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Precursors to Social and Communication Difficulties in Infants At-Risk for Autism: Gaze Following and Attentional Engagement

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Abstract

Whilst joint attention (JA) impairments in autism have been widely studied, little is known about the early development of gaze following, a precursor to establishing JA. We employed eye-tracking to record gaze following longitudinally in infants with and without a family history of autism spectrum disorder (ASD) at 7 and 13 months. No group difference was found between at-risk and low-risk infants in gaze following behaviour at either age. However, despite following gaze successfully at 13 months, at-risk infants with later emerging socio-communication difficulties (both those with ASD and atypical development at 36 months of age) allocated less attention to the congruent object compared to typically developing at-risk siblings and low-risk controls. The findings suggest that the subtle emergence of difficulties in JA in infancy may be related to ASD and other atypical outcomes.

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Abbreviations

AOI:

Area of interest

AT-sibs:

Atypically developing siblings

ADI-R:

Autism Diagnostic Interview-Revised

ADOS-G:

Autism Diagnostic Observation Schedule-Generic

ASD:

Autism spectrum disorder

ASD-sibs:

Autism spectrum disorder siblings

BASIS:

British Autism Study of Infant Siblings

BAP:

Broader autism phenotype

DAWBA:

Development and Wellbeing Assessment

ELC:

Early learning composite

ESCS:

Early Social Communication Scales

EL:

Expressive language

GEE:

Generalised estimating equation

JA:

Joint attention

MSEL:

Mullen Scales of Early Learning

PDD:

Pervasive developmental disorder

RL:

Receptive language

RJA:

Responding to joint attention

SCQ:

Social Communication Questionnaire

TD-sibs:

Typically developing siblings

References

  • Baird, G., Simonoff, E., Pickles, A., Chandler, S., Loucas, T., Meldrum, D., et al. (2006). Prevalence of disorders of the autism spectrum in a population cohort of children in South Thames: The Special Needs and Autism Project (SNAP). Lancet, 368, 210–215.

    Article  PubMed  Google Scholar 

  • Baron-Cohen, S. (1989). Perceptual role taking and protodeclarative pointing in autism. British Journal of Developmental Psychology, 7, 113–127.

    Article  Google Scholar 

  • Baron-Cohen, S. (1995). Mindblindness: An essay on autism and theory of mind. Boston: MIT Press/Bradford Books.

    Google Scholar 

  • Batki, A., Baron-Cohen, S., Wheelwright, S., Connellan, J., & Ahluwalia, J. (2000). Is there an innate gaze module? Evidence from human neonates. Infant Behavior and Development, 23, 223–229.

    Article  Google Scholar 

  • Bolton, P., Macdonald, H., Pickles, A., Rios, P., Goode, S., Crowson, M. E., et al. (1994). A case-control family history study of autism. Journal of Child Psychology and Psychiatry, 35, 877–900.

    Article  PubMed  Google Scholar 

  • Brooks, R., & Meltzoff, A. N. (2005). The development of gaze following and its relation to language. Developmental Science, 8, 535–543.

    Article  PubMed  Google Scholar 

  • Butterworth, G., & Jarrett, N. (1991). What minds have in common in space: Spatial mechanisms serving joint visual attention in infancy. British Journal of Developmental Psychology, 9, 55–72.

    Article  Google Scholar 

  • Caron, A. J., Caron, R., Roberts, J., & Brooks, R. (1997). Infant sensitivity to deviations in dynamic facial-vocal displays: The role of eye regard. Developmental Psychology, 33, 802–813.

    Article  PubMed  Google Scholar 

  • Carpenter, M., Nagell, K., & Tomasello, M. (1998). Social cognition, joint attention, and communicative competence from 9 to 15 months of age. Monographs of the Society for Research in Child Development, 63 (4, Serial No. 255).

  • Cassel, T. D., Messinger, D. S., Ibanez, L. V., Haltigan, J. D., Acosta, S. I., & Buchman, A. C. (2007). Early social and emotional communication in the infant siblings of children with autism spectrum disorders: An examination of the broad phenotype. Journal of Autism and Developmental Disorders, 37, 122–132.

    Article  PubMed  Google Scholar 

  • Charman, T. (2003). Why is joint attention a pivotal skill in autism? Philosophical Transactions of the Royal Society B, 358, 315–324.

    Article  Google Scholar 

  • Charman, T., & Baird, G. (2002). Practitioner review: Assessment and diagnosis of autism spectrum disorders in the pre-school years. Journal of Child Psychology and Psychiatry, 43, 289–305.

