Abstract
Sensory differences are nearly universal in autism, but their genetic origins are poorly understood. Here, we tested how individuals with an autism-linked genotype, 16p.11.2 deletion (“16p”), attend to visual information in immersive, real-world photospheres. We monitored participants’ (N = 44) gaze while they actively explored 360° scenes via headmounted virtual reality. We modeled the visually salient and semantically meaningful information in scenes and quantified the relative bottom-up vs. top-down influences on attentional deployment. We found, when compared to typically developed control (TD) participants, 16p participants’ attention was less dominantly predicted by semantically meaningful scene regions, relative to visually salient regions. These results suggest that a reduction in top-down relative to bottom-up attention characterizes how individuals with 16p.11.2 deletions engage with naturalistic visual environments.
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References
Açik, A., Sarwary, A., Schultze-Kraft, R., Onat, S., & König, P. (2010). Developmental changes in natural viewing behavior: Bottom-up and top-down differences between children, young adults and older adults. Frontiers in Psychology, 1, 207. https://doi.org/10.3389/fpsyg.2010.00207
American Psychiatric Association. (2013). Diagnostic and statistical manual of mental disorders (5th ed). https://doi.org/10.1176/appi.books.9780890425596
Amso, D., Haas, S., & Markant, J. (2014a). An eye tracking investigation of developmental change in bottom-up attention orienting to faces in cluttered natural scenes. PLoS ONE, 9(1), e85701. https://doi.org/10.1371/journal.pone.0085701
Amso, D., Haas, S., Tenenbaum, E., Markant, J., & Sheinkopf, S. J. (2014b). Bottom-up attention orienting in young children with autism. Journal of Autism and Developmental Disorders, 44(3), 664–673. https://doi.org/10.1007/s10803-013-1925-5
Baron-Cohen, S., Hoekstra, R. A., Knickmeyer, R., & Wheelwright, S. (2006). The Autism-Spectrum Quotient (AQ)—Adolescent version. Journal of Autism and Developmental Disorders, 36(3), 343–350. https://doi.org/10.1007/s10803-006-0073-6
Bates, D., Mächler, M., Bolker, B. M., & Walker, S. C. (2015). Fitting linear mixed-effects models using lme4. Journal of Statistical Software. https://doi.org/10.18637/jss.v067.i01
Bijlsma, E.K., Gijsbers, A.C.J., Schuurs-Hoeijmakers, J.H.M., Van Haeringen, A., van de Putte, D.F., Anderlid, B.M., Lundin, J., Lapunzina, P., Jurado, L.P., Delle Chiaie, B.A., & Loeys, B. (2009). Extending the phenotype of recurrent rearrangements of 16p11.2: Deletions in mentally retarded patients without autism and in normal individuals. European Journal of Medical Genetics, 52(2–3), 77–87. https://doi.org/10.1016/j.ejmg.2009.03.006
Brauer, M., & Curtin, J. J. (2018). Linear mixed-effects models and the analysis of nonindependent data: A unified framework to analyze categorical and continuous independent variables that vary within-subjects and/or within-items. Psychological Methods, 23(3), 389–411. https://doi.org/10.1037/met0000159
Constantino, J. N., Kennon-McGill, S., Weichselbaum, C., Marrus, N., Haider, A., Glowinski, A. L., Gillespie, S., Klaiman, C., Klin, A., & Jones, W. (2017). Infant viewing of social scenes is under genetic control and is atypical in autism. Nature, 547(7663), 340–344. https://doi.org/10.1038/nature22999
Del Barrio, V. (2016). Diagnostic and statistical manual of mental disorders. In The Curated Reference Collection in Neuroscience and Biobehavioral Psychology. American Psychiatric Association. https://doi.org/10.1016/B978-0-12-809324-5.05530-9
Fischer, J., Smith, H., Martinez-Pedraza, F., Carter, A. S., Kanwisher, N., & Kaldy, Z. (2016). Unimpaired attentional disengagement in toddlers with autism spectrum disorder. Developmental Science, 19(6), 1095–1103. https://doi.org/10.1111/desc.12386
Fletcher-Watson, S., Leekam, S. R., Benson, V., Frank, M. C., & Findlay, J. M. (2009). Eye-movements reveal attention to social information in autism spectrum disorder. Neuropsychologia, 47(1), 248–257. https://doi.org/10.1016/j.neuropsychologia.2008.07.016
