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Brief Report: Visual Perception, Task-Induced Pupil Response Trajectories and ASD Features in Children

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Abstract

We applied a trajectory-based analysis to eye tracking data in order to quantify individualized patterns of pupil response in the context of global–local processing that may be associated with autism spectrum disorder (ASD) features. Multiple pupil response trajectories across both global and local conditions were identified. Using the combined trajectory patterns for global and local conditions for each individual, we were able to identify three groups based on trajectory group membership that were thought to reflect perceptual strategy. Results indicated that the proportion of children with ASD was significantly greater in the group demonstrating a local-focus response. This research presents a novel analytic approach to the objective characterization of individualized pupil response patterns that are associated with ASD features.

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Notes

  1. While stimuli were presented for 5.5 s, due to consistent variability in Tobii eyetracking acquisitions (some having slightly over and/or under 330 samples taken across each 5.5 stimulus presentation) the initial 300 collected samples within each trial were used in analyses.

  2. We also explored potential differences in baseline pupil diameter between global and local conditions between our pupil trajectory groups; however, results did not indicate significant differences in baseline pupil diameter associated with pupil trajectory groups (p’s > 0.73).

References

  • Ahissar, M., & Hochstein, S. (2004). The reverse hierarchy theory of visual perceptual learning. Trends in Cognitive Sciences, 8(10), 457–464.

    Article  Google Scholar 

  • Anderson, C. J., & Colombo, J. (2009). Larger tonic pupil size in young children with autism spectrum disorder. Developmental Psychobiology, 51(2), 207–211. https://doi.org/10.1002/dev.20352.

    Article  PubMed  PubMed Central  Google Scholar 

  • Antezana, L., Mosner, M. G., Troiani, V., & Yerys, B. E. (2016). Social-emotional inhibition of return in children with autism spectrum disorder versus typical development. Journal of Autism and Developmental Disorders, 46(4), 1236–1246. https://doi.org/10.1007/s10803-015-2661-9.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ashwin, E., Ashwin, C., Rhydderch, D., Howells, J., & Baron-Cohen, S. (2009a). Eagle-eyed visual acuity: An experimental investigation of enhanced perception in autism. Biological Psychiatry, 65(1), 17–21.

    Article  Google Scholar 

  • Ashwin, E., Ashwin, C., Tavassoli, T., Chakrabarti, B., & Baron-Cohen, S. (2009b). Eagle-eyed visual acuity in autism. Biological Psychiatry, 66(10), e23–e24.

    Article  Google Scholar 

  • Baayen, R. H., Davidson, D. J., & Bates, D. M. (2008). Mixed-effects modeling with crossed random effects for subjects and items. Journal of Memory and Language, 59(4), 390–412.

    Article  Google Scholar 

  • Bach, M., & Dakin, S. C. (2009). Regarding “Eagle-eyed visual acuity: An experimental investigation of enhanced perception in autism”. Biological Psychiatry, 66(10), e19–e20.

    Article  Google Scholar 

  • Binda, P., & Murray, S. O. (2015a). Spatial attention increases the pupillary response to light changes. Journal of Vision, 15(2), 1. https://doi.org/10.1167/15.2.1.

    Article  PubMed  Google Scholar 

  • Binda, P., & Murray, S. O. (2015b). Keeping a large-pupilled eye on high-level visual processing. Trends in Cognitive Sciences, 19(1), 1–3. https://doi.org/10.1016/j.tics.2014.11.002.

    Article  PubMed  Google Scholar 

  • Binda, P., Pereverzeva, M., & Murray, S. O. (2013). Attention to bright surfaces enhances the pupillary light reflex. Journal of Neuroscience, 33(5), 2199–2204.

    Article  Google Scholar 

  • Blaser, E., Eglington, L., Carter, A. S., & Kaldy, Z. (2014). Pupillometry reveals a mechanism for the autism spectrum disorder (ASD) advantage in visual tasks. Scientific Reports. https://doi.org/10.1038/srep04301.

