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Distance from Typical Scan Path When Viewing Complex Stimuli in Children with Autism Spectrum Disorder and its Association with Behavior

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Abstract

Eye-tracking is often used to study attention in children with autism spectrum disorder (ASD). Previous research has identified multiple atypical patterns of attention in children with ASD based on areas-of-interest analysis. Fewer studies have investigated gaze path, a measure which is dependent on the dynamic content of the stimulus presented. Here, rather than looking at proportions of looking time to areas of interest, we calculated mean fixations frame-by-frame in a group of typically developing children (36 to 72 months) and determined the distance from those typical fixations for 155 children with ASD (27–95 months). Findings revealed that distance from the typical scan path among the children with ASD was associated with lower communication abilities and greater ASD symptomatology.

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References

  • Aman, M. G., Singh, N. N., Stewart, A. W., & Field, C. J. (1985). The aberrant behavior checklist: A behavior rating scale for the assessment of treatment effects. American Journal Of Mental Deficiency, 89, 485.

    PubMed  Google Scholar 

  • American Psychiatric Association. (2013). Diagnostic and statistical manual of mental disorders (5th ed.). Arlington, VA: American Psychiatric Publishing.

    Google Scholar 

  • Arunachalam, S., & Luyster, R. J. (2015). The integrity of lexical acquisition mechanisms in autism spectrum disorders: A research review. Autism Research, 9, 810.

    Article  PubMed  PubMed Central  Google Scholar 

  • Charman, T. (2003). Why is joint attention a pivotal skill in autism? Philosophical Transactions of The Royal Society of London Series B Biological Sciences, 358(1430), 315–324. https://doi.org/10.1098/Rstb.2002.1199.

    Article  PubMed  Google Scholar 

  • Chawarska, K., Macari, S., & Shic, F. (2012). Context modulates attention to social scenes in toddlers with autism. Journal Of Child Psychology And Psychiatry, 53(8), 903–913. https://doi.org/10.1111/J.1469-7610.2012.02538.X.

    Article  PubMed  Google Scholar 

  • Chawarska, K., Macari, S., & Shic, F. (2013). Decreased spontaneous attention to social scenes in 6-month-old infants later diagnosed with autism spectrum disorders. Biological Psychiatry, 74(3), 195–203. https://doi.org/10.1016/J.Biopsych.2012.11.022.

    Article  PubMed  PubMed Central  Google Scholar 

  • Chawarska, K., Ye, S., Shic, F., & Chen, L. (2015). Multilevel differences in spontaneous social attention in toddlers with autism spectrum disorder. Child Development, 87, 543.

    Article  PubMed  PubMed Central  Google Scholar 

  • Chevallier, C., Parish-Morris, J., Mcvey, A., Rump, K. M., Sasson, N. J., Herrington, J. D., & Schultz, R. T. (2015). Measuring social attention and motivation in autism spectrum disorder using eye-tracking: Stimulus type matters. Autism Research, 8(5), 620–628.

    Article  PubMed  PubMed Central  Google Scholar 

  • Chita-Tegmark, M. (2016). Social attention in asd: A review and meta-analysis of eye-tracking studies. Research in Developmental Disabilities, 48, 79–93.

    Article  PubMed  Google Scholar 

  • Cilia, F., Aubry, A., Le Driant, B., Bourdin, B., & Vandromme, L. (2019). Visual exploration of dynamic or static joint attention bids in children with autism syndrome disorder. Frontiers in Psychology, 10, 2187.

    Article  PubMed  PubMed Central  Google Scholar 

  • Cohen, I. L., Schmidt-Lackner, S., Romanczyk, R., & Sudhalter, V. (2003). The pdd behavior inventory: A rating scale for assessing response to intervention in children with pervasive developmental disorder. Journal of Autism and Developmental Disorders, 33(1), 31–45.

    Article  PubMed  Google Scholar 

  • Constantino, J. N., Kennon-Mcgill, S., Weichselbaum, C., Marrus, N., Haider, A., Glowinski, A. L., et al. (2017). Infant viewing of social scenes is under genetic control and is atypical in autism. Nature, 547(7663), 340.

    Article  PubMed  PubMed Central  Google Scholar 

  • Dawson, G., Munson, J., Estes, A., Osterling, J., Mcpartland, J., Toth, K., et al. (2002). Neurocognitive function and joint attention ability in young children with autism spectrum disorder versus developmental delay. Child Development, 73(2), 345–358. https://doi.org/10.1111/1467-8624.00411.

