Context Modulates Attention to Faces in Dynamic Social Scenes in Children and Adults with Autism Spectrum Disorder

Dzmitry A Kaliukhovich, Nikolay V Manyakov, Abigail Bangerter, Gahan Pandina, Dzmitry A Kaliukhovich, Nikolay V Manyakov, Abigail Bangerter, Gahan Pandina

Abstract

Individuals with autism spectrum disorder (ASD) have been found to view social scenes differently compared to typically developing (TD) peers, but results can vary depending on context and age. We used eye-tracking in children and adults (age 6-63) to assess allocation of visual attention in a dynamic social orientation paradigm previously used only in younger children. The ASD group (n = 94) looked less at the actor's face compared to TD (n = 38) when they were engaged in activity (mean percentage of looking time, ASD = 30.7% vs TD = 34.9%; Cohen's d = 0.56; p value < 0.03) or looking at a moving toy (24.5% vs 33.2%; d = 0.65; p value < 0.001). Findings indicate that there are qualitative differences in allocation of visual attention to social stimuli across ages in ASD.ClinicalTrials.gov identifier: NCT02668991.

Keywords: Autism spectrum disorder; Biomarkers; Eye-tracking; Faces; Social attention.

Conflict of interest statement

All authors are employees of Janssen Research & Development, LLC and hold company stocks/stock options. The authors have no relevant non-financial interests to disclose.

© 2021. Janssen Research & Development, LLC.

Figures

Fig. 1
Fig. 1
Stimuli and stimulus conditions. Each of the four stimulus conditions is represented by a single frame from each of the two video stimuli. One video shows a female actor (A), whereas the other shows a male actor (B). Stimulus conditions are indicated in bold above the frames in the first row (A)
Fig. 2
Fig. 2
Distributions of % looking time for each stimulus condition, group of participants and region-of-interest separately. The data are summarized in a form of boxplots. Black dots in each panel denote individual participants. The white and grey boxplots correspond to the data of individuals with ASD and TD controls, respectively. ‘n’ indicates the number of participants. Only significant between-group differences are shown. *p value < 0.05, **p value < 0.005 (corrected for multiple comparisons for each stimulus condition separately using the Tukey–Kramer method) (Color figure online)
Fig. 3
Fig. 3
Distributions of % looking time for the core features of faces for each stimulus condition and group of participants separately. The data are summarized in a form of boxplots. Black dots in each panel denote individual participants. The white and grey boxplots correspond to the data of individuals with ASD and TD controls, respectively. ‘n’ indicates the number of participants. Only significant between-group differences are shown. **p value < 0.005 (corrected for multiple comparisons for each stimulus condition separately using the Tukey–Kramer method) (Color figure online)

