Journal of Autism and Developmental Disorders

, Volume 43, Issue 11, pp 2536–2548 | Cite as

The Influences of Face Inversion and Facial Expression on Sensitivity to Eye Contact in High-Functioning Adults with Autism Spectrum Disorders

  • Mark D. Vida
  • Daphne Maurer
  • Andrew J. Calder
  • Gillian Rhodes
  • Jennifer A. Walsh
  • Matthew V. Pachai
  • M. D. Rutherford
Original Paper

Abstract

We examined the influences of face inversion and facial expression on sensitivity to eye contact in high-functioning adults with and without an autism spectrum disorder (ASD). Participants judged the direction of gaze of angry, fearful, and neutral faces. In the typical group only, the range of directions of gaze leading to the perception of eye contact (the cone of gaze) was narrower for upright than inverted faces. In both groups, the cone of gaze was wider for angry faces than for fearful or neutral faces. These results suggest that in high-functioning adults with ASD, the perception of eye contact is not tuned to be finer for upright than inverted faces, but that information is nevertheless integrated across expression and gaze direction.

Keywords

Autism Gaze Eye contact Cone of gaze Facial expression Face inversion 

Notes

Acknowledgments

This research was supported by the Australian Research Council (ARC) Centre of Excellence in Cognition and its Disorders (project number CE110001021), an ARC Professorial Fellowship to GR (project number DP0877379), Grant 9797 from the Natural Sciences and Engineering Council of Canada (NSERC) to DM, and an NSERC Vanier Canada Graduate Scholarship (CGS-V) to MV.