Frazier, T. W., Strauss, M., Klingemier, E. W., Zetzer, E. E., Hardan, A. Y., Eng, C., & Youngstrom, E. A. (2017). A meta-analysis of gaze differences to social and nonsocial information between individuals with and without autism. Journal of the American Academy of Child and Adolescent Psychiatry, 56(7), 546–555. https://doi.org/10.1016/j.jaac.2017.05.005
Freeth, M., Foulsham, T., & Chapman, P. (2011). The influence of visual saliency on fixation patterns in individuals with Autism Spectrum Disorders. Neuropsychologia, 49(1), 156–160. https://doi.org/10.1016/j.neuropsychologia.2010.11.012
Grubb, M. A., Behrmann, M., Egan, R., Minshew, N. J., Carrasco, M., & Heeger, D. J. (2013). Endogenous spatial attention: Evidence for intact functioning in adults with autism. Autism Research, 6(2), 108–118. https://doi.org/10.1002/aur.1269
De Haas, B., Iakovidis, A. L., Schwarzkopf, D. S., & Gegenfurtner, K. R. (2019). Individual differences in visual salience vary along semantic dimensions. Proceedings of the National Academy of Sciences of the United States of America, 116(24), 11687–11692. https://doi.org/10.1073/pnas.1820553116
Hamner, T., & Vivanti, G. (2019). Eye-tracking research in Autism Spectrum Disorder: What are we measuring and for what purposes? Current Developmental Disorders Reports, 6(2), 37–44. https://doi.org/10.1007/s40474-019-00158-w
Hanson, E., Nasir, R. H., Fong, A., Lian, A., Hundley, R., Shen, Y., Wu, B. L., Holm, I. A., & Miller, D. T. (2010). Cognitive and behavioral characterization of 16p11.2 deletion syndrome. Journal of Developmental and Behavioral Pediatrics, 31(8), 649–657. https://doi.org/10.1097/DBP.0b013e3181ea50ed
Harel, J., Koch, C., & Perona, P. (2007). Graph-based visual saliency. Advances in Neural Information Processing Systems. https://doi.org/10.7551/mitpress/7503.003.0073
Haskins, A. J., Mentch, J., Botch, T. L., & Robertson, C. E. (2020). Active vision in immersive, 360° real-world environments. Scientific Reports, 10(1), 1–11. https://doi.org/10.1038/s41598-020-71125-4
Henderson, J. M., & Hayes, T. R. (2017). Meaning-based guidance of attention in scenes as revealed by meaning maps. Nature Human Behaviour, 1(10), 743–747. https://doi.org/10.1038/s41562-017-0208-0
Henderson, J. M., & Hayes, T. R. (2018). Meaning guides attention in real-world scene images: Evidence from eye movements and meaning maps. Journal of Vision, 18(6), 1–18. https://doi.org/10.1167/18.6.10
Hessels, R. S., Hooge, I. T. C., Snijders, T. M., & Kemner, C. (2014). Is there a limit to the superiority of individuals with ASD in visual search? Journal of Autism and Developmental Disorders, 44(2), 443–451. https://doi.org/10.1007/s10803-013-1886-8
Horder, J., Wilson, C. E., Mendez, M. A., & Murphy, D. G. (2014). Autistic traits and abnormal sensory experiences in adults. Journal of Autism and Developmental Disorders, 44(6), 1461–1469. https://doi.org/10.1007/s10803-013-2012-7
Insel, T., Cuthbert, B., Garvey, M., Heinssen, R., Pine, D. S., Quinn, K., Sanislow, C., & Wang, P. (2010). Research Domain Criteria (RDoC): Toward a new classification framework for research on mental disorders. In American Journal of Psychiatry (Vol. 167, Issue 7, pp. 748–751). American Psychiatric Association. https://doi.org/10.1176/appi.ajp.2010.09091379
Iossifov, I., O’roak, B. J., Sanders, S. J., Ronemus, M., Krumm, N., Levy, D., Stessman, H. A., Witherspoon, K. T., Vives, L., Patterson, K. E., & Smith, J. D. (2014). The contribution of de novo coding mutations to autism spectrum disorder. Nature, 515(7526), 216–221. https://doi.org/10.1038/nature13908
John, B., Raiturkar, P., Le Meur, O., & Jain, E. (2019). A benchmark of four methods for generating 360° saliency maps from eye tracking data. International Journal of Semantic Computing, 13(3), 329–341. https://doi.org/10.1142/S1793351X19400142
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
Kaufman, A. S., & Kaufman, N. L. (2004). Kaufman brief intelligence test, 2, Ed. Pearson Inc.
