Journal of Autism and Developmental Disorders

, Volume 43, Issue 12, pp 2779–2792 | Cite as

Atypical Gaze Following in Autism: A Comparison of Three Potential Mechanisms

  • K. Gillespie-LynchEmail author
  • R. Elias
  • P. Escudero
  • T. Hutman
  • S. P. Johnson
Original Paper


In order to evaluate the following potential mechanisms underlying atypical gaze following in autism, impaired reflexive gaze following, difficulty integrating gaze and affect, or reduced understanding of the referential significance of gaze, we administered three paradigms to young children with autism (N = 21) and chronological (N = 21) and nonverbal mental age (N = 21) matched controls. Children with autism exhibited impaired reflexive gaze following. The absence of evidence of integration of gaze and affect, regardless of diagnosis, indicates ineffective measurement of this construct. Reduced gaze following was apparent among children with autism during eye-tracking and in-person assessments. Word learning from gaze cues was better explained by developmental level than autism. Thus, gaze following may traverse an atypical, rather than just delayed, trajectory in autism.


Response to joint attention Autism Reflexive gaze following Word learning 



We are very grateful to all of the children and families who participated in our study. We would like to thank Devi Beck-Pancer and Brian Nguyen for their invaluable contributions to stimuli design. We would like to thank the following people for help with data collection and/or coding: Mithi del Rosario, Kia Dela Cruz, Lovella Gomez, Nancy Lê, Jane Lee, Jennifer Nicole Loa, Brigid McCarthy, Christine Park. Connie Kasari provided excellent guidance on study design. This work was supported by National Institutes of Health Grant R01-HD40432 to Scott P. Johnson, NICHD/NIH Autism Centers of Excellence (ACE) Grant Number P50-HD-055784 to Susan Bookheimer, and the FPR-UCLA Center for Culture, Brain and Development. We would also like to thank reviewers for their extremely helpful comments.


  1. Adamson, L. B., & Bakeman, R. (1985). Affect and attention: Infants observed with mothers and peers. Child Development, 56(3), 582–593.CrossRefGoogle Scholar
  2. Akechi, H., Senju, A., Kikuchi, Y., Tojo, Y., Osanai, H., & Hasegawa, T. (2011). Do children with ASD use referential gaze to learn the name of an object? An eye-tracking study. Research in Autism Spectrum Disorders, 5, 1230–1242.CrossRefGoogle Scholar
  3. Baldwin, D. A. (1991). Infants’ contribution to the achievement of joint reference. Child Development, 62, 875–890.PubMedCrossRefGoogle Scholar
  4. Baron-Cohen, S., Baldwin, D. A., & Crowson, M. (1997). Do children with autism use the speaker’s direction of gaze strategy to crack the code of language? Child Development, 68(1), 48–57.PubMedCrossRefGoogle Scholar
  5. Baron-Cohen, S., Leslie, A., & Frith, U. (1985). Does the autistic child have a theory of mind? Cognition, 21, 37–46.PubMedCrossRefGoogle Scholar
  6. Bayliss, A. P., Schuch, S., & Tipper, S. P. (2010). Gaze cueing elicited by emotional faces is influenced by emotional context. Visual Cognition, 18(8), 1214–1232.PubMedCrossRefGoogle Scholar
  7. Bishop, S. L., Guthrie, W., Coffing, M., & Lord, C. (2011). Convergent validity of the Mullen Scales of Early Learning and the differential ability scales in children with autism spectrum disorders. American Journal of Intellectual and Developmental Disabilities, 16(5), 331–343.CrossRefGoogle Scholar
  8. Brodeur, M. S., Dionne-Dostie, E., Montreuil, T., & Lepage, M. (2010). The Bank of Standardized Stimuli (BOSS), a new set of 480 normative photos of objects to be used as visual stimuli in cognitive research. PLoS ONE, 5(5), e10773.PubMedCrossRefGoogle Scholar
  9. Butler, S. C., Caron, A. J., & Brooks, R. (2009). Infant understanding of the referential nature of looking. Journal of Cognition and Development, 1(4), 359–377.CrossRefGoogle Scholar
  10. Butterworth, G., & Jarrett, N. (1991). What minds have in common is space: Spatial mechanisms serving joint visual attention in infancy. British Journal of Developmental Psychology, 9, 55–73.CrossRefGoogle Scholar
  11. Chawarska, K., Klin, A., & Volkmar, F. (2003). Automatic attention cueing through eye movement in 2-year old children with autism. Child Development, 74(4), 1108–1122.PubMedCrossRefGoogle Scholar
  12. Constantino, J. N., & Gruber, C. P. (2002). The social responsiveness scale. Los Angeles: Western Psychological Services.Google Scholar
  13. Corkum, V., & Moore, C. (1998). The origins of joint visual attention in infants. Developmental Psychology, 34(1), 28–38.PubMedCrossRefGoogle Scholar
  14. D’Entremont, B., Hains, S. M. J., & Muir, D. W. (1997). A demonstration of gaze following in 3- to 6-month olds. Infant Behavior and Development, 20(4), 569–572.CrossRefGoogle Scholar
  15. Dawson, G., Bernier, R., & Ring, R. H. (2012). Social attention: A possible early indicator of efficacy in autism clinical trials. Journal of Neurodevelopmental Disorders, 4(1). doi: 10.1186/1866-1955-4-11.