References

  1. Adams, R. B., Jr, & Kleck, R. E. (2003). Perceived gaze direction and the processing of facial displays of emotion. Psychological Science, 14, 644–647.PubMedCrossRefGoogle Scholar
  2. Adams, R. B., Jr, & Kleck, R. E. (2005). Effects of direct and averted gaze on facially communicated emotion. Emotion, 5, 3–11.PubMedCrossRefGoogle Scholar
  3. Akechi, H., Senju, A., Kikuchi, Y., Tojo, Y., Osanai, H., & Hasagawa, T. (2009). Does gaze direction modulate facial expression processing in children with autism spectrum disorder? Child Development, 80, 1134–1146.PubMedCrossRefGoogle Scholar
  4. Akechi, H., Senju, A., Kikuchi, Y., Tojo, Y., Osanai, H., & Hasegawa, T. (2010). The effect of gaze direction on the processing of facial expressions in children with autism spectrum disorder: An ERP study. Neuropsychologia, 48, 2841–2851.PubMedCrossRefGoogle Scholar
  5. American Psychiatric Association. (2000). Diagnostic and statistical manual of mental disorders (DSM-IV-TR) (4th ed.). Washington, DC: American Psychiatric Publishing, Inc.Google Scholar
  6. Argyle, M., & Cook, M. (1976). Gaze and mutual gaze. New York: Cambridge University Press.Google Scholar
  7. 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, 2–14.PubMedCrossRefGoogle Scholar
  8. Ashwin, C., Ricciardelli, P., & Baron-Cohen, S. (2009). Positive and negative gaze perception in autism spectrum disorders. Social Neuroscience, 4, 153–164.PubMedCrossRefGoogle Scholar
  9. Ashwin, C., Wheelwright, S., & Baron-Cohen, S. (2006). Finding a face in the crowd: Testing the anger superiority effect in autism. Brain and Cognition, 61, 78–95.PubMedCrossRefGoogle Scholar
  10. Baron-Cohen, S. (1995). The eye direction detector (EDD) and the shared attention mechanism (SAM): Two cases for evolutionary psychology. In C. Moore & P. J. Dunham (Eds.), Joint attention: Its origins and role in development (pp. 41–59). Hillsdale, NJ: Lawrence Erlbaum.Google Scholar
  11. Baron-Cohen, S., Baldwin, D., & Crowson, M. (1997). Do children with autism use the speaker’s direction of gaze (SDG) strategy to crack the code of language? Child Development, 68, 48–57.PubMedCrossRefGoogle Scholar
  12. Baron-Cohen, S., Campbell, R., Karmiloff-Smith, A., Grant, J., & Walker, J. (1995). Are children with autism blind to the mentalistic significance of the eyes? British Journal of Developmental Psychology, 13, 379–398.CrossRefGoogle Scholar
  13. Baron-Cohen, S., & Goodhart, F. (1994). The “seeing leads to knowing” deficit in autism: The Pratt and Bryant probe. British Journal of Developmental Psychology, 12, 397–402.CrossRefGoogle Scholar
  14. Baron-Cohen, S., Ring, H., Wheelwright, S., Bullmore, E., Brammer, M., Simmons, A., et al. (1999). Social intelligence in the normal and autistic brain: An fMRI study. European Journal of Neuroscience, 11, 1891–1898.PubMedCrossRefGoogle Scholar
  15. Baron-Cohen, S., Wheelwright, S., Hill, J., Raste, Y., & Plumb, I. (2001). 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, 42, 241–251.PubMedCrossRefGoogle Scholar
  16. Becker, D. V., Kenrick, D. T., Nueberg, S. L., Blackwell, K. C., & Smith, D. M. (2007). The confounded nature of angry men and happy women. Journal of Personality and Social Psychology, 92, 179–190.PubMedCrossRefGoogle Scholar
  17. Bindemann, M. A., Burton, M., & Langton, S. R. H. (2008). How do eye gaze and expression interact? Visual Cognition, 16, 708–733.CrossRefGoogle Scholar
  18. Blake, R., Turner, L. M., Smoski, M. J., Pozdol, S. L., & Stone, W. L. (2003). Visual recognition of biological motion is impaired in children with autism. Psychological Science, 14, 151–157.PubMedCrossRefGoogle Scholar
  19. Bock, S. W., Dicke, P., & Thier, P. (2008). How precise is gaze following in humans? Vision Research, 48, 946–957.PubMedCrossRefGoogle Scholar
  20. Brainard, D. H. (1997). The psychophysics toolbox. Spatial Vision, 10, 433–436.PubMedCrossRefGoogle Scholar
  21. Calder, A. J., Jenkins, R., Cassel, A., & Clifford, C. W. G. (2008). Visual representation of eye gaze is coded by a non-opponent multichannel system. Journal of Experimental Psychology: General, 137, 244–261.CrossRefGoogle Scholar
  22. Campbell, R., Lawrence, K., Mandy, W., Mitra, C., Jeyakuma, L., & Skuse, D. (2006). Meanings in motion and faces: Developmental associations between the processing of intention from geometrical animations and gaze detection accuracy. Development and Psychopathology, 18, 99–118.PubMedCrossRefGoogle Scholar
  23. Critchley, H. D., Daly, E. M., Bullmore, E. T., Williams, S. C., 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
  24. Dalgaard, P. (2008). Introductory statistics with R. New York: Springer.CrossRefGoogle Scholar