    Article  PubMed  PubMed Central  Google Scholar 

  • Boev, A. N., Fountas, K. N., Karampelas, I., Boev, C., Machinis, T. G., Feltes, C., et al. (2005). Quantitative pupillometry: Normative data in healthy pediatric volunteers. Journal of Neurosurgery: Pediatrics, 103(6), 496–500.

    Google Scholar 

  • Bölte, S., Schlitt, S., Gapp, V., Hainz, D., Schirman, S., Poustka, F., et al. (2012). A close eye on the eagle-eyed visual acuity hypothesis of autism. Journal of Autism and Developmental Disorders, 42(5), 726–733.

    Article  Google Scholar 

  • Busch, N. A., Dubois, J., & VanRullen, R. (2009). The phase of ongoing EEG oscillations predicts visual perception. Journal of Neuroscience, 29(24), 7869–7876.

    Article  Google Scholar 

  • Constantino, J. N., Davis, S. A., Todd, R. D., Schindler, M. K., Gross, M. M., Brophy, S. L., et al. (2003). Validation of a brief quantitative measure of autistic traits: Comparison of the social responsiveness scale with the autism diagnostic interview-revised. Journal of Autism and Developmental Disorders, 33(4), 427–433.

    Article  Google Scholar 

  • Constantino, J. N., & Todd, R. D. (2003). Autistic traits in the general population: A twin study. Archives of General Psychiatry, 60(5), 524–530.

    Article  Google Scholar 

  • Crewther, D. P., & Sutherland, A. (2009). The more he looked inside, the more piglet wasn’t there: Is autism really blessed with visual hyperacuity? Biological Psychiatry, 66(10), e21–e22.

    Article  Google Scholar 

  • D’Souza, D., Booth, R., Connolly, M., Happé, F., & Karmiloff-Smith, A. (2016). Rethinking the concepts of ‘local or global processors’: Evidence from Williams syndrome, Down syndrome, and Autism Spectrum Disorders. Developmental Science, 19(3), 452–468.

    Article  Google Scholar 

  • Dakin, S., & Frith, U. (2005). Vagaries of visual perception in autism. Neuron, 48(3), 497–507. https://doi.org/10.1016/j.neuron.2005.10.018.

    Article  PubMed  Google Scholar 

  • Dale, G., & Arnell, K. M. (2013). Investigating the stability of and relationships among global/local processing measures. Attention, Perception, & Psychophysics, 75(3), 394–406. https://doi.org/10.3758/s13414-012-0416-7.

    Article  Google Scholar 

  • Dale, G., & Arnell, K. M. (2014). Lost in the forest, stuck in the trees: Dispositional global/local bias is resistant to exposure to high and low spatial frequencies. PLoS ONE, 9(7), e98625. https://doi.org/10.1371/journal.pone.0098625.

    Article  PubMed  PubMed Central  Google Scholar 

  • Daniels, L. B., Nichols, D. F., Seifert, M. S., & Hock, H. S. (2012). Changes in pupil diameter entrained by cortically initiated changes in attention. Visual Neuroscience, 29(02), 131–142. https://doi.org/10.1017/S0952523812000077.

    Article  PubMed  Google Scholar 

  • DiCriscio, A. S., Hu, Y., & Troiani, V. (2018). Task induced pupil response and visual perception in adults. PLoS ONE, 13(12), e0209556.

    Article  Google Scholar 

  • DiCriscio, A. S., Miller, S. J., Hanna, E. K., Kovac, M., Turner-Brown, L., Sasson, N. J., et al. (2016). Brief report: Cognitive control of social and nonsocial visual attention in autism. Journal of Autism and Developmental Disorders, 46(8), 2797–2805.

    Article  Google Scholar 

  • DiCriscio, A. S., & Troiani, V. (2017). Pupil adaptation corresponds to quantitative measures of autism traits in children. Scientific Reports, 7(1), 6476.