    Article  PubMed  Google Scholar 

  • Chawarska, K., Klin, A., & Volkmar, F. (2003). Automatic attention cueing through eye movement in 2-year-old children with autism. Child Development, 74, 1108–1122.

    Article  PubMed  Google Scholar 

  • Constantino, J. N., Zhang, Y., Frazier, T., Abbacchi, A. M., & Law, P. (2010). Sibling recurrence and the genetic epidemiology of autism. American Journal of Psychiatry, 167, 1349–1356.

    Article  PubMed  Google Scholar 

  • Deaner, R. O., & Platt, M. L. (2003). Reflexive social attention in monkeys and humans. Current Biology, 13, 1609–1613.

    Article  PubMed  Google Scholar 

  • Driver, J., Davis, G., Ricciardelli, P., Kidd, P., Maxwell, E., & Baron-Cohen, S. (1999). Gaze perception triggers reflexive visuospatial orienting. Visual Cognition, 6, 509–540.

    Article  Google Scholar 

  • Elsabbagh, M., & Johnson, M. H. (2007). Infancy and autism: Progress, prospects, and challenges. Progress in Brain Research, 164, 355–382.

    Article  PubMed  Google Scholar 

  • Elsabbagh, M., & Johnson, M. H. (2010). Getting answers from babies about autism. Trends in Cognitive Sciences, 14, 81–87.

    Article  PubMed  Google Scholar 

  • Elsabbagh, M., Volein, A., Csibra, G., Holmboe, K., Garwood, H., Tucker, L., et al. (2009). Neural correlates of eye gaze processing in the infant broader autism phenotype. Biological Psychiatry, 65, 31–38.

    Article  PubMed  Google Scholar 

  • Farroni, T., Csibra, G., Simion, F., & Johnson, M. H. (2002). Eye contact detection in humans from birth. Proceedings of the National Academy of Sciences of the United States of America, 99, 9602–9605.

    Article  PubMed  Google Scholar 

  • Farroni, T., Mansfield, E. M., Lai, C., & Johnson, M. H. (2003). Infants perceiving and acting on the eyes: Tests of an evolutionary hypothesis. Journal of Experimental Child Psychology, 85, 199–212.

    Article  PubMed  Google Scholar 

  • Farroni, T., Massaccesi, S., Pividori, D., & Johnson, M. H. (2004). Gaze following in Newborns. Infancy, 5, 39–60.

    Article  Google Scholar 

  • Fombonne, E., Simmons, H., Ford, T., Meltzer, H., & Goodman, R. (2003). Prevalence of pervasive developmental disorders in the British nationwide survey of child mental health. International Review of Psychiatry, 15, 158–165.

    Article  PubMed  Google Scholar 

  • Frischen, A., Bayliss, A. P., & Tipper, S. P. (2007). Gaze cueing of attention. Visual attention, social cognition, and individual differences. Psychological Bulletin, 133, 694–724.

    Article  PubMed  Google Scholar 

  • Goldberg, W. A., Jarvis, K. L., Osann, K., Laulhere, T. M., Straub, C., Thomas, E., et al. (2005). Brief report: Early social communication behaviors in the younger siblings of children with autism. Journal of Autism and Developmental Disorders, 35, 657–664.

    Article  PubMed  Google Scholar 

  • Goodman, R., Ford, T., Richards, H., Gatward, R., & Meltzer, H. (2000). The development and well-being assessment: Description and initial validation of an integrated assessment of child and adolescent psychopathology. Journal of Child Psychology and Psychiatry, 41, 645–655.

    Article  PubMed  Google Scholar 

  • Hare, B., Call, J., & Tomasello, M. (1998). Communication of food location between human and dog (Canis Familiaris). Evolution of Communication, 2, 137–159.

    Google Scholar 

  • Hood, B. M., & Atkinson, J. (1993). Disengaging visual-attention in the infant and adult. Infant Behavior and Development, 16(4), 423–439.

    Article  Google Scholar 

  • Hood, B. M., Willen, J. D., & Driver, J. (1998). Gaze perception triggers corresponding shifts of visual attention in young infants. Psychological Science, 9, 131–134.

    Article  Google Scholar 

  • Landa, R., Holman, K. C., & Garrett-Mayer, E. (2007). Social and communication development in toddlers with early and later diagnosis of autism spectrum disorders. Archives of General Psychiatry, 64, 853–864.

    Article  PubMed  Google Scholar 

  • Lord, C., Risi, S., Lambrecht, L., Cook, E. H., Jr., Leventhal, B. L., DiLavore, P. C., et al. (2000). The autism diagnostic observation schedule-generic: A standard measure of social and communicative deficits associated with the spectrum of autism. Journal of Autism Developmental Disorders, 30, 205–223.