  25. 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
  26. Dratsch, T., Schwartz, C., Yanev, K., Schilbach, L., Vogeley, K., & Bente, G. (2013). Getting a grip on social gaze: Control over others’ gaze helps gaze detection in high-functioning autism. Journal of Autism and Developmental Disorders, 43, 286–300.Google Scholar
  27. Ewbank, M. P., Jennings, C., & Calder, A. (2009). Why are you angry with me? Facial expressions of threat influence perception of gaze direction. Journal of Vision, 9, 1–7.PubMedCrossRefGoogle Scholar
  28. Falck-Ytter, T., & von Hofsten, C. (2011). How special is social looking in ASD? A review. In O. Braddick, J. Atkinson, & G. Innocenti (Eds.), Progress in brain research (Vol. 189, pp. 225–238). Burlington: Academic Press.Google Scholar
  29. Freitag, C. M., Konrad, C., Häberlen, M., Kleser, C., von Gontard, A., Reith, W., et al. (2008). Perception of biological motion in autism spectrum disorders. Neuropsychologia, 46, 1480–1494.PubMedCrossRefGoogle Scholar
  30. Gamer, M., & Hecht, H. (2007). Are you looking at me? Measuring the cone of gaze. Journal of Experimental Psychology: Human Perception and Performance, 33, 705–715.PubMedCrossRefGoogle Scholar
  31. Gamer, M., Hecht, H., Seipp, N., & Hiller, W. (2011). Who is looking at me? The cone of gaze widens in social phobia. Cognition and Emotion, 25, 756–764.PubMedCrossRefGoogle Scholar
  32. Geisler, W. S. (1989). Sequential ideal-observer analysis of visual discriminations. Psychological Review, 96, 267–314.PubMedCrossRefGoogle Scholar
  33. Gepner, B., de Gelder, B., & de Schonen, S. (1996). Face processing in autistics: Evidence for a generalised deficit? Child Neuropsychology, 2, 123–139.CrossRefGoogle Scholar
  34. Gibson, J. T., & Pick, A. D. (1963). Perception of another person’s looking behavior. American Journal of Psychology, 76, 386–394.PubMedCrossRefGoogle Scholar
  35. Graham, R., & LaBar, K. S. (2012). Neurocognitive mechanisms of gaze-expression interactions in face processing and social attention. Neuropsychologia, 50, 553–566.PubMedCrossRefGoogle Scholar
  36. 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, 2931–2935.PubMedCrossRefGoogle Scholar
  37. Jenkins, R., & Langton, S. R. H. (2003). Configural processing in the perception of eye-gaze direction. Perception, 32, 1181–1188.PubMedCrossRefGoogle Scholar
  38. Jones, W. B. A., Carr, K. B. A., & Klin, A. (2008). Absence of preferentially looking to the eyes of approaching adults predicts level of social disability in 2-year-old toddlers with autism spectrum disorder. Archives of General Psychiatry, 65, 946–954.PubMedCrossRefGoogle Scholar
  39. Joseph, R. M., Ehrman, K., McNally, R., & Keehn, B. (2008). Affective response to eye contact and face recognition ability in children with ASD. Journal of the International Neuropsychological Society, 14, 947–955.PubMedCrossRefGoogle Scholar
  40. Kaartinen, M., Puura, K., Mäkelä, T., Rannisto, M., Lemponen, R., Helminen, M., Salmenin, R., Himanen, S., & Hietanen, J. K. (2012). Autonomic arousal to direct gaze correlates with social impairments among children with ASD. Journal of Autism and Developmental Disorders, 42, 1917–1927.Google Scholar
  41. Kendon, A. (1967). Some functions of gaze-direction in social interaction. Acta Psychologica, 26, 22–63.PubMedCrossRefGoogle Scholar
  42. Kleinhans, N. M., Johnson, L. C., Richards, T., Mahurin, R., Greenson, J., Dawson, G., et al. (2009). Reduced neural habituation in the amygdala and social impairments in autism spectrum disorders. American Journal of Psychiatry, 166, 467–475.PubMedCrossRefGoogle Scholar
  43. 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, 809–816.PubMedCrossRefGoogle Scholar
  44. Krysko, K. M., & Rutherford, M. D. (2009). A threat-detection advantage in those with autism spectrum disorders. Brain and Cognition, 69, 472–480.PubMedCrossRefGoogle Scholar
  45. Kyläiinen, A., & Hietanen, J. K. (2006). Skin conductance responses to another person’s gaze in children with autism. Journal of Autism and Developmental Disorders, 36, 517–525.CrossRefGoogle Scholar
  46. Lord, C., & Haith, M. M. (1974). The perception of eye contact. Perception and Psychophysics, 16, 413–416.CrossRefGoogle Scholar
  47. 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, 205–223.PubMedCrossRefGoogle Scholar
  48. Lundqvist, D., & Litton, J. E. (1998). The averaged Karolinska directed emotional faces—AKDEF. AKDEF CD ROM. Stockholm: Psychology section, Karolinska Institutet.Google Scholar
  49. McCullagh, P., & Nelder, J. (1989). Generalized linear models (2nd ed.). Boca Raton, FL: Chapman & Hall/CRC.Google Scholar