    Article  Google Scholar 

  • Dukette, D., & Stiles, J. (2001). The effects of stimulus density on children’s analysis of hierarchical patterns. Developmental Science, 4(2), 233–251.

    Article  Google Scholar 

  • Happe, F. (1999). Autism: Cognitive deficit or cognitive style? Trends in Cognitive Science, 3(6), 216–222.

    Article  Google Scholar 

  • Happé, F., Briskman, J., & Frith, U. (2001). Exploring the cognitive phenotype of autism: Weak “central coherence” in parents and siblings of children with autism: I. Experimental tests. Journal of Child Psychology and Psychiatry, 42(3), 299–307. https://doi.org/10.1111/1469-7610.00723.

    Article  PubMed  Google Scholar 

  • Hayward, D. A., Fenerci, C., & Ristic, J. (2018). An investigation of global–local processing bias in a large sample of typical individuals varying in autism traits. Consciousness and Cognition, 65, 271–279.

    Article  Google Scholar 

  • Heitmann, A., Guttkuhn, R., Aguirre, A., Trutschel, U., & Moore-Ede, M. (2001). Technologies for the monitoring and prevention of driver fatigue. In Proceedings of the first international driving symposium on human factors in driver assessment, training and vehicle design (Vol. 86). Retrieved from https://www.researchgate.net/profile/Udo_Trutschel/publication/233389964_TECHNOLOGIES_FOR_THE_MONITORING_AND_PREVENTION_OF_DRIVER_FATIGUE/links/0fcfd50a13bf28da3e000000.pdf.

  • Hobson, R. P., & Bishop, M. (2003). The pathogenesis of autism: Insights from congenital blindness. Philosophical Transactions of the Royal Society B: Biological Sciences, 358(1430), 335–344. https://doi.org/10.1098/rstb.2002.1201.

    Article  Google Scholar 

  • Hobson, R. P., Lee, A., & Brown, R. (1999). Autism and congenital blindness. Journal of Autism and Developmental Disorders, 29(1), 45–56.

    Article  Google Scholar 

  • Hochstein, S., & Ahissar, M. (2002). View from the top: Hierarchies and reverse hierarchies in the visual system. Neuron, 36(5), 791–804.

    Article  Google Scholar 

  • Insel, T., Cuthbert, B., Garvey, M., Heinssen, R., Pine, D. S., Quinn, K., et al. (2010). Research domain criteria (RDoC): Toward a new classification framework for research on mental disorders. American Journal of Psychiatry, 167(7), 748–751. https://doi.org/10.1176/appi.ajp.2010.09091379.

    Article  PubMed  Google Scholar 

  • Jackson, I., & Sirois, S. (2009). Infant cognition: Going full factorial with pupil dilation. Developmental Science, 12(4), 670–679.

    Article  Google Scholar 

  • Jepma, M., & Nieuwenhuis, S. (2011). Pupil diameter predicts changes in the exploration–exploitation trade-off: Evidence for the adaptive gain theory. Journal of Cognitive Neuroscience, 23(7), 1587–1596.

    Article  Google Scholar 

  • Kaldy, Z., Giserman, I., Carter, A. S., & Blaser, E. (2013). The mechanisms underlying the ASD advantage in visual search. Journal of Autism and Developmental Disorders, 56, 67. https://doi.org/10.1007/s10803-013-1957-x.

    Article  Google Scholar 

  • Kaldy, Z., Kraper, C., Carter, A. S., & Blaser, E. (2011). Toddlers with autism spectrum disorder are more successful at visual search than typically developing toddlers. Developmental Science, 14(5), 980–988. https://doi.org/10.1111/j.1467-7687.2011.01053.x.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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. https://doi.org/10.1001/archpsyc.59.9.809.

