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Decreased Spontaneous Attention to Social Scenes in 6-Month-Old Infants Later Diagnosed with Autism Spectrum Disorders

      Background

      The ability to spontaneously attend to the social overtures and activities of others is essential for the development of social cognition and communication. This ability is critically impaired in toddlers with autism spectrum disorders (ASD); however, it is not clear if prodromal symptoms in this area are already present in the first year of life of those affected by the disorder.

      Methods

      To examine whether 6-month-old infants later diagnosed with ASD exhibit atypical spontaneous social monitoring skills, visual responses of 67 infants at high-risk and 50 at low-risk for ASD were studied using an eye-tracking task. Based on their clinical presentation in the third year, infants were divided into those with ASD, those exhibiting atypical development, and those developing typically.

      Results

      Compared with the control groups, 6-month-old infants later diagnosed with ASD attended less to the social scene, and when they did look at the scene, they spent less time monitoring the actress in general and her face in particular. Limited attention to the actress and her activities was not accompanied by enhanced attention to objects.

      Conclusions

      Prodromal symptoms of ASD at 6 months include a diminished ability to attend spontaneously to people and their activities. A limited attentional bias toward people early in development is likely to have a detrimental impact on the specialization of social brain networks and the emergence of social interaction patterns. Further investigation into its underlying mechanisms and role in psychopathology of ASD in the first year is warranted.