    Article  PubMed  Google Scholar 

  • Dawson, G., Toth, K., Abbott, R., Osterling, J., Munson, J., Estes, A., & Liaw, J. (2004). Early social attention impairments in autism: Social orienting, joint attention, and attention to distress. Developmental Psychology, 40(2), 271–283. https://doi.org/10.1037/0012-1649.40.2.271.

    Article  PubMed  Google Scholar 

  • Elliott, C. (2007). Differential ability scales (Vol. 22, pp. 128–132). San Antonio, TX: Harcourt Assessment.

    Google Scholar 

  • Elsabbagh, M., Bedford, R., Senju, A., Charman, T., Pickles, A., Johnson, M. H., & Team B. (2014). What you see is what you get: Contextual modulation of face scanning in typical and atypical development. Social Cognitive and Affective Neuroscience, 9(4), 538–543.

    Article  PubMed  Google Scholar 

  • Falck-Ytter, T., Bölte, S., & Gredebäck, G. (2013). Eye tracking in early autism research. Journal of Neurodevelopmental Disorders, 5(1), 28.

    Article  PubMed  PubMed Central  Google Scholar 

  • Falck-Ytter, T., Von Hofsten, C., Gillberg, C., & Fernell, E. (2013). Visualization and analysis of eye movement data from children with typical and atypical development. Journal of Autism and Developmental Disorders, 43(10), 2249–2258.

    Article  PubMed  PubMed Central  Google Scholar 

  • Goodman, R. (1997). The strengths and difficulties questionnaire: A research note. Journal of Child Psychology and Psychiatry, 38(5), 581–586.

    Article  Google Scholar 

  • Goodman, R. (2001). Psychometric properties of the strengths and difficulties questionnaire. Journal of The American Academy of Child & Adolescent Psychiatry, 40(11), 1337–1345.

    Article  Google Scholar 

  • Goodman, R., Ford, T., Simmons, H., Gatward, R., & Meltzer, H. (2000). Using the strengths and difficulties questionnaire (Sdq) to screen for child psychiatric disorders in a community sample. The British Journal of Psychiatry, 177(6), 534–539.

    Article  PubMed  Google Scholar 

  • Guillon, Q., Hadjikhani, N., Baduel, S., & Rogé, B. (2014). Visual social attention in autism spectrum disorder: Insights from eye tracking studies. Neuroscience & Biobehavioral Reviews, 42, 279–297.

    Article  Google Scholar 

  • Habayeb, S., Tsang, T., Saulnier, C., Klaiman, C., Jones, W., Klin, A., & Edwards, L. A. (2020). Visual traces of language acquisition in toddlers with autism spectrum disorder during the second year of life. Journal of Autism and Developmental Disorders. https://doi.org/10.1007/s10803-020-04730-x.

    Article  PubMed  Google Scholar 

  • Hanley, M., Mcphillips, M., Mulhern, G., & Riby, D. M. (2013). Spontaneous attention to faces in asperger syndrome using ecologically valid static stimuli. Autism, 17(6), 754–761.

    Article  PubMed  Google Scholar 

  • 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-old toddlers with autism spectrum disorder. Archives of General Psychiatry, 65(8), 946–954. https://doi.org/10.1001/Archpsyc.65.8.946.

    Article  PubMed  Google Scholar 

  • Kennedy, D. P., D’onofrio, B. M., Quinn, P. D., Bölte, S., Lichtenstein, P., & Falck-Ytter, T. (2017). Genetic influence on eye movements to complex scenes at short timescales. Current Biology, 27(22), 3554–3560.

    Article  PubMed  Google Scholar 

  • Klin, A., Jones, W., Schultz, R., Volkmar, F., & Cohen, D. (2002a). Defining and quantifying the social phenotype in autism. American Journal of Psychiatry, 159(6), 895–908.

    Article  Google Scholar 

  • Klin, A., Jones, W., Schultz, R., Volkmar, F., & Cohen, D. (2002b). 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. https://doi.org/10.1001/Archpsyc.59.9.809.

    Article  PubMed  Google Scholar 

  • Klin, A., Lin, D. J., 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • Le Couteur, A., Lord, C., & Rutter, M. (2003). The autism diagnostic interview-revised (Adi-R) (pp. 659–685). Los Angeles: Western Psychological Services.