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.e3. https://doi.org/10.1016/j.cub.2017.10.007
Kojovic, N., Hadid, L. B., Franchini, M., & Schaer, M. (2019). Sensory processing issues and their association with social difficulties in children with Autism spectrum disorders. Journal of Clinical Medicine. https://doi.org/10.3390/jcm8101508
Kumar, R. A., Karamohamed, S., Sudi, J., Conrad, D. F., Brune, C., Badner, J. A., Gilliam, T. C., Nowak, N. J., Cook, E. H., Dobyns, W. B., & Christian, S. L. (2008). Recurrent 16p11.2 microdeletions in autism. Human Molecular Genetics, 17(4), 628–638. https://doi.org/10.1093/hmg/ddm376
Peterson, M. F., Lin, J., Zaun, I., & Kanwisher, N. (2016). Individual differences in face-looking behavior generalize from the lab to the world. Journal of Vision, 16(7), 12–12. https://doi.org/10.1167/16.7.12
Plaisted, K., O’Riordan, M., & Baron-Cohen, S. (1998). Enhanced visual search for a conjunctive target in autism: A research note. Journal of Child Psychology and Psychiatry, 39(5), 777–783. https://doi.org/10.1111/1469-7610.00376
Robertson, C. E., & Baron-Cohen, S. (2017). Sensory perception in autism. Nature Reviews Neuroscience, 18(11), 671–684. https://doi.org/10.1038/nrn.2017.112
Robertson, C. E., Kravitz, D. J., Freyberg, J., Baron-Cohen, S., & Baker, C. I. (2013). Tunnel vision: Sharper gradient of spatial attention in autism. Journal of Neuroscience, 33(16), 6776–6781. https://doi.org/10.1523/JNEUROSCI.5120-12.2013
Ronconi, L., Devita, M., Molteni, M., Gori, S., & Facoetti, A. (2018). Brief report: When large becomes slow: Zooming-out visual attention is associated to orienting deficits in autism. Journal of Autism and Developmental Disorders, 48(7), 2577–2584. https://doi.org/10.1007/s10803-018-3506-0
Sabatos-DeVito, M., Schipul, S. E., Bulluck, J. C., Belger, A., & Baranek, G. T. (2016). Eye tracking reveals impaired attentional disengagement associated with sensory response patterns in children with autism. Journal of Autism and Developmental Disorders, 46(4), 1319–1333. https://doi.org/10.1007/s10803-015-2681-5
Shinawi, M., Liu, P., Kang, S. H. L., Shen, J., Belmont, J. W., Scott, D. A., Probst, F. J., Craigen, W. J., Graham, B. H., Pursley, A., & Clark, G. (2010). Recurrent reciprocal 16p11.2 rearrangements associated with global developmental delay, behavioural problems, dysmorphism, epilepsy, and abnormal head size. Journal of Medical Genetics, 47(5), 332–341. https://doi.org/10.1136/jmg.2009.073015
Sitzmann, V., Serrano, A., Pavel, A., Agrawala, M., Gutierrez, D., Masia, B., & Wetzstein, G. (2018). Saliency in VR: How do people explore virtual environments? IEEE Transactions on Visualization and Computer Graphics, 24(4), 1633–1642. https://doi.org/10.1109/TVCG.2018.2793599
Tavassoli, T., Miller, L. J., Schoen, S. A., Nielsen, D. M., & Baron-Cohen, S. (2014). Sensory over-responsivity in adults with autism spectrum conditions. Autism, 18(4), 428–432. https://doi.org/10.1177/1362361313477246
Tomchek, S. D., Huebner, R. A., & Dunn, W. (2014). Patterns of sensory processing in children with an autism spectrum disorder. Research in Autism Spectrum Disorders, 8(9), 1214–1224. https://doi.org/10.1016/j.rasd.2014.06.006
Wang, S., Jiang, M., Duchesne, X. M., Laugeson, E. A., Kennedy, D. P., Adolphs, R., & Zhao, Q. (2015). Atypical visual saliency in Autism Spectrum Disorder quantified through model-based eye tracking. Neuron, 88(3), 604–616. https://doi.org/10.1016/j.neuron.2015.09.042
Wass, S. V., Smith, T. J., & Johnson, M. H. (2013). Parsing eye-tracking data of variable quality to provide accurate fixation duration estimates in infants and adults. Behavior Research Methods, 45(1), 229–250. https://doi.org/10.3758/s13428-012-0245-6
Weiss, L. A., Shen, Y., Korn, J. M., Arking, D. E., Miller, D. T., Fossdal, R., Saemundsen, E., Stefansson, H., Ferreira, M. A., Green, T., & Platt, O. S. (2008). Association between microdeletion and microduplication at 16p11.2 and autism. New England Journal of Medicine, 358(7), 667–675. https://doi.org/10.1056/nejmoa075974
Xu, J., Jiang, M., Wang, S., Kankanhalli, M. S., & Zhao, Q. (2014). Predicting human gaze beyond pixels. Journal of Vision, 14(1), 28–28. https://doi.org/10.1167/14.1.28
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Funding was provided by Nancy Lurie Marks Family Foundation and Simons Foundation Autism Research Initiative (Grant Number 597694).
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CER conceived the idea and designed the research. JM, CVW, AJH, and YBC collected the data. AJH and JM analyzed the data. AJH, JM, and CER wrote the manuscript.
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Haskins, A.J., Mentch, J., Van Wicklin, C. et al. Brief Report: Differences in Naturalistic Attention to Real-World Scenes in Adolescents with 16p.11.2 Deletion. J Autism Dev Disord 54, 1078–1087 (2024). https://doi.org/10.1007/s10803-022-05850-2
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DOI: https://doi.org/10.1007/s10803-022-05850-2