References

    1. Aman MG, Novotny S, Samango-Sprouse C, Lecavalier L, Leonard E, Gadow KD, King BH, Pearson DA, AnnGernsbacher M, Chez M. Outcome measures for clinical drug trials in autism. CNS Spectrums. 2004;9(1):36–47. doi: 10.1017/s1092852900008348.
    1. Aman MG, Singh NN. Aberrant behavior checklist manual. 2. Slosson Educational Publications Inc.; 2017.
    1. Avni I, Meiri G, Bar-Sinai A, Reboh D, Manelis L, Flusser H, Michaelovski A, Menashe I, Dinstein I. Children with autism observe social interactions in an idiosyncratic manner. Autism Research. 2020;13(6):935–946. doi: 10.1002/aur.2234.
    1. Bangerter A, Chatterjee M, Manfredonia J, Manyakov NV, Ness S, Boice MA, Skalkin A, Goodwin MS, Dawson G, Hendren R, Leventhal B, Shic F, Pandina G. Automated recognition of spontaneous facial expression in individuals with autism spectrum disorder: Parsing response variability. Molecular Autism. 2020;11(1):31. doi: 10.1186/s13229-020-00327-4.
    1. Bangerter A, Chatterjee M, Manyakov NV, Ness S, Lewin D, Skalkin A, Boice M, Goodwin MS, Dawson G, Hendren R, Leventhal B, Shic F, Esbensen A, Pandina G. Relationship between sleep and behavior in autism spectrum disorder: Exploring the impact of sleep variability. Frontiers in Neuroscience. 2020;14:211. doi: 10.3389/fnins.2020.00211.
    1. Bangerter A, Ness S, Aman MG, Esbensen AJ, Goodwin MS, Dawson G, Hendren R, Leventhal B, Khan A, Opler M, Harris A, Pandina G. Autism behavior inventory: A novel tool for assessing core and associated symptoms of autism spectrum disorder. Journal of Child and Adolescent Psychopharmacology. 2017;27(9):814–822. doi: 10.1089/cap.2017.0018.
    1. Baron-Cohen S, Wheelwright S, Hill J, Raste Y, Plumb I. The “reading the mind in the eyes” test revised version: A study with normal adults, and adults with Asperger syndrome or high-functioning autism. Journal of Child Psychology and Psychiatry. 2001;42(2):241–251. doi: 10.1111/1469-7610.00715.
    1. Blignaut P, Wium D. Eye-tracking data quality as affected by ethnicity and experimental design. Behavior Research Methods. 2014;46(1):67–80. doi: 10.3758/s13428-013-0343-0.
    1. Campbell DJ, Shic F, Macari S, Chawarska K. Gaze response to dyadic bids at 2 years related to outcomes at 3 years in autism spectrum disorders: A subtyping analysis. Journal of Autism and Developmental Disorders. 2014;44(2):431–442. doi: 10.1007/s10803-013-1885-9.
    1. Caruana N, Stieglitz Ham H, Brock J, Woolgar A, Kloth N, Palermo R, McAethur G. Joint attention difficulties in autistic adults: An interactive eye-tracking study. Autism. 2018;22(4):502–512. doi: 10.1177/1362361316676204.
    1. Chawarska K, Macari S, Shic F. Context modulates attention to social scenes in toddlers with autism. Journal of Child Psychology and Psychiatry. 2012;53(8):903–913. doi: 10.1111/j.1469-7610.2012.02538.x.
    1. Chawarska K, Macari S, Shic F. Decreased spontaneous attention to social scenes in 6-month-old infants later diagnosed with autism spectrum disorders. Biological Psychiatry. 2013;74(3):195–203. doi: 10.1016/j.biopsych.2012.11.022.
    1. Chawarska K, Ye S, Shic F, Chen L. Multilevel differences in spontaneous social attention in toddlers with autism spectrum disorder. Child Development. 2016;87(2):543–557. doi: 10.1111/cdev.12473.
    1. Chevallier C, Parish-Morris J, McVey A, Rump KM, Sasson NJ, Herrington JD, Schultz RT. Measuring social attention and motivation in autism spectrum disorder using eye-tracking: Stimulus type matters. Autism Research. 2015;8(5):620–628. doi: 10.1002/aur.1479.
    1. Chita-Tegmark M. Social attention in ASD: A review and meta-analysis of eye-tracking studies. Research in Developmental Disabilities. 2016;48:79–93. doi: 10.1016/j.ridd.2015.10.011.