    Google Scholar 

  • Lönnqvist, L., Loukusa, S., Hurtig, T., Mäkinen, L., Siipo, A., Väyrynen, E., et al. (2017). How young adults with autism spectrum disorder watch and interpret pragmatically complex scenes. The Quarterly Journal of Experimental Psychology, 70(11), 2331–2346.

    Article  PubMed  Google Scholar 

  • Lord, C., Rutter, M., Dilavore, P., Risi, S., Gotham, K., & Bishop, S. (2012). Autism diagnostic observation schedule–2nd edition (Ados-2). Los Angeles: Western Psychological Corporation.

    Google Scholar 

  • Mastergeorge, A. M., Kahathuduwa, C., & Blume, J. (2020). Eye-tracking in infants and young children at risk for autism spectrum disorder: A systematic review of visual stimuli in experimental paradigms. Journal of Autism and Developmental Disorders. https://doi.org/10.1007/s10803-020-04731-w.

    Article  Google Scholar 

  • Mullen, E. M. (1995). Mullen scales of early learning. Circle Pines, MN: American Guidance Service.

    Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Murias, M., Major, S., Davlantis, K., Franz, L., Harris, A., Rardin, B., et al. (2018). Validation of eye-tracking measures of social attention as a potential biomarker for autism clinical trials. Autism Research, 11(1), 166–174.

    Article  PubMed  Google Scholar 

  • Nakano, T., Tanaka, K., Endo, Y., Yamane, Y., Yamamoto, T., Nakano, Y., et al. (2010). Atypical gaze patterns in children and adults with autism spectrum disorders dissociated from developmental changes in gaze behaviour. Proceedings of The Royal Society B, 277(1696), 2935–2943. https://doi.org/10.1098/Rspb.2010.0587.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 & Developmental Disorders, 32(4), 249–261.

    Article  Google Scholar 

  • Rice, K., Moriuchi, J. M., Jones, W., & Klin, A. (2012). Parsing heterogeneity in autism spectrum disorders: Visual scanning of dynamic social scenes in school-aged children. Journal of The American Academy of Child & Adolescent Psychiatry, 51(3), 238–248.

    Article  Google Scholar 

  • Sargezeh, B. A., Ayatollahi, A., & Daliri, M. R. (2019). Investigation of eye movement pattern parameters of individuals with different fluid intelligence. Experimental Brain Research, 237(1), 15–28.

    Article  Google Scholar 

  • Sasson, N. J., Turner-Brown, L. M., Holtzclaw, T. N., Lam, K. S. L., & Bodfish, J. W. (2008). Children with autism demonstrate circumscribed attention during passive viewing of complex social and nonsocial picture arrays. Autism Research, 1(1), 31–42. https://doi.org/10.1002/Aur.4.

    Article  PubMed  Google Scholar 

  • Schomaker, J., Walper, D., Wittmann, B. C., & Einhäuser, W. (2017). Attention in natural scenes: Affective-motivational factors guide gaze independently of visual salience. Vision Research, 133, 161–175.

    Article  PubMed  Google Scholar 

  • Shic, F., Bradshaw, J., Klin, A., Scassellati, B., & Chawarska, K. (2011). Limited activity monitoring in toddlers with autism spectrum disorder. Brain Research, 1380, 246–254.

    Article  PubMed  Google Scholar 

  • Shic, F., Macari, S., & Chawarska, K. (2013). Speech disturbs face scanning in 6-month-old infants who develop autism spectrum disorder. Biological Psychiatry, 75, 231.

    Article  PubMed  Google Scholar 

  • Sinha, P., Kjelgaard, M. M., Gandhi, T. K., Tsourides, K., Cardinaux, A. L., Pantazis, D., et al. (2014). Autism as a disorder of prediction. Proceedings of The National Academy of Sciences, 111(42), 15220–15225.

    Article  Google Scholar 

  • Sparrow, S. S. (2011). Vineland adaptive behavior scales. In J. Kreutzer, J. Deluca, & B. Caplan (Eds.), Encyclopedia of clinical neuropsychology (pp. 2618–2621). New York: Springer.

    Chapter  Google Scholar 

  • Sparrow, S. S., Cicchetti, D. V., & Saulnier, C. A. (2016). Vineland-3: Vineland adaptive behavior scales. San Antonio: Pearson.