    Article  PubMed  Google Scholar 

  • Koldewyn, K., Jiang, Y. V., Weigelt, S., & Kanwisher, N. (2013). Global/local processing in autism: Not a disability, but a disinclination. Journal of Autism and Developmental Disorders, 43(10), 2329–2340.

    Article  Google Scholar 

  • Landry, R., & Bryson, S. E. (2004). Impaired disengagement of attention in young children with autism. Journal of Child Psychology and Psychiatry, 45(6), 1115–1122. https://doi.org/10.1111/j.1469-7610.2004.00304.x.

    Article  PubMed  Google Scholar 

  • Martin, I., & McDonald, S. (2003). Weak coherence, no theory of mind, or executive dysfunction? Solving the puzzle of pragmatic language disorders. Brain and Language, 85(3), 451–466.

    Article  Google Scholar 

  • Martineau, J., Hernandez, N., Hiebel, L., Roché, L., Metzger, A., & Bonnet-Brilhault, F. (2011). Can pupil size and pupil responses during visual scanning contribute to the diagnosis of autism spectrum disorder in children? Journal of Psychiatric Research, 45(8), 1077–1082. https://doi.org/10.1016/j.jpsychires.2011.01.008.

    Article  PubMed  Google Scholar 

  • Mathôt, S., van der Linden, L., Grainger, J., & Vitu, F. (2013). The pupillary light response reveals the focus of covert visual attention. PLoS ONE, 8(10), e78168. https://doi.org/10.1371/journal.pone.0078168.

    Article  PubMed  PubMed Central  Google Scholar 

  • McKone, E., Davies, A. A., Fernando, D., Aalders, R., Leung, H., Wickramariyaratne, T., et al. (2010). Asia has the global advantage: Race and visual attention. Vision Research, 50(16), 1540–1549.

    Article  Google Scholar 

  • Mottron, L., Burack, J. A., Stauder, J. E. A., & Robaey, P. (1999). Perceptual processing among high-functioning persons with autism. The Journal of Child Psychology and Psychiatry and Allied Disciplines, 40(02), 203–211.

    Article  Google Scholar 

  • Naber, M., Alvarez, G. A., & Nakayama, K. (2013). Tracking the allocation of attention using human pupillary oscillations. Frontiers in Psychology, 4, 919.

    Article  Google Scholar 

  • Nagin, D. S., & Nagin, D. (2005). Group-based modeling of development. Cambridge: Harvard University Press.

    Book  Google Scholar 

  • Navon, D. (1977). Forest before trees: The precedence of global features in visual perception. Cognitive Psychology, 9(3), 353–383.

    Article  Google Scholar 

  • Navon, D. (1981). The forest revisited: More on global precedence. Psychological Research, 43(1), 1–32.

    Article  Google Scholar 

  • Palinko, O., Kun, A. L., Shyrokov, A., & Heeman, P. (2010). Estimating cognitive load using remote eye tracking in a driving simulator. In Proceedings of the 2010 symposium on eye-tracking research & applications (pp. 141–144). New York: ACM.

  • Pellicano, E., Maybery, M., Durkin, K., & Maley, A. (2006). Multiple cognitive capabilities/deficits in children with an autism spectrum disorder: “Weak” central coherence and its relationship to theory of mind and executive control. Development and Psychopathology, 18(1), 77–98.

    Article  Google Scholar 

  • Poirel, N., Mellet, E., Houdé, O., & Pineau, A. (2008). First came the trees, then the forest: Developmental changes during childhood in the processing of visual local–global patterns according to the meaningfulness of the stimuli. Developmental Psychology, 44(1), 245.

    Article  Google Scholar 

  • Poirel, N., Pineau, A., & Mellet, E. (2006). Implicit identification of irrelevant local objects interacts with global/local processing of hierarchical stimuli. Acta Psychologica, 122(3), 321–336.

    Article  Google Scholar 

  • Poirel, N., Simon, G., Cassotti, M., Leroux, G., Perchey, G., Lanoë, C., et al. (2011). The shift from local to global visual processing in 6-year-old children is associated with grey matter loss. PLoS ONE, 6(6), e20879.

