for briefly exposed visual stimuli in the paired-comparison recognition-memory paradigm. Developmental Psychology, 33, 22–31.CrossRefPubMedGoogle Scholar
  48. Robinson, A. J., & Pascalis, O. (2004). Development of flexible visual recognition memory in human infants. Developmental Science, 7(5), 527–533.CrossRefPubMedGoogle Scholar
  49. Rose, S. A., Gottfried, A. W., Melloy-Carminar, P., & Bridger, W. H. (1981). Familiarity and novelty preference in infant recognition memory: Implications for information processing. Developmental Psychology, 18, 704–713.CrossRefGoogle Scholar
  50. Rutherford, M., & Towns, A. (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. doi: 10.1007/s10803-007-0525-7.CrossRefPubMedGoogle Scholar
  51. Rutter, M., Le Couter, A., & Lord, C. (2003). ADI-R: Autism diagnostic interview-revised. Los Angeles, CA: Western Psychological Services.Google Scholar
  52. SAS Institute Inc. (2004). SAS 9.1.3 Help and Documentation, Cary, NC: SAS Institute Inc., (2000–2004).Google Scholar
  53. 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(2–3), 125–141.CrossRefPubMedGoogle Scholar
  54. Schyns, P. G., Bonnar, L., & Gosselin, F. (2002). Show me the features! Understanding recognition from the use of visual information. Psychological Science, 13(5), 402–409.CrossRefPubMedGoogle Scholar
  55. Sensomotoric Instruments (2005). iView X (TM) RED.Google Scholar
  56. Shic, F. (2008). Computational methods for eye-tracking analysis: Applications to autism. Ph.D. thesis, Yale University.Google Scholar
  57. Shic, F., Chawarska, K., Lin, D., & Scassellati, B. (2007). Measuring context: The gaze patterns of children with autism evaluated from the bottom-up. Development and learning, 2007. ICDL IEEE 6th international conference on. pp. 70–75.Google Scholar
  58. Speer, L. L., Cook, A. E., McMahon, W. M., & Clark, E. (2007). Face processing in children with autism. Autism, 11(3), 265–277.CrossRefPubMedGoogle Scholar
  59. Sterling, L., Dawson, G., Webb, S., Murias, M., Munson, J., Panagiotides, H., et al. (2008). The role of face familiarity in eye tracking of faces by individuals with autism spectrum disorders. Journal of Autism and Developmental Disorders, 38, 166–1675.Google Scholar
  60. van der Geest, J. N., Kemner, C., Verbaten, M. N., & van Engeland, H. (2002). Gaze behavior of children with pervasive developmental disorder toward human faces: A fixation time study. Journal of Child Psychology and Psychiatry and Allied Disciplines, 43(5), 669–678.CrossRefGoogle Scholar
  61. 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
  62. Wolfe, J. M., & Horowitz, T. S. (2004). What attributes guide the deployment of visual attention and how do they do it? Nature Reviews Neuroscience, 5(6), 495–501.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  1. 1.Child Study CenterYale University School of MedicineNew HavenUSA

Personalised recommendations