Measuring social attention and motivation in autism spectrum disorder using eye-tracking: Stimulus type matters

Coralie Chevallier, Julia Parish-Morris, Alana McVey, Keiran M Rump, Noah J Sasson, John D Herrington, Robert T Schultz, Coralie Chevallier, Julia Parish-Morris, Alana McVey, Keiran M Rump, Noah J Sasson, John D Herrington, Robert T Schultz

Abstract

Autism Spectrum Disorder (ASD) is characterized by social impairments that have been related to deficits in social attention, including diminished gaze to faces. Eye-tracking studies are commonly used to examine social attention and social motivation in ASD, but they vary in sensitivity. In this study, we hypothesized that the ecological nature of the social stimuli would affect participants' social attention, with gaze behavior during more naturalistic scenes being most predictive of ASD vs. typical development. Eighty-one children with and without ASD participated in three eye-tracking tasks that differed in the ecological relevance of the social stimuli. In the "Static Visual Exploration" task, static images of objects and people were presented; in the "Dynamic Visual Exploration" task, video clips of individual faces and objects were presented side-by-side; in the "Interactive Visual Exploration" task, video clips of children playing with objects in a naturalistic context were presented. Our analyses uncovered a three-way interaction between Task, Social vs. Object Stimuli, and Diagnosis. This interaction was driven by group differences on one task only-the Interactive task. Bayesian analyses confirmed that the other two tasks were insensitive to group membership. In addition, receiver operating characteristic analyses demonstrated that, unlike the other two tasks, the Interactive task had significant classification power. The ecological relevance of social stimuli is an important factor to consider for eye-tracking studies aiming to measure social attention and motivation in ASD.

Keywords: autism spectrum disorder; eye-tracking; face processing; methodology; social attention; social motivation.

© 2015 International Society for Autism Research, Wiley Periodicals, Inc.

Figures

Figure 1
Figure 1
Representative stimuli for each task: (A) “Static Visual Exploration” task, (B) “Dynamic Visual Exploration” task, and (C) “Interactive Visual Exploration” task.
Figure 2
Figure 2
Receiver operating characteristic (ROC) curves comparing the sensitivity and specificity of the Face prioritization index in the Interactive task (black), the Dynamic task (dark gray) and the Static task (light gray).