  16. Dawson, G., Toth, K., Abbott, R., Osterling, J., Munson, J., Estes, A., et al. (2004). Early social attention impairments in autism: Social orienting, joint attention, and attention to distress. Developmental Psychology, 40(2), 271–282.PubMedCrossRefGoogle Scholar
  17. de Jong, M. C., van Engeland, H., & Kemner, C. (2008). Attentional effects of gaze shifts are influenced by emotion and spatial frequency, but not in autism. Journal of the American Academy of Child and Adolescent Psychiatry, 47(4), 443–454.PubMedCrossRefGoogle Scholar
  18. Deák, G. O., Flom, R. A., & Pick, A. D. (2000). Effects of gesture and target on 12- and 18-month-olds joint visual attention to objects in front or behind them. Developmental Psychology, 36(4), 511–523.PubMedCrossRefGoogle Scholar
  19. Elliot, C. D. (1990). Differential ability scales. San Antonio, TX: The psychological corporation.Google Scholar
  20. Farroni, T., Massaccesi, S., Pividori, D., & Johnson, M. H. (2004). Gaze following in newborns. Infancy, 5(1), 39–60.CrossRefGoogle Scholar
  21. Friesen, C. K., Halvorson, K. M., & Graham, R. (2011). Emotionally meaningful targets enhance orienting triggered by a fearful face. Cognition and Emotion, 25(1), 73–88.PubMedCrossRefGoogle Scholar
  22. Gergely, G. (2001). The obscure object of desire-‘Nearly, but clearly not, like me’: Contingency preference in normal children versus children with autism. Bulletin of the Menninger Clinic, 65(3: special issue), 411–426.PubMedCrossRefGoogle Scholar
  23. Gernsbacher, M. A., Stevenson, J. L., Khandakar, S., & Goldsmith, H. H. (2008). Why does joint attention look atypical in autism? Child Development Perspectives, 2(1), 38–45.CrossRefGoogle Scholar
  24. Geschwind, D. H. (2009). Advances in autism. Annual Review of Medicine, 60, 367–380.PubMedCrossRefGoogle Scholar
  25. Gillespie-Lynch, K., Sepeta, L., Wang, Y., Marshall, S., Gomez, L., Sigman, M., et al. (2012). Early childhood predictors of the social competence of adults with autism. Journal of Autism and Developmental Disorders, 42(2), 161–174.PubMedCrossRefGoogle Scholar
  26. Gliga, T., Elsabbagh, M., Hudry, K., Charman, T., & Johnson, M. H. (2012). Gaze following, gaze reading, and word learning in children at risk for autism. Child Development, 83(3), 926–938.Google Scholar
  27. Goldberg, M. C., Mostow, A. J., Vecera, S. P., Gidley Larson, J. C., Mostofsky, S. H., Mahone, E. H., et al. (2008). Evidence for impairments in using static line drawings of eye gaze cues to orient visual-spatial attention in children with high functioning autism. Journal of Autism and Developmental Disorders, 38, 1405–1413.PubMedCrossRefGoogle Scholar
  28. Graham, R., Friesen, C. K., Fichtenholtz, H. M., & LaBar, K. S. (2010). Modulation of reflexive orienting to gaze direction by facial expressions. Visual Cognition, 18(3), 331–368.CrossRefGoogle Scholar
  29. Greene, D. J., Colich, N., Iacoboni, M., Zaidel, E., Bookheimer, S. Y., & Dapretto, M. (2011). Atypical neural networks for social orienting in autism spectrum disorders. Neuroimage, 56(1), 354–362.PubMedCrossRefGoogle Scholar
  30. Heitanen, J. K., & Leppänen, J. M. (2003). Does facial expression affect attention orientation by gaze direction cues? Journal of Experimental Psychology, 29(6), 1228–1243.Google Scholar
  31. Hollich, G. J., Hirsh-Pasek, K., Golinkoff, R. M., Brand, R. J., Brown, E., Chung, H. L., et al. (2000). Breaking the language barrier: An emergentist coalition model for the origins of word learning. Monographs of the Society for Research in Child Development, 65(3), 1–135.CrossRefGoogle Scholar
  32. Hood, B. M., Willen, J. D., & Driver, J. (1998). Adult’s eyes trigger shifts of visual attention in young infants. Psychological Science, 9(2), 131–134.CrossRefGoogle Scholar