    Google Scholar 

  • Speer, L. L., Cook, A. E., Mcmahon, W. M., & Clark, E. (2007). Face processing in children with autism: Effects of stimulus contents and type. Autism, 11(3), 265–277. https://doi.org/10.1177/1362361307076925.

    Article  PubMed  Google Scholar 

  • 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(1), 37–48.

    Article  PubMed  Google Scholar 

  • Tenenbaum, E. J., Amso, D., Abar, B., & Sheinkopf, S. J. (2014). Attention and word learning in autistic, language delayed and typically developing children. Frontiers in Psychology, 5, 490.

    Article  PubMed  PubMed Central  Google Scholar 

  • Tenenbaum, E. J., Amso, D., Righi, G., & Sheinkopf, S. J. (2017). Attempting to “increase intake from the input”: Attention and word learning in children with autism. Journal of Autism and Developmental Disorders, 47(6), 1791–1805.

    Article  PubMed  PubMed Central  Google Scholar 

  • Tenenbaum, E. J., Sobel, D. M., Sheinkopf, S. J., Malle, B. F., & Morgan, J. L. (2014). Attention to the mouth and gaze following in infancy predict language development. Journal of Child Language, 42, 1173.

    Article  PubMed  PubMed Central  Google Scholar 

  • Wagner, J. B., Hirsch, S. B., Vogel-Farley, V. K., Redcay, E., & Nelson, C. A. (2013). Eye-tracking, autonomic, and electrophysiological correlates of emotional face processing in adolescents with autism spectrum disorder. Journal of Autism and Developmental Disorders, 43(1), 188–199.

    Article  PubMed  PubMed Central  Google Scholar 

  • Wakabayashi, A., Baron-Cohen, S., Wheelwright, S., & Tojo, Y. (2006). The autism-spectrum quotient (Aq) in Japan: A cross-cultural comparison. Journal of Autism and Developmental Disorders, 36(2), 263–270.

    Article  PubMed  Google Scholar 

  • Wang, Q., Campbell, D. J., Macari, S. L., Chawarska, K., & Shic, F. (2018). Operationalizing atypical gaze in toddlers with autism spectrum disorders: A cohesion-based approach. Molecular Autism, 9(1), 25.

    Article  PubMed  PubMed Central  Google Scholar 

  • Wechsler, D. (2002). Wechsler preschool and primary scale of intelligence (Wppsi-Iii) (3rd ed.). San Antonio: Pearson.

    Google Scholar 

  • Young, G. S., Merin, N., Rogers, S. J., & Ozonoff, S. (2009). Gaze behavior and affect at 6 months: Predicting clinical outcomes and language development in typically developing infants and infants at risk for autism. Developmental Science, 12(5), 798–814.

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This research was supported by grants from NICHD P50HD093074, the Marcus Foundation, and a NARSAD Young Investigator Grant from the Brain & Behavior Research Foundation (#23807). We thank Fred Shic, PhD for his input on this work.

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Correspondence to Elena J. Tenenbaum.

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Dr. Dawson is on the Scientific Advisory Boards of Janssen Research and Development, Akili, Inc, LabCorp, Inc, Roche Pharmaceutical Company, and Tris Pharma, and is a consultant to Apple, Gerson Lehrman Group, Guidepoint, Inc, Axial Ventures, Teva Pharmaceutical, and is CEO of DASIO, LLC. Dr. Dawson has received book royalties from Guilford Press, Oxford University Press, Springer Nature Press. In addition, Dr. Dawson has the following patent applications: 1802952, 1802942, 15141391, and 16493754. Dawson and Carpenter helped develop technology for early screening for ASD. The technology has been licensed and Dawson, Carpenter, and Duke University have benefited financially. Dr. Howard reports personal fees from Roche.

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Video shows the full stimulus overlain with the mean fixations frame-by-frame. Blue indicates the mean for the TD group. Red indicates mean fixation for the ASD participants. Boxes show standard deviation for X and Y axes.

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Tenenbaum, E.J., Major, S., Carpenter, K.L.H. et al. Distance from Typical Scan Path When Viewing Complex Stimuli in Children with Autism Spectrum Disorder and its Association with Behavior. J Autism Dev Disord 51, 3492–3505 (2021). https://doi.org/10.1007/s10803-020-04812-w

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