    1. Constantino JN, Davis SA, Todd RD, Schindler MK, Gross MM, Brophy SL, Metzger LM, Shoushtari CS, Splinter R, Reich W. 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. 2003;33(4):427–433. doi: 10.1023/a:1025014929212.
    1. Dawson G, Meltzoff AN, Osterling J, Rinaldi J, Brown E. Children with autism fail to orient to naturally occurring social stimuli. Journal of Autism and Developmental Disorders. 1998;28(6):479–485. doi: 10.1023/a:1026043926488.
    1. Del Bianco T, Mazzoni N, Bentenuto A, Venuti P. An investigation of attention to faces and eyes: Looking time is task-dependent in autism spectrum disorder. Frontiers in Psychology. 2018;9:2629. doi: 10.3389/fpsyg.2018.02629.
    1. Fletcher-Watson S, Leekam SR, Benson V, Frank MC, Findlay JM. Eye-movements reveal attention to social information in autism spectrum disorder. Neuropsychologia. 2009;47(1):248–257. doi: 10.1016/j.neuropsychologia.2008.07.016.
    1. Fox J, Weisberg S. An R companion to applied regression. 2. Sage; 2011.
    1. Frazier TW, Klingemier EW, Parikh S, Speer L, Strauss MS, Eng C, Harden AY, Youngstrom EA. Development and validation of objective and quantitative eye tracking-based measures of autism risk and symptom levels. Journal of the American Academy of Child and Adolescent Psychiatry. 2018;57(11):858–866. doi: 10.1016/j.jaac.2018.06.023.
    1. Frazier TW, Strauss M, Klingemier EW, Zetzer EE, Hardan AY, Eng C, Youngstrom EA. 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. 2017;56(7):546–555. doi: 10.1016/j.jaac.2017.05.005.
    1. Freeth M, Bugembe P. Social partner gaze direction and conversational phase; factors affecting social attention during face-to-face conversations in autistic adults? Autism. 2019;23(2):503–513. doi: 10.1177/1362361318756786.
    1. Freeth M, Chapman P, Ropar D, Mitchell P. Do gaze cues in complex scenes capture and direct the attention of high functioning adolescents with ASD? Evidence from eye-tracking. Journal of Autism and Developmental Disorders. 2010;40(5):534–547. doi: 10.1007/s10803-009-0893-2.
    1. Frischen A, Bayliss AP, Tipper SP. Gaze cueing of attention: Visual attention, social cognition, and individual differences. Psychological Bulletin. 2007;133(4):694–724. doi: 10.1037/0033-2909.133.4.694.
    1. Frost-Karlsson M, Galazka MA, Gillberg C, Gillberg C, Miniscalco C, Billstedt E, Hadjikhani N, Åsberg Johnels J. Social scene perception in autism spectrum disorder: An eye-tracking and pupillometric study. Journal of Clinical and Experimental Neuropsychology. 2019;41(10):1024–1032. doi: 10.1080/13803395.2019.1646214.
    1. Fujioka T, Tsuchiya KJ, Saito M, Hirano Y, Matsuo M, Kikuchi M, Maegaki Y, Choi D, Kato S, Yoshida T, Yoshimura Y, Ooba S, Mizuno Y, Takiguchi S, Matsuzaki H, Tomoda A, Shudo K, Ninomiya M, Katayama T, Kosaka H. Developmental changes in attention to social information from childhood to adolescence in autism spectrum disorders: A comparative study. Molecular Autism. 2020;11(1):24. doi: 10.1186/s13229-020-00321-w.
    1. Gadow K, Sprafkin J. Early childhood inventory-4 norms manual. Checkmate Plus; 1997.
    1. Grossman RB, Zane E, Mertens J, Mitchell T. Facetime vs. Screentime: Gaze patterns to live and video social stimuli in adolescents with ASD. Scientific Reports. 2019;9(1):12643. doi: 10.1038/s41598-019-49039-7.
    1. Guillon Q, Hadjikhani N, Baduel S, Roge B. Visual social attention in autism spectrum disorder: Insights from eye tracking studies. Neuroscience and Biobehavioral Reviews. 2014;42:279–297. doi: 10.1016/j.neubiorev.2014.03.013.