    Article  Google Scholar 

  • Raney, G. E., Campbell, S. J., & Bovee, J. C. (2014). Using eye movements to evaluate the cognitive processes involved in text comprehension. Journal of Visualized Experiments: JoVE, 10(83), e50780.

    Google Scholar 

  • RDevelopment, C. (2012). TEAM 2009: R: A language and environment for statistical computing. Vienna: RDevelopment. Retrieved from http://www.r-project.org.

  • Samson, F., Mottron, L., Soulières, I., & Zeffiro, T. A. (2012). Enhanced visual functioning in autism: An ALE meta-analysis. Human Brain Mapping, 33(7), 1553–1581. https://doi.org/10.1002/hbm.21307.

    Article  PubMed  Google Scholar 

  • Sasson, N. J., Elison, J. T., Turner-Brown, L. M., Dichter, G. S., & Bodfish, J. W. (2011). Brief report: Circumscribed attention in young children with autism. Journal of Autism and Developmental Disorders, 41(2), 242–247. https://doi.org/10.1007/s10803-010-1038-3.

    Article  PubMed  PubMed Central  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 

  • Scherf, K. S., Behrmann, M., Kimchi, R., & Luna, B. (2009). Emergence of global shape processing continues through adolescence. Child Development, 80(1), 162–177.

    Article  Google Scholar 

  • Simmons, D. R., Robertson, A. E., McKay, L. S., Toal, E., McAleer, P., & Pollick, F. E. (2009). Vision in autism spectrum disorders. Vision Research, 49(22), 2705–2739. https://doi.org/10.1016/j.visres.2009.08.005.

    Article  PubMed  Google Scholar 

  • Stewart, L., Overath, T., Warren, J. D., Foxton, J. M., & Griffiths, T. D. (2008). fMRI evidence for a cortical hierarchy of pitch pattern processing. PLoS ONE, 3(1), e1470. https://doi.org/10.1371/journal.pone.0001470.

    Article  PubMed  PubMed Central  Google Scholar 

  • Stiles, J., & Tada, W. L. (1996). Developmental change in children’s analysis of spatial patterns. Developmental Psychology, 32(5), 951.

    Article  Google Scholar 

  • Van der Hallen, R., Evers, K., Brewaeys, K., Van den Noortgate, W., & Wagemans, J. (2015). Global processing takes time: A meta-analysis on localglobal visual processing in ASD. Worcester: American Psychological Association. Retrieved from http://psycnet.apa.org/journals/bul/141/3/549/.

  • Varnum, M. E., Shi, Z., Chen, A., Qiu, J., & Han, S. (2014). When “Your” reward is the same as “My” reward: Self-construal priming shifts neural responses to own vs. friends’ rewards. NeuroImage, 87, 164–169.

    Article  Google Scholar 

  • Wechsler, D., & Hsiao-pin, C. (2011). WASI-II: Wechsler abbreviated scale of intelligence. London: Pearson.

    Google Scholar 

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Acknowledgments

The authors are grateful to Kayleigh M. Adamson, BS for her help with recruitment and data collection. This study was funded by the Simons Foundation, SFARI Explorer Award #350225.

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ASD and VT designed the research. ASD programmed the task and collected the data. YH and ASD completed data analysis. ASD, YH and VT interpreted the data. ASD drafted the manuscript. ASD, YH and VT critically revised the manuscript. All authors have read and approved the final version of the manuscript. All authors reviewed the manuscript.

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Correspondence to Antoinette Sabatino DiCriscio or Vanessa Troiani.

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DiCriscio, A.S., Hu, Y. & Troiani, V. Brief Report: Visual Perception, Task-Induced Pupil Response Trajectories and ASD Features in Children. J Autism Dev Disord 49, 3016–3030 (2019). https://doi.org/10.1007/s10803-019-04028-7

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