  50. Milders, M., Hietanen, J. K., Leppänen, J. M., & Braun, M. (2011). Detection of emotional faces is modulated by the direction of eye gaze. Emotion, 11, 1456–1461.PubMedCrossRefGoogle Scholar
  51. Miyahara, M., Ruffman, T., Fujita, C., & Tsujii, M. (2010). How well can young people with Asperger’s disorder recognize threat and learn about affect in faces? A pilot study. Research in Autism Spectrum Disorders, 4, 242–248.CrossRefGoogle Scholar
  52. Monk, C. S., Weng, S., Wiggins, J. L., Kurapati, N., Louro, H. M. C., Carrasco, M., et al. (2010). Neural circuit of emotional face processing in autism spectrum disorders. Journal of Psychiatry and Neuroscience, 35, 105–114.PubMedCrossRefGoogle Scholar
  53. Peli, E. (1991). Contrast sensitivity function and image discrimination. Journal of the Optical Society of America A, 18, 283–293.CrossRefGoogle Scholar
  54. 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, 249–261.PubMedCrossRefGoogle Scholar
  55. Rhodes, G., Addison, B., Jeffery, L., Ewbank, M., & Calder, A. J. (2012). Facial expressions of threat influence perceived gaze direction in 8-year-olds. Public Library of Science One, 7, e49317.Google Scholar
  56. 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
  57. Schwaninger, A., Lobmaier, J. S., & Fischer, M. H. (2005). The inversion effect on gaze perception reflects processing of component information. Experimental Brain Research, 167, 49–55.CrossRefGoogle Scholar
  58. Senju, A., Kikuchi, Y., Hasegawa, T., Tojo, Y., & Osanai, H. (2008). Is anyone looking at me? Direct gaze detection in children with and without autism. Brain and Cognition, 67, 127–139.PubMedCrossRefGoogle Scholar
  59. Spezio, M. L., Adolphs, R., Hurley, R. S. E., & Piven, J. (2007). Analysis of face gaze in autism with “Bubbles”. Neuropsychologia, 45, 144–151.PubMedCrossRefGoogle Scholar
  60. Symons, L. A., Lee, K., Cedrone, C. C., & Nishimura, M. (2004). What are you looking at? Acuity for triadic eye gaze. Journal of General Psychology, 131, 451–469.PubMedGoogle Scholar
  61. Tjan, B. S., Braje, W. L., Legge, G. E., & Kersten, D. (1995). Human efficiency for recognizing 3-D objects in luminance noise. Vision Research, 35, 3053–3069.PubMedCrossRefGoogle Scholar
  62. Tottenham, N., Tanaka, J. W., Leon, A. C., McCarry, T., Nurse, M., Hare, T. A., et al. (2009). The NimStim set of facial expressions: Judgments from untrained research participants. Psychiatry Research, 168, 242–249.PubMedCrossRefGoogle Scholar
  63. Vida, M. D., & Maurer, D. (2012a). Gradual improvement in fine-grained sensitivity to triadic gaze after 6 years of age. Journal of Experimental Child Psychology, 111, 299–318.PubMedCrossRefGoogle Scholar
  64. Vida, M. D., & Maurer, D. (2012b). The development of fine-grained sensitivity to eye contact after 6 years of age. Journal of Experimental Child Psychology, 112, 243–256.PubMedCrossRefGoogle Scholar
  65. Wallace, S., Coleman, M., Pascalis, O., & Bailey, A. (2006). A study of impaired judgment of eye-gaze direction and related face processing deficits in autism spectrum disorders. Perception, 35, 1651–1664.PubMedCrossRefGoogle Scholar
  66. Watson, A. B., & Pelli, D. G. (1983). QUEST: A Bayesian adaptive psychometric method. Perception and Psychophysics, 33, 113–120.PubMedCrossRefGoogle Scholar
  67. Watt, R., Craven, B., & Quinn, S. (2007). A role for the eyebrows in regulating the visibility of eye gaze direction. The Quarterly Journal of Experimental Psychology, 60, 1169–1177.PubMedCrossRefGoogle Scholar
  68. Webster, S., & Potter, D. D. (2008). Brief report: Eye direction detection improves with development in autism. Journal of Autism and Developmental Disorders, 38, 1184–1186.PubMedCrossRefGoogle Scholar
  69. Webster, S., & Potter, D. D. (2011). Gaze perception develops atypically in children with autism. Child Development Research, Article ID 462389, 1–9.Google Scholar
  70. Weigelt, S., Koldewyn, K., & Kanwisher, N. (2012). Face identity recognition in autism spectrum disorders: A review of behavioural studies. Neuroscience and Biobehavioral Reviews, 36, 1060–1084.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Mark D. Vida
    • 1
  • Daphne Maurer
    • 1
    • 2
  • Andrew J. Calder
    • 2
    • 3
  • Gillian Rhodes
    • 2
  • Jennifer A. Walsh
    • 1
  • Matthew V. Pachai
    • 1
  • M. D. Rutherford
    • 1
    • 2
  1. 1.Department of Psychology, Neuroscience & BehaviourMcMaster UniversityHamiltonCanada
  2. 2.ARC Centre of Excellence in Cognition and its Disorders, School of PsychologyUniversity of Western AustraliaCrawleyAustralia
  3. 3.MRC Cognition and Brain Sciences UnitCambridgeUK

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