    1. Hanley M, Riby DM, Carty C, Melaugh McAteer A, Kennedy A, McPhillips M. The use of eye-tracking to explore social difficulties in cognitively able students with autism spectrum disorder: A pilot investigation. Autism. 2015;19(7):868–873. doi: 10.1177/1362361315580767.
    1. Heaton TJ, Freeth M. Reduced visual exploration when viewing photographic scenes in individuals with autism spectrum disorder. Journal of Abnormal Psychology. 2016;125(3):399–411. doi: 10.1037/abn0000145.
    1. Hessels R, Holleman G, Cornelissen T, Hooge I, Kemner C. Eye contact takes two—Autistic and social anxiety traits predict gaze behavior in dyadic interaction. Journal of Experimental Psychopathology. 2018;9(2):jep.062917. doi: 10.5127/jep.062917.
    1. Hirose Y, Kennedy A, Tatler BW. Perception and memory across viewpoint changes in moving images. Journal of Vision. 2010;10(4):1–19. doi: 10.1167/10.4.2.
    1. Hutchins T, Brien A. Conversational topic moderates social attention in autism spectrum disorder: Talking about emotions is like driving in a snowstorm. Research in Autism Spectrum Disorders. 2016;26:99–110. doi: 10.1016/j.rasd.2016.03.006.
    1. Jagannatha S, Sargsyan D, Manyakov N, Skalkin A, Bangerter A, Ness S, Lewin D, Johnson K, Durham K, Pandina G. A practical application of data mining methods to build predictive models for autism spectrum disorder based on biosensor data from Janssen autism knowledge engine (JAKE®) Statistics in Biopharmaceutical Research. 2019;11(2):111–117. doi: 10.1080/19466315.2018.1527247.
    1. Jones W, Klin A. Attention to eyes is present but in decline in 2–6-month-old infants later diagnosed with autism. Nature. 2013;504(7480):427–431. doi: 10.1038/nature12715.
    1. Kaufman A, Kaufman N. Kaufman brief intelligence test. 2. Pearson Inc.; 2004.
    1. Kim S. ppcor: An R package for a fast calculation to semi-partial correlation coefficients. Communications for Statistical Applications and Methods. 2015;22(6):665–674. doi: 10.5351/CSAM.2015.22.6.665.
    1. Klin A, Jones W, Schultz R, Volkmar F, Cohen D. Visual fixation patterns during viewing of naturalistic social situations as predictors of social competence in individuals with autism. Archives of General Psychiatry. 2002;59(9):809–816. doi: 10.1001/archpsyc.59.9.809.
    1. Kwon MK, Moore A, Barnes CC, Cha D, Pierce K. Typical levels of eye-region fixation in toddlers with autism spectrum disorder across multiple contexts. Journal of the American Academy of Child and Adolescent Psychiatry. 2019;58(10):1004–1015. doi: 10.1016/j.jaac.2018.12.011.
    1. Lam KS, Aman MG. The repetitive behavior scale-revised: Independent validation in individuals with autism spectrum disorders. Journal of Autism and Developmental Disorders. 2007;37(5):855–866. doi: 10.1007/s10803-006-0213-z.
    1. Lenth R. Least-squares means: The R package lsmeans. Journal of Statistical Software. 2016 doi: 10.18637/jss.v069.i01.
    1. Lord C, Luyster R, Gotham K, Guthrie W. Autism Diagnostic Observation Schedule, Second Edition (ADOS-2) Western Psychological Services; 2012.
    1. Macari S, Milgramm A, Reed J, Shic F, Powell KK, Macris D, Chawarska K. Context-specific dyadic attention vulnerabilities during the first year in infants later developing autism spectrum disorder. Journal of the American Academy of Child and Adolescent Psychiatry. 2021;60(1):166–175. doi: 10.1016/j.jaac.2019.12.012.
    1. Manfredonia J, Bangerter A, Manyakov NV, Ness S, Lewin D, Skalkin A, Boice M, Goodwin MS, Dawson G, Hendren R, Leventhal B, Shic F, Pandina G. Automatic recognition of posed facial expression of emotion in individuals with autism spectrum disorder. Journal of Autism and Developmental Disorders. 2019;49(1):279–293. doi: 10.1007/s10803-018-3757-9.