  33. Johnson, M. H., Griffin, R., Csibra, G., Halit, H., Farroni, T., & Haan, M. (2005). The emergence of the social brain network: Evidence from typical and atypical development. Development and Psychopathology, 17, 599–619.PubMedCrossRefGoogle Scholar
  34. Kasari, C., Sigman, M., Mundy, P., & Yirmiya, N. (1990). Affective sharing in the context of joint attention interactions of normal, autistic, and mentally retarded children. Journal of Autism and Developmental Disorders, 20(1), 87–100.PubMedCrossRefGoogle Scholar
  35. Kelly, D. J., Walker, R., & Norbury, C. F. (2012). Deficits in volitional oculomotor control align with language status in autism spectrum disorders. Developmental Science, 16(1), 56–66.PubMedCrossRefGoogle Scholar
  36. Kuhn, G., Benson, V., Fletcher-Watson, S., Kovshoff, H., McCormick, C. A., Kirkby, J., et al. (2010). Eye movements affirm: Automatic overt gaze cueing effects for typical adults and adults with autism spectrum disorder. Experimental Brain Research, 201, 155–165.CrossRefGoogle Scholar
  37. Kylliainen, A., & Hietanen, J. K. (2004). Attention orienting by another’s gaze direction in children with autism. Journal of Child Psychology and Psychiatry, 45(3), 435–444.PubMedCrossRefGoogle Scholar
  38. Landa, R. J., Holman, K. C., & Garrett-Mayer, E. (2007). Social and communication development in toddlers with early and late diagnosis of autism spectrum disorders. Archives of General Psychiatry, 64(7), 853–864.PubMedCrossRefGoogle Scholar
  39. Leekam, S., Baron-Cohen, S., Perrett, D., Milders, M., & Brown, S. (1997). Eye-direction detection: A dissociation between geometric and joint attention skills in autism. British Journal of Developmental Psychology, 15, 77–95.CrossRefGoogle Scholar
  40. Leekam, S. R., Hunnisett, E., & Moore, C. (1998). Target and cues: Gaze-following in children with autism. Journal of Child Psychology and Psychiatry, 39(7), 951–962.PubMedCrossRefGoogle Scholar
  41. Leekam, S. R., López, B., & Moore, C. (2000). Attention and joint attention in preschool children with autism. Developmental Psychology, 36(2), 261–273.PubMedCrossRefGoogle Scholar
  42. Loveland, K. A., & Landry, S. H. (1986). Joint attention and language in autism and developmental language delay. Journal of Autism and Developmental Disorders, 16(3), 335–349.PubMedCrossRefGoogle Scholar
  43. Luyster, R., & Lord, C. (2009). Word learning in children with autism spectrum disorders. Developmental Psychology, 45(6), 1774–1786.PubMedCrossRefGoogle Scholar
  44. Morgante, J. D., Zolfaghari, R., & Johnson, S. P. (2012). A critical test of temporal and spatial accuracy of the Tobii T60XL eye tracker. Infancy, 17, 9–32.CrossRefGoogle Scholar
  45. Mullen, E. M. (1995). Mullen Scales of Early Learning (AGS ed.). Circle Pines, MN: American Guidance Service.Google Scholar
  46. Mundy, P., Sigman, M., & Kasari, C. (1990). A longitudinal study of joint attention and language development in autistic children. Journal of Autism and Developmental Disorders, 20(1), 115–128.PubMedCrossRefGoogle Scholar
  47. Mundy, P., Sigman, M., & Kasari, C. (1994). Joint attention, developmental level, and symptom presentation in autism. Development and Psychopathology, 6, 389–401.CrossRefGoogle Scholar
  48. Nation, K., & Penny, S. (2008). Sensitivity to eye gaze in autism: Is it normal? Is it automatic? Is it social? Development and Psychopathology, 20, 79–97.PubMedCrossRefGoogle Scholar
  49. Parish-Morris, J., Hennon, E. A., Hirsh-Pasek, K., Golinkoff, R. M., & Tager-Flusberg, H. (2007). Children with autism illuminate the role of social intention in word learning. Child Development, 78(4), 1265–1287.PubMedCrossRefGoogle Scholar