    Article  Google Scholar 

  • Lord, C., Rutter, M. L., & LeCouteur, A. (1994). The autism diagnostic interview-revised: A revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders. Journal of Autism and Developmental Disorders, 24, 659–685.

    Article  PubMed  Google Scholar 

  • Moore, C., & Corkum, V. (1998). Infant gaze following based on eye direction. British Journal of Developmental Psychology, 16, 495–503.

    Article  Google Scholar 

  • Mullen, E. M. (1995). Mullen scales of early learning (AGS ed.). Circle Pines, MN: American Guidance Service Inc.

    Google Scholar 

  • Mundy, P., Hogan, A., & Doehring, P. (1996). A preliminary manual for the abridged early social-communication scales. Coral Gables, FL: University of Miami. www.psy.miami.edu/faculty/pmundy.

  • Mundy, P., Sigman, M., Ungerer, J., & Sherman, T. (1986). Defining the social deficits of autism: The contribution of non-verbal communication measures. Journal of Child Psychology and Psychiatry, 27, 657–669.

    Article  PubMed  Google Scholar 

  • Mundy, P., Sullivan, L., & Mastergeorge, A. M. (2009). A parallel and distributed-processing model of joint attention, social cognition and autism. Autism Research, 2, 2–21.

    Article  PubMed  Google Scholar 

  • Nation, K., & Penny, S. (2008). Sensitivity to eye gaze in autism: Is it normal? Is it automatic? Is it social? Development and Psychopathology, 20, 79–97.

    Article  PubMed  Google Scholar 

  • Ozonoff, S., Young, G. S., Carter, A., Messinger, D., Yirmiya, N., Zwaigenbaum, L., et al. (2011). Recurrence risk for autism spectrum disorders: A baby siblings research consortium study. Pediatrics, 128, e1–e8.

    Article  Google Scholar 

  • Pickles, A. (1998). Generalized estimating equations. In P. Armitage, T. Colton (Eds.), The encyclopedia of biostatistics Vol 2 (pp. 1626–1637). New York: Wiley.

  • Povinelli, D. J., Bierschwale, D. T., & Cech, C. G. (1999). Comprehension of seeing as a referential act in young children, but not juvenile chimpanzees. British Journal of Developmental Psychology, 17, 37–60.

    Article  Google Scholar 

  • Presmanes, A. G., Walden, T. A., Stone, W. L., & Yoder, P. J. (2007). Effects of different attentional cues on responding to joint attention in younger siblings of children with autism spectrum disorders. Journal of Autism and Developmental Disorders, 37, 133–144.

    Article  PubMed  Google Scholar 

  • Risi, S., Lord, C., Gotham, K., Corsello, C., Chrysler, C., Szatmari, P., et al. (2006). Combining information from multiple sources in the diagnosis of autism spectrum disorders. Journal of the American Academy of Child and Adolescent Psychiatry, 45, 1094–1103.

    Article  PubMed  Google Scholar 

  • Rogers, S. J. (2009). What are infant siblings teaching us about autism in infancy? Autism Research, 2, 125–137.

    Article  PubMed  Google Scholar 

  • Rutter, M., Bailey, A., & Lord, C. (2003) SCQ: Social communication questionnaire. Manual. Los Angeles, CA: Western Psychological Services.

  • Scaife, M., & Bruner, J. S. (1975). The capacity for joint visual attention in the infant. Nature, 253, 265–266.

    Article  PubMed  Google Scholar 

  • Senju, A., & Csibra, G. (2008). Gaze following in human infants depends on communicative signals. Current Biology, 18, 668–671.

    Article  PubMed  Google Scholar 

  • Senju, A., Tojo, Y., Dairoku, H., & Hasegawa, T. (2004). Reflexive orienting in response to eye gaze and an arrow in children with and without autism. Journal of Child Psychology and Psychiatry, 45, 445–458.

    Article  PubMed  Google Scholar 

  • Striano, T., Reid, V. M., & Hoehl, S. (2006). Neural mechanisms of joint attention in infancy. European Journal of Neuroscience, 23, 2819–2823.

    Article  PubMed  Google Scholar 

  • Swettenham, J., Condie, S., Campbell, R., Milne, E., & Coleman, M. (2003). Does the perception of moving eyes trigger reflexive visual orienting in autism? Philosophical Transactions of the Royal Society B, 358, 325–334.

    Article  Google Scholar 

  • Tomasello, M., Call, J., & Hare, B. (1