    1. Manyakov NV, Bangerter A, Chatterjee M, Mason L, Ness S, Lewin D, Skalkin A, Boice M, Goodwin MS, Dawson G, Hendren R, Leventhal B, Shic F, Pandina G. Visual exploration in autism spectrum disorder: Exploring age differences and dynamic features using recurrence quantification analysis. Autism Research. 2018;11(11):1554–1566. doi: 10.1002/aur.2021.
    1. Murias M, Major S, Davlantis K, Franz L, Harris A, Rardin B, Sabatos-DeVito M, Dawson G. Validation of eye-tracking measures of social attention as a potential biomarker for autism clinical trials. Autism Research. 2018;11(1):166–174. doi: 10.1002/aur.1894.
    1. Ness SL, Manyakov NV, Bangerter A, Lewin D, Jagannatha S, Boice M, Skalkin A, Dawson G, Janvier YM, Goodwin MS, Hendren R, Leventhal B, Shic F, Cioccia W, Pandina G. JAKE(R) multimodal data capture system: Insights from an observational study of autism spectrum disorder. Frontiers in Neuroscience. 2017;11:517. doi: 10.3389/fnins.2017.00517.
    1. Peterson MF, Eckstein MP. Looking just below the eyes is optimal across face recognition tasks. Proceeding of the National Academy of Sciences USA. 2012;109(48):E3314–3323. doi: 10.1073/pnas.1214269109.
    1. Pinheiro, J., Bates, D., DebRoy, S., & Sarkar, D. (2018). nlme: linear and nonlinear mixed effects models. R package version 3.1–137. Retrieved from
    1. Plesa Skwerer D, Brukilacchio B, Chu A, Eggleston B, Meyer S, Tager-Flusberg H. Do minimally verbal and verbally fluent individuals with autism spectrum disorder differ in their viewing patterns of dynamic social scenes? Autism. 2019;23(8):2131–2144. doi: 10.1177/1362361319845563.
    1. Risko E, Richardson D, Kingstone A. Breaking the fourth wall of cognitive science: Real-world social attention and the dual function of gaze. Current Directions in Psychological Science. 2016;25(1):70–74. doi: 10.1177/0963721415617806.
    1. Rutter M, Bailey A, Lord C. Social communication questionnaire. Western Psychological Services; 2003.
    1. Sargsyan D, Jagannatha S, Manyakov N, Skalkin A, Bangerter A, Ness S. Feature selection with weighted importance index in an autism spectrum disorder study. Statistics in Biopharmaceutical Research. 2017;11:118–125. doi: 10.1080/19466315.2018.1537886.
    1. Senju A, Csibra G, Johnson MH. Understanding the referential nature of looking: Infants’ preference for object-directed gaze. Cognition. 2008;108(2):303–319. doi: 10.1016/j.cognition.2008.02.009.
    1. Sheehan DV, Lecrubier Y, Sheehan KH, Amorim P, Janavs J, Weiller E, Hergueta T, Baker R, Dunbar GC. The mini-international neuropsychiatric interview (MINI): The development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. Journal of Clinical Psychiatry. 1998;59(Suppl 20):22–33.
    1. Sheehan DV, Sheehan KH, Shytle RD, Janavs J, Bannon Y, Rogers JE, Milo KM, Stock SL, Wilkinson B. Reliability and validity of the mini international neuropsychiatric interview for children and adolescents (MINI-KID) Journal of Clinical Psychiatry. 2010;71(3):313–326. doi: 10.4088/JCP.09m05305whi.
    1. Vabalas A, Freeth M. Brief report: Patterns of eye movements in face to face conversation are associated with autistic traits: Evidence from a student sample. Journal of Autism and Developmental Disorders. 2016;46(1):305–314. doi: 10.1007/s10803-015-2546-y.
    1. Wang Q, Campbell DJ, Macari SL, Chawarska K, Shic F. Operationalizing atypical gaze in toddlers with autism spectrum disorders: A cohesion-based approach. Molecular Autism. 2018;9:25. doi: 10.1186/s13229-018-0211-y.

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