  50. Pecchinenda, A., Pes, M., Ferlazzo, F., & Zoccolotti, P. (2008). The combined effect of gaze direction and facial expression on cueing spatial attention. Emotion, 8(5), 628–634.PubMedCrossRefGoogle Scholar
  51. Posner, M. I. (1980). Orienting of attention. Quarterly Journal of Experimental Psychology, 32, 3–25.PubMedCrossRefGoogle Scholar
  52. Preissler, M. A., & Carey, S. (2005). The role of inferences about referential intent in word learning: Evidence from autism. Cognition, 97, B13–B23.PubMedCrossRefGoogle Scholar
  53. Pruett, J. R., LaMacchia, A., Hoertel, S., Squire, E., McVey, K., Todd, R. D., et al. (2011). Social and non-social cueing of visuospatial attention in autism and typical development. Journal of Autism and Developmental Disorders, 41(6), 715–731.PubMedCrossRefGoogle Scholar
  54. Reddy, V. (2003). On being the object of attention: Implications for self-other consciousness. TRENDS in Cognitive Sciences, 7(9), 397–402.PubMedCrossRefGoogle Scholar
  55. Ristic, J., Friesen, C. K., & Kingstone, A. (2002). Are eyes special? It depends on how you look at it. Psychonomic Bulletin Review, 9(3), 507–513.PubMedCrossRefGoogle Scholar
  56. Ristic, J., Mottron, L., Friesen, C. K., Iarocci, G., Burack, J. A., & Kingstone, A. (2005). Eyes are special: But not for everyone. Cognitive Brain Research, 24, 715–718.PubMedCrossRefGoogle Scholar
  57. Rombough, A., & Iarocci, G. (in press). Orienting in response to gaze and the social use of gaze among children with autism spectrum disorders. Journal of Autism and Developmental Disorders, 1–13.Google Scholar
  58. Roseberry, S., Hirsh-Pasek, K., Parish-Morris, J., & Golinkoff, R. M. (2009). Live action: Can young children learn verbs from video? Child Development, 80(5), 1360–1375.PubMedCrossRefGoogle Scholar
  59. Rozga, A., Hutman, T., Young, G. S., Rogers, S. J., Ozonoff, S., Dapretto, M., et al. (2011). Behavioral profiles of affected and unaffected siblings of children with autism: Contribution of measures of mother–infant interaction and nonverbal communication. Journal of Autism and Developmental Disorders, 41, 287–301.PubMedCrossRefGoogle Scholar
  60. Rutherford, M. D., & Krysko, K. M. (2008). Eye direction, not movement direction, predicts attention shifts in those with autism spectrum disorders. Journal of Autism and Developmental Disorders, 38, 1958–1965.PubMedCrossRefGoogle Scholar
  61. Scaife, M., & Bruner, J. S. (1975). The capacity for joint visual attention in the infant. Nature, 265–266.Google Scholar
  62. Schietecatte, I., Roeyers, H., & Warreyn, P. (2012). Exploring the nature of joint attention impairments in young children with autism spectrum disorder: Associated social and cognitive skills. Journal of Autism and Developmental Disorders, 42(1), 1–12.PubMedCrossRefGoogle Scholar
  63. Schilbach, L., Eickhoff, S. B., Cieslik, E. C., Kuzmanovic, B., & Vogelely, K. (2012). Shall we do this together? Social gaze influences action control in a comparison group, but not in individuals with high-functioning autism. Autism, 16(2), 151–162.PubMedCrossRefGoogle Scholar
  64. Schilbach, L., Timmermans, B., Reddy, V., Costall, A., Bente, G., Schlicht, T., & Vogeley, K. (in press). Toward a second-person neuroscience. Behavioral and Brain Sciences. Google Scholar
  65. Schopler, E., Van Bourgondien, M., Wellman, J., & Love, S. (2010). Childhood Autism Rating Scale—Second edition (CARS2): Manual. Los Angeles: Western Psychological Services.Google Scholar
  66. Seibert, J. M., Sliwin, L., & Hogan, A. E. (1986). Social and cognitive bases of early comprehension of object reference. Cognitive Development, 1(4), 391–404.CrossRefGoogle Scholar
  67. 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