References

    1. Bar-Haim Y, Shulman C, Lamy D, Reuveni A. Attention to Eyes and Mouth in High-Functioning Children with Autism. Journal of Autism and Developmental Disorders. 2006;36(1):131–137.
    1. Birmingham E, Cerf M, Adolphs R. Comparing social attention in autism and amygdala lesions: Effects of stimulus and task condition. Social Neuroscience. 2011;6(5-6):420–435.
    1. Blatter K, Schultz W. Rewarding properties of visual stimuli. Experimental Brain Research. 2006;168(4):541–546.
    1. Boyd BA, Conroy MA, Mancil GR, Nakao T, Alter PJ. Effects of circumscribed interests on the social behaviors of children with autism spectrum disorders. Journal of Autism and Developmental Disorders. 2007;37(8):1550–1561.
    1. Butler RA, Woolpy JH. Visual attention in the rhesus monkey. Journal of Comparative and Physiological Psychology. 1963;56(2):324.
    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.
    1. Chevallier C, Kohls G, Troiani V, Brodkin ES, Schultz RT. The social motivation theory of autism. Trends in Cognitive Sciences 2012
    1. Dalton KM, Nacewicz BM, Johnstone T, Schaefer HS, Gernsbacher MA, Goldsmith HH, et al. Davidson RJ. Gaze fixation and the neural circuitry of face processing in autism. Nature Neuroscience. 2005;8(4):519–526.
    1. Dawson G, Webb S, McPartland J. Understanding the nature of face processing impairment in autism: Insights from behavioral and electrophysiological studies. Developmental Neuropsychology. 2005;27(3):403–424.
    1. Dennis M, Francis DJ, Cirino PT, Schachar R, Barnes MA, Fletcher JM. Why IQ is not a covariate in cognitive studies of neurodevelopmental disorders. Journal of the International Neuropsychological Society: JINS. 2009;15(3):331–343. doi: 10.1017/S1355617709090481.
    1. Dichter GS, Richey JA, Rittenberg AM, Sabatino A, Bodfish JW. Reward Circuitry Function in Autism During Face Anticipation and Outcomes. Journal of Autism and Developmental Disorders. 2012;42(2):147–160.
    1. Dienes Z. Understanding psychology as a science: An introduction to scientific and statistical inference. 2008 Retrieved from .
    1. Dienes Z. Bayesian versus orthodox statistics: Which side are you on? Perspectives on Psychological Science. 2011;6(3):274–290.
    1. Elliott C. Differential Ability Scales-II (DAS-II) San Antonio, Texas: The Psychological Corporation; 2007. Retrieved from .
    1. Falck-Ytter T, Bölte S, Gredebäck G. Eye tracking in early autism research. Journal of Neurodevelopmental Disorders. 2013;528(1)
    1. Falck-Ytter T, von Hofsten C. How special is social looking in ASD: a review. Progress in Brain Research. 2010;189:209–222.
    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.
    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.
    1. Guillon Q, Hadjikhani N, Baduel S, Rogé B. Visual social attention in autism spectrum disorder: Insights from eye tracking studies. Neuroscience & Biobehavioral Reviews. 2014;42:279–297.
    1. Hanley M, McPhillips M, Mulhern G, Riby DM. Spontaneous attention to faces in Asperger Syndrome using ecologically valid static stimuli. Autism. 2012 Retrieved from .
    1. Horlin C, Falkmer M, Fitzgerald P, Leung D, Ordqvist A, Falkmer T. The influence of static versus naturalistic stimuli on face processing in children with and without Asperger syndrome or high-functioning autism. Research in Autism Spectrum Disorders. 2013;7(12):1617–1624.
    1. Humphrey NK. “Interest” and ‘pleasure’: two determinants of a monkey's visual preferences. Perception. 1972;1:395–416.
    1. Klin A, Jones W, Schultz R, Volkmar F. The enactive mind, or from actions to cognition: lessons from autism. Philosophical Transactions: Biological Sciences. 2003;358(1430):345–360.
    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.
    1. Kohls G, Chevallier C, Troiani V, Schultz RT. Social ‘wanting’ dysfunction in autism: neurobiological underpinnings and treatment implications. J Neurodevelopmental Disord. 2012;4(10) Retrieved from .
    1. Miller GA, Chapman JP. Misunderstanding analysis of covariance. Journal of Abnormal Psychology. 2001;110(1):40.
    1. Noris B, Nadel J, Barker M, Hadjikhani N, Billard A. Investigating gaze of children with ASD in naturalistic settings. PloS One. 2012;7(9):e44144. doi: 10.1371/journal.pone.0044144.
    1. Parish-Morris J, Chevallier C, Tonge N, Letzen J, Pandey J, Schultz RT. Visual attention to dynamic faces and objects is linked to face processing skills: a combined study of children with autism and controls. Frontiers in Psychology. 2013;4 Retrieved from
    1. Pelphrey KA, Sasson NJ, Reznick JS, Paul G, Goldman BD, Piven J. Visual scanning of faces in autism. Journal of Autism and Developmental Disorders. 2002;32(4):249–261.
    1. Riby D, Hancock PJ. Looking at movies and cartoons: eye-tracking evidence from Williams syndrome and autism. Journal of Intellectual Disability Research. 2009;53(2):169–181.
    1. Risko EF, Laidlaw KE, Freeth M, Foulsham T, Kingstone A. Social attention with real versus reel stimuli: toward an empirical approach to concerns about ecological validity. Frontiers in Human Neuroscience. 2012;6 Retrieved from
    1. Saitovitch A, Bargiacchi A, Chabane N, Philippe A, Samson Y, Zilbovicius M. Studying Gaze abnormalities in autism, Which type of stimulus to use. Open Journal of Psychiatry. 2013;3:32–38.
    1. Sasson NJ, Touchstone EW. Visual attention to competing social and object images by preschool children with autism spectrum disorder. Journal of Autism and Developmental Disorders. 2014;44:584–592.
    1. Sasson NJ, Elison JT, Turner-Brown LM, Dichter GS, Bodfish JW. Brief report: Circumscribed attention in young children with autism. Journal of Autism and Developmental Disorders. 2011;41(2):242–247.
    1. Sasson NJ, Turner Brown LM, Holtzclaw TN, Lam KSL, Bodfish JW. Children with autism demonstrate circumscribed attention during passive viewing of complex social and nonsocial picture arrays. Autism Research. 2008;1(1):31–42.
    1. Schultz W. Behavioral theories and the neurophysiology of reward. Annu Rev Psychol. 2006;57:87–115.
    1. South M, Ozonoff S, McMahon WM. Repetitive behavior profiles in Asperger syndrome and high-functioning autism. Journal of Autism and Developmental Disorders. 2005;35(2):145–158.
    1. Speer LL, Cook AE, McMahon WM, Clark E. Face processing in children with autism Effects of stimulus contents and type. Autism. 2007;11(3):265–277.
    1. Spezio ML, Adolphs R, Hurley RS, Piven J. Abnormal use of facial information in high-functioning autism. Journal of Autism and Developmental Disorders. 2007;37(5):929–939.
    1. Turner-Brown LM, Lam KSL, Holtzclaw TN, Dichter GS, Bodfish JW. Phenomenology and measurement of circumscribed interests in autism spectrum disorders. Autism. 2011;15(4):437–456.
    1. Van der Geest JN, Kemner C, Camfferman G, Verbaten MN, Van Engeland H. Looking at images with human figures: comparison between autistic and normal children. Journal of Autism and Developmental Disorders. 2002;32(2):69–75.
    1. Van der Geest JN, Kemner C, Verbaten MN, Van Engeland H. Gaze behavior of children with pervasive developmental disorder toward human faces: a fixation time study. Journal of Child Psychology and Psychiatry. 2002;43(5):669–678.
    1. Wang S, Xu J, Jiang M, Zhao Q, Hurlemann R, Adolphs R. Autism spectrum disorder, but not amygdala lesions, impairs social attention in visual search. Neuropsychologia. 2014;63:259–274.
    1. Weisberg J, Milleville SC, Kenworthy L, Wallace GL, Gotts SJ, Beauchamp MS, Martin A. Social perception in autism spectrum disorders: impaired category selectivity for dynamic but not static images in ventral temporal cortex. Cerebral Cortex. 2012 Retrieved from .
    1. Wolf JM, Tanaka JW, Klaiman C, Cockburn J, Herlihy L, Brown C, et al. Specific impairment of face-processing abilities in children with autism spectrum disorder using the Let's Face It! skills battery. Autism Research. 2008;1(6):329–340.

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