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Philosophical Transactions of the Royal Society B: Biological Sciences logoLink to Philosophical Transactions of the Royal Society B: Biological Sciences
. 2003 Feb 28;358(1430):325–334. doi: 10.1098/rstb.2002.1203

Does the perception of moving eyes trigger reflexive visual orienting in autism?

John Swettenham 1, Samantha Condie 1, Ruth Campbell 1, Elizabeth Milne 1, Mike Coleman 1
PMCID: PMC1693118  PMID: 12639330

Abstract

Does movement of the eyes in one or another direction function as an automatic attentional cue to a location of interest? Two experiments explored the directional movement of the eyes in a full face for speed of detection of an aftercoming location target in young people with autism and in control participants. Our aim was to investigate whether a low-level perceptual impairment underlies the delay in gaze following characteristic of autism. The participants' task was to detect a target appearing on the left or right of the screen either 100 ms or 800 ms after a face cue appeared with eyes averting to the left or right. Despite instructions to ignore eye-movement in the face cue, people with autism and control adolescents were quicker to detect targets that had been preceded by an eye movement cue congruent with target location compared with targets preceded by an incongruent eye movement cue. The attention shifts are thought to be reflexive because the cue was to be ignored, and because the effect was found even when cue-target duration was short (100 ms). Because (experiment two) the effect persisted even when the face was inverted, it would seem that the direction of movement of eyes can provide a powerful (involuntary) cue to a location.

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Selected References

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  1. Aitken K. J., Trevarthen C. Self/other organization in human psychological development. Dev Psychopathol. 1997 Fall;9(4):653–677. doi: 10.1017/s0954579497001387. [DOI] [PubMed] [Google Scholar]
  2. Atkinson J., Hood B., Wattam-Bell J., Braddick O. Changes in infants' ability to switch visual attention in the first three months of life. Perception. 1992;21(5):643–653. doi: 10.1068/p210643. [DOI] [PubMed] [Google Scholar]
  3. Baird G., Charman T., Baron-Cohen S., Cox A., Swettenham J., Wheelwright S., Drew A. A screening instrument for autism at 18 months of age: a 6-year follow-up study. J Am Acad Child Adolesc Psychiatry. 2000 Jun;39(6):694–702. doi: 10.1097/00004583-200006000-00007. [DOI] [PubMed] [Google Scholar]
  4. Baron-Cohen S., Cox A., Baird G., Swettenham J., Nightingale N., Morgan K., Drew A., Charman T. Psychological markers in the detection of autism in infancy in a large population. Br J Psychiatry. 1996 Feb;168(2):158–163. doi: 10.1192/bjp.168.2.158. [DOI] [PubMed] [Google Scholar]
  5. Campbell R., Heywood C. A., Cowey A., Regard M., Landis T. Sensitivity to eye gaze in prosopagnosic patients and monkeys with superior temporal sulcus ablation. Neuropsychologia. 1990;28(11):1123–1142. doi: 10.1016/0028-3932(90)90050-x. [DOI] [PubMed] [Google Scholar]
  6. Casey B. J., Gordon C. T., Mannheim G. B., Rumsey J. M. Dysfunctional attention in autistic savants. J Clin Exp Neuropsychol. 1993 Nov;15(6):933–946. doi: 10.1080/01688639308402609. [DOI] [PubMed] [Google Scholar]
  7. Charman T., Swettenham J., Baron-Cohen S., Cox A., Baird G., Drew A. Infants with autism: an investigation of empathy, pretend play, joint attention, and imitation. Dev Psychol. 1997 Sep;33(5):781–789. doi: 10.1037//0012-1649.33.5.781. [DOI] [PubMed] [Google Scholar]
  8. Corkum V., Moore C. The origins of joint visual attention in infants. Dev Psychol. 1998 Jan;34(1):28–38. doi: 10.1037/0012-1649.34.1.28. [DOI] [PubMed] [Google Scholar]
  9. Courchesne E., Lincoln A. J., Kilman B. A., Galambos R. Event-related brain potential correlates of the processing of novel visual and auditory information in autism. J Autism Dev Disord. 1985 Mar;15(1):55–76. doi: 10.1007/BF01837899. [DOI] [PubMed] [Google Scholar]
  10. Courchesne E., Townsend J., Akshoomoff N. A., Saitoh O., Yeung-Courchesne R., Lincoln A. J., James H. E., Haas R. H., Schreibman L., Lau L. Impairment in shifting attention in autistic and cerebellar patients. Behav Neurosci. 1994 Oct;108(5):848–865. doi: 10.1037//0735-7044.108.5.848. [DOI] [PubMed] [Google Scholar]
  11. Curcio F. Sensorimotor functioning and communication in mute autistic children. J Autism Child Schizophr. 1978 Sep;8(3):281–292. doi: 10.1007/BF01539631. [DOI] [PubMed] [Google Scholar]
  12. Davies S., Bishop D., Manstead A. S., Tantam D. Face perception in children with autism and Asperger's syndrome. J Child Psychol Psychiatry. 1994 Sep;35(6):1033–1057. doi: 10.1111/j.1469-7610.1994.tb01808.x. [DOI] [PubMed] [Google Scholar]
  13. Emery N. J. The eyes have it: the neuroethology, function and evolution of social gaze. Neurosci Biobehav Rev. 2000 Aug;24(6):581–604. doi: 10.1016/s0149-7634(00)00025-7. [DOI] [PubMed] [Google Scholar]
  14. Farroni Teresa, Csibra Gergely, Simion Francesca, Johnson Mark H. Eye contact detection in humans from birth. Proc Natl Acad Sci U S A. 2002 Jun 24;99(14):9602–9605. doi: 10.1073/pnas.152159999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gilmore R. O., Johnson M. H. Working memory in infancy: six-month-olds' performance on two versions of the oculomotor delayed response task. J Exp Child Psychol. 1995 Jun;59(3):397–418. doi: 10.1006/jecp.1995.1019. [DOI] [PubMed] [Google Scholar]
  16. Grelotti David J., Gauthier Isabel, Schultz Robert T. Social interest and the development of cortical face specialization: what autism teaches us about face processing. Dev Psychobiol. 2002 Apr;40(3):213–225. doi: 10.1002/dev.10028. [DOI] [PubMed] [Google Scholar]
  17. Hietanen J. K. Does your gaze direction and head orientation shift my visual attention? Neuroreport. 1999 Nov 8;10(16):3443–3447. doi: 10.1097/00001756-199911080-00033. [DOI] [PubMed] [Google Scholar]
  18. Kleinke C. L. Gaze and eye contact: a research review. Psychol Bull. 1986 Jul;100(1):78–100. [PubMed] [Google Scholar]
  19. Lambert A. J., Sumich A. L. Spatial orienting controlled without awareness: a semantically based implicit learning effect. Q J Exp Psychol A. 1996 May;49(2):490–518. doi: 10.1080/713755621. [DOI] [PubMed] [Google Scholar]
  20. Landry S. H., Loveland K. A. Communication behaviors in autism and developmental language delay. J Child Psychol Psychiatry. 1988 Sep;29(5):621–634. doi: 10.1111/j.1469-7610.1988.tb01884.x. [DOI] [PubMed] [Google Scholar]
  21. Langdell T. Recognition of faces: an approach to the study of autism. J Child Psychol Psychiatry. 1978 Jul;19(3):255–268. doi: 10.1111/j.1469-7610.1978.tb00468.x. [DOI] [PubMed] [Google Scholar]
  22. Leekam S. R., Hunnisett E., Moore C. Targets and cues: gaze-following in children with autism. J Child Psychol Psychiatry. 1998 Oct;39(7):951–962. [PubMed] [Google Scholar]
  23. Leekam S. R., López B., Moore C. Attention and joint attention in preschool children with autism. Dev Psychol. 2000 Mar;36(2):261–273. doi: 10.1037//0012-1649.36.2.261. [DOI] [PubMed] [Google Scholar]
  24. Lord C. Follow-up of two-year-olds referred for possible autism. J Child Psychol Psychiatry. 1995 Nov;36(8):1365–1382. doi: 10.1111/j.1469-7610.1995.tb01669.x. [DOI] [PubMed] [Google Scholar]
  25. Lord C., Rutter M., Le Couteur A. Autism Diagnostic Interview-Revised: a revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders. J Autism Dev Disord. 1994 Oct;24(5):659–685. doi: 10.1007/BF02172145. [DOI] [PubMed] [Google Scholar]
  26. Loveland K. A., Landry S. H. Joint attention and language in autism and developmental language delay. J Autism Dev Disord. 1986 Sep;16(3):335–349. doi: 10.1007/BF01531663. [DOI] [PubMed] [Google Scholar]
  27. Posner M. I. Orienting of attention. Q J Exp Psychol. 1980 Feb;32(1):3–25. doi: 10.1080/00335558008248231. [DOI] [PubMed] [Google Scholar]
  28. Rincover A., Ducharme J. M. Variables influencing stimulus overselectivity and "tunnel vision" in developmentally delayed children. Am J Ment Defic. 1987 Jan;91(4):422–430. [PubMed] [Google Scholar]
  29. Swettenham J., Baron-Cohen S., Charman T., Cox A., Baird G., Drew A., Rees L., Wheelwright S. The frequency and distribution of spontaneous attention shifts between social and nonsocial stimuli in autistic, typically developing, and nonautistic developmentally delayed infants. J Child Psychol Psychiatry. 1998 Jul;39(5):747–753. [PubMed] [Google Scholar]
  30. Volkmar F. R., Sparrow S. S., Rende R. D., Cohen D. J. Facial perception in autism. J Child Psychol Psychiatry. 1989 Jul;30(4):591–598. doi: 10.1111/j.1469-7610.1989.tb00270.x. [DOI] [PubMed] [Google Scholar]
  31. Vuilleumier P. Perceived gaze direction in faces and spatial attention: a study in patients with parietal damage and unilateral neglect. Neuropsychologia. 2002;40(7):1013–1026. doi: 10.1016/s0028-3932(01)00153-1. [DOI] [PubMed] [Google Scholar]
  32. Wainwright-Sharp J. A., Bryson S. E. Visual orienting deficits in high-functioning people with autism. J Autism Dev Disord. 1993 Mar;23(1):1–13. doi: 10.1007/BF01066415. [DOI] [PubMed] [Google Scholar]
  33. Wainwright J. A., Bryson S. E. Visual-spatial orienting in autism. J Autism Dev Disord. 1996 Aug;26(4):423–438. doi: 10.1007/BF02172827. [DOI] [PubMed] [Google Scholar]

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