  68. Senju, A., Tojo, Y., Dairoku, H., & Hasegawa, T. (2004). Reflexive orienting in response to eye gaze and an arrow in children with and without autism. Journal of Child Psychology and Psychiatry, 45(3), 445–458.PubMedCrossRefGoogle Scholar
  69. Sigman, M., & McGovern, C. W. (2005). Improvement in cognitive and language skills from preschool to adolescence in autism. Journal of Autism and Developmental Disorders, 35(1), 15–23.PubMedCrossRefGoogle Scholar
  70. Sigman, M., & Ruskin, E. (1999). References. Monographs of the society for research in child development, 64(1), 109–113.CrossRefGoogle Scholar
  71. Sullivan, M., Finelli, J., Marvin, A., Garrett-Mayer, E., Bauman, M., & Landa, R. (2007). Response to joint attention in toddlers at risk for autism spectrum disorder: A prospective study. Journal of Autism and Developmental Disorders, 37, 37–48.PubMedCrossRefGoogle Scholar
  72. Swettenham, J., Condie, S., Campbell, R., Milne, E., & Coleman, M. (2003). Does the perception of moving eyes trigger reflexive visual orienting in autism? Philosophical Transactions of the Royal Society of London, B, 358, 325–334.CrossRefGoogle Scholar
  73. Teufel, C., Gutmann, A., Pirow, R., & Fischer, J. (2010). Facial expression modulates the ontogenetic trajectory of gaze following among monkeys. Developmental Science, 13(6), 913–922.PubMedCrossRefGoogle Scholar
  74. Tipples, J. (2006). Fear and fearfulness potentiate automatic orienting to eye gaze. Cognition and Emotion, 26(2), 309–320.Google Scholar
  75. Tottenham, N., Tanaka, J. M., 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(3), 242–249.PubMedCrossRefGoogle Scholar
  76. Uono, S., Sato, W., & Toichi, M. (2009). Dynamic fearful gaze does not enhance attention orienting in individuals with Asperger’s disorder. Brain and Cognition, 71, 229–233.PubMedCrossRefGoogle Scholar
  77. Vlamings, P. H. J. M., Stauder, J. E. A., van Son, I. A. M., & Mottron, L. (2003). Atypical visual orienting to gaze- and arrow-cues in adults with high-functioning autism. Journal of Autism and Developmental Disorders, 35(3), 267–277.CrossRefGoogle Scholar
  78. Wilms, M., Schilbach, L., Pfeiffer, U., Bente, G., Fink, G. R., & Vogeley, K. (2010). It’s in your eyes- using gaze-contingent stimuli to create truly interactive paradigms for social cognitive and affective neuroscience. Scan, 5, 98–107.PubMedGoogle Scholar
  79. Yechiam, E., Arshavsky, O., Shamay-Tsoory, S. G., Yaniv, S., & Aharon, J. (2010). Adapted to explore: Reinforcement learning in autistic spectrum conditions. Brain and Cognition, 72(2), 317–324.PubMedCrossRefGoogle Scholar
  80. Yoder, P., Stone, W. L., Walden, T., & Malesa, E. (2009). Predicting social impairment and ASD diagnosis in younger siblings of children with autism spectrum disorder. Journal of Autism and Developmental Disorders, 39, 1381–1391.PubMedCrossRefGoogle Scholar
  81. Yu, C., & Smith, L. B. (2012). Embodied attention and word learning by toddlers. Cognition.Google Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • K. Gillespie-Lynch
    • 1
    • 2
    Email author
  • R. Elias
    • 3
  • P. Escudero
    • 4
  • T. Hutman
    • 5
  • S. P. Johnson
    • 2
    • 5
  1. 1.Department of PsychologyCollege of Staten Island, City University of New YorkStaten IslandUSA
  2. 2.Department of PsychologyUniversity of CaliforniaLos AngelesUSA
  3. 3.Department of PsychologyUniversity of California, BerkeleyBerkeleyUSA
  4. 4.MARCS InstituteUniversity of Western SydneySydneyAustralia
  5. 5.Department of Psychiatry and Biobehavioral Sciences, Semel Insitute for Neuroscience and Human BehaviorUniversity of California, Los AngelesLos AngelesUSA

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