      Key Words

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      References

        • U.S. Department of Health & Human Services, Interagency Autism Coordinating Committee
        The 2011 Interagency Autism Coordinating Committee Strategic Plan for Autism Spectrum Disorder Research-January 28, 2011. 2011 (Available at: http://iacc.hhs.gov/strategic-plan/2011/index.shtml. Accessed August 12, 2012)
        • Zwaigenbaum L.
        • Thurm A.
        • Stone W.
        • Baranek G.
        • Bryson S.
        • Iverson J.
        • et al.
        Studying the emergence of autism spectrum disorders in high-risk infants: Methodological and practical issues.
        J Autism Dev Disord. 2007; 37: 466-480
        • Tager-Flusberg H.
        The origins of social impairments in autism spectrum disorder: Studies of infants at risk.
        Neural Netw. 2010; 23: 1072-1076
        • Rogers S.J.
        What are infant siblings teaching us about autism in infancy?.
        Autism Res. 2009; 2: 125-137
        • Macari S.
        • Campbell D.
        • Gengoux G.
        • Saulnier C.
        • Klin A.
        • Chawarska K.
        Predicting developmental status from 12 to 24 months in infants at risk for autism spectrum disorder: A preliminary report.
        J Autism Dev Disord. 2012; 42: 2636-2647
        • Elsabbagh M.
        • Johnson M.H.
        Getting answers from babies about autism.
        Trends Cogn Sci. 2010; 14: 81-87
        • Gupta A.R.
        • State M.W.
        Recent advances in the genetics of autism.
        Biol Psychiatry. 2007; 61: 429-437
        • Fombonne E.
        Epidemiology of pervasive developmental disorders.
        Pediatr Res. 2009; 65: 591-598
        • Yeargin-Allsopp M.
        • Rice C.
        • Karapurkar T.
        • Doernberg N.
        • Boyle C.
        • Murphy C.
        Prevalence of autism in a US metropolitan area [see comment].
        JAMA. 2003; 289: 49-55
        • Baird G.
        • Simonoff E.
        • Pickles A.
        • Chandler S.
        • Loucas T.
        • Meldrum D.
        • Charman T.
        Prevalence of disorders of the autism spectrum in a population cohort of children in South Thames: The Special Needs and Autism Project (SNAP).
        Lancet. 2006; 368: 210-215
        • Autism and Developmental Disabilities Monitoring Network Surveillance Year 2008 Principal Investigators, Centers for Disease Control and Prevention
        Prevalence of autism spectrum disorders— Autism and Developmental Disabilities Monitoring Network, 14 sites, United States, 2008.
        MMWR Surveill Summ. 2012; 61: 1-19
        • Kim Y.S.
        • Leventhal B.L.
        • Koh Y.
        • Fombonne E.
        • Laska E.
        • Lim E.C.
        • et al.
        Prevalence of autism spectrum disorders in a total population sample.
        Am J Psychiatry. 2011; 168: 904-912
        • Ozonoff S.
        • Young G.S.
        • Carter A.
        • Messinger D.
        • Yirmiya N.
        • Zwaigenbaum L.
        • et al.
        Recurrence risk for autism spectrum disorders: A Baby Siblings Research Consortium Study.
        Pediatrics. 2011; 128 (e499–e495)
        • Landa R.J.
        • Holman K.C.
        • Garrett-Mayer E.
        Social and communication development in toddlers with early and later diagnosis of autism spectrum disorders.
        Arch Gen Psychiatry. 2007; 64: 853-864
        • Bedford R.
        • Elsabbagh M.
        • Gliga T.
        • Pickles A.
        • Senju A.
        • Charman T.
        • et al.
        Precursors to social and communication difficulties in infants at-risk for autism: Gaze following and attentional engagement.
        J Autism Dev Disord. 2012; 42: 2208-2218
        • Toth K.
        • Dawson G.
        • Meltzoff A.N.
        • Greenson J.
        • Fein D.
        Early social, imitation, play, and language abilities of young non-autistic siblings of children with autism.
        J Autism Dev Disord. 2007; 37: 145-157
        • Georgiades S.
        • Szatmari P.
        • Boyle M.
        • Hanna S.
        • Duku E.
        • Zwaigenbaum L.
        • et al.
        Investigating phenotypic heterogeneity in children with autism spectrum disorder: A factor mixture modeling approach [published online ahead of print August 1].
        J Child Psychol Psychiatry. 2012;
        • Zwaigenbaum L.
        • Bryson S.
        • Rogers T.
        • Roberts W.
        • Brian J.
        • Szatmari P.
        Behavioral manifestations of autism in the first year of life.
        Int J Dev Neurosci. 2005; 23: 143-152
        • Ozonoff S.
        • Iosif A.
        • Baguio F.
        • Cook I.
        • Hill M.
        • Hutman T.
        • et al.
        A prospective study of the emergence of early behavioral signs of autism.
        J Am Acad Child Adolesc Psychiatry. 2010; 49: 258-268
        • Rozga A.
        • Hutman T.
        • Young G.S.
        • Rogers S.
        • Ozonoff S.
        • Dapretto M.
        • Sigman M.
        Behavioral profiles of affected and unaffected siblings of children with autism: Contribution of measures of mother-infant interaction and nonverbal communication.
        J Autism Dev Disord. 2011; 41: 287-301
        • Hutman T.
        • Rozga A.
        • DeLaurentis A.D.
        • Barnwell J.M.
        • Sugar C.A.
        • Sigman M.
        Response to distress in infants at risk for autism: A prospective longitudinal study.
        J Child Psychol Psychiatry. 2010; 51: 1010-1020
        • Paul R.
        • Fuerst Y.
        • Ramsay G.
        • Chawarska K.
        • Klin A.
        Out of the mouths of babes: Vocal production in infant siblings of children with ASD.
        J Child Psychol Psychiatry. 2011; 52: 588-598
        • Ozonoff S.
        • Macari S.
        • Young G.S.
        • Goldring S.
        • Thompson M.
        • Rogers S.J.
        Atypical object exploration at 12 months of age is associated with autism in a prospective sample.
        Autism. 2008; 12: 457-472
        • Nadig A.S.
        • Ozonoff S.
        • Young G.S.
        • Rozga A.
        • Sigman M.
        • Rogers S.
        A prospective study of response to name in infants at risk for autism [see comment].
        Arch Pediatr Adolesc Med. 2007; 161: 378-383
        • Hutman T.
        • Rozga A.
        • DeLaurentis A.
        • Sigman M.
        • Dapretto M.
        Infants’ pre-empathic behaviors are associated with language skills.
        Infant Behav Dev. 2012; 35: 561-569
        • Luyster R.
        • Gotham K.
        • Guthrie W.
        • Coffing M.
        • Petrak R.
        • Pierce K.
        • et al.
        The Autism Diagnostic Observation Schedule--toddler module: A new module of a standardized diagnostic measure for autism spectrum disorders.
        J Autism Dev Disord. 2009; 39: 1305-1320
        • Young G.S.
        • Merin N.
        • Rogers S.J.
        • Ozonoff S.
        Gaze behavior and affect at 6 months: Predicting clinical outcomes and language development in typically developing infants and infants at risk for autism.
        Dev Sci. 2009; 12: 798-814
        • Noland J.S.
        • Reznick J.
        • Stone W.L.
        • Walden T.
        • Sheridan E.H.
        Better working memory for non-social targets in infant siblings of children with Autism Spectrum Disorder.
        Dev Sci. 2010; 13: 244-251
        • Wolff J.J.
        • Gu H.
        • Gerig G.
        • Elison J.T.
        • Styner M.
        • Gouttard S.
        • Botteron K.N.
        • et al.
        Differences in white matter fiber tract development present from 6 to 24 months in infants with autism.
        Am J Psychiatry. 2012; 169: 589-600
        • Chawarska K.
        • Campbell D.
        • Chen L.
        • Shic F.
        • Klin A.
        • Chang J.
        Early generalized overgrowth in boys with autism.
        Arch Gen Psychiatry. 2011; 68: 1021-1031
        • Elsabbagh M.
        • Mercure E.
        • Hudry K.
        • Chandler S.
        • Pasco G.
        • Charman T.
        • et al.
        Infant neural sensitivity to dynamic eye gaze is associated with later emerging autism.
        Curr Biol. 2012; 22: 338-342
        • Landa R.J.
        • Gross A.L.
        • Stuart E.A.
        • Bauman M.
        Latent class analysis of early developmental trajectory in baby siblings of children with autism.
        J Child Psychol Psychiatry. 2012; 53: 986-996
        • Chawarska K.
        • Macari S.
        • Shic F.
        Context modulates attention to social scenes in toddlers with autism.
        J Child Psychol Psychiatry. 2012; 53: 903-913
        • Shic F.
        • Bradshaw J.
        • Klin A.
        • Scassellati B.
        • Chawarska K.
        Limited activity monitoring in toddlers with autism spectrum disorder.
        Brain Res. 2010; 1380: 246-254
        • Jones W.
        • Carr K.
        • Klin A.
        Absence of preferential looking to the eyes of approaching adults predicts level of social disability in 2-year-old toddlers with autism spectrum disorder.
        Arch Gen Psychiatry. 2008; 65: 946-954
        • Farroni T.
        • Csibra G.
        • Simion F.
        • Johnson M.H.
        Eye contact detection in humans from birth.
        Proc Natl Acad Sci U S A. 2002; 99: 9602-9605
        • Kisilevsky B.S.
        • Hains S.M.J.
        • Brown C.A.
        • Cowperthwaite B.
        • Stutzman S.S.
        • Swansburg M.L.
        • et al.
        Fetal sensitivity to properties of maternal speech and language.
        Infant Behav Dev. 2009; 32: 59-71
        • Vouloumanos A.
        • Hauser M.D.
        • Werker J.F.
        • Martin A.
        The tuning of human neonates’ preference for speech.
        Child Dev. 2010; 81: 517-527
        • Greenough W.T.
        • Black J.E.
        • Wallace C.S.
        Experience and brain development.
        in: Johnson M.H. Munakata Y. Gilmore R. Brain Development and Cognition: A Reader. 2nd ed. Blackwell Publishers, Oxford, UK2002: 186-216
        • Johnson M.H.
        • Grossmann T.
        • Kadosh K.C.
        Mapping functional brain development: Building a social brain through interactive specialization.
        Dev Psychol. 2009; 45: 151-159
        • Lord C.
        • Rutter M.
        • DiLavore P.C.
        • Risi S.
        Autism Diagnostic Observation Schedule. Western Psychological Services, Los Angeles2000
        • Rutter M.
        • Le Couter A.
        • Lord C.
        ADI-R: Autism Diagnostic Interview-Revised. Western Psychological Services, Los Angeles2003
        • Mullen E.
        Mullen Scales of Early Learning. AGS Edition.
        American Guidance Serivce, Inc, Circle Pines, MN1995
        • Wetherby A.M.
        • Prizant B.M.
        Communication and Symbolic Behavior Scales: Developmental Profile.
        1st ed. Paul H. Brookes Publishing Co., Baltimore2002
        • Edwards S.
        • Fletcher P.
        • Garman M.
        • Hughes A.
        • Letts C.
        • Sinka I.
        The Reynell Developmental Language Scales III: The University of Reading Edition.
        NFER-Nelson, London1997
        • MathWorks
        MATLAB 7.8 (Release R2009a) [computer program].
        MathWorks, Natick, MA2009
        • Shic F F.
        Computational Methods for Eye-Tracking Analysis: Applications to Autism.
        Computer Science, Yale University, New Haven, CT2008
        • Duchowski A.T.
        Eye Tracking Methodology: Theory and Practice.
        Springer, New York2003
        • SAS
        SAS Prioprietary Software 9.3 [computer program].
        SAS, Cary, NC2010
        • Wan M.W.
        • Green J.
        • Elsabbagh M.
        • Johnson M.
        • Charman T.
        • Plummer F.
        Parent–infant interaction in infant siblings at risk of autism.
        Res Dev Disabil. 2012; 33: 924-932
        • Nelson C.A.
        • de Haan M.
        • Thomas K.M.
        Neuroscience of Cognitive Development: The Role of Experience and the Developing Brain.
        John Wiley & Sons Inc., Hoboken, NJ2006
        • Pascalis O.
        • de Haan M.
        • Nelson C.A.
        Is face processing species-specific during the first year of life?.
        Science. 2002; 296: 1321-1323
        • Sangrigoli S.
        • de Schonen S.
        Effect of visual experience on face processing: A developmental study of inversion and non-native effects.
        Dev Sci. 2004; 7: 74-87
        • Cheour M.
        • Ceponiene R.
        • Lehtokoski A.
        • Luuk A.
        • Allik J.
        • Alho K.
        • Näätänen R.
        Development of language-specific phoneme representations in the infant brain.
        Nat Neurosci. 1998; 1: 351-353
        • Kuhl P.K.
        • Williams K.A.
        • Lacerda F.
        • Stevens K.N.
        • Lindlom B.
        Linguistic experience alters phonetic perception in infants by 6 months of age.
        Science. 1992; 255: 606-608
        • Elsabbagh M.
        • Volein A.
        • Holmboe K.
        • Tucker L.
        • Csibra G.
        • Baron-Cohen S.
        • et al.
        Visual orienting in the early broader autism phenotype: Disengagement and facilitation.
        J Child Psychol Psychiatry. 2009; 50: 637-642
      1. Campbell D, Shic F, Macari S, Chawarska K. (under review): Gaze patterns in response to dyadic bids at 2 years predict functioning at 3 years in Autism Spectrum Disorders: A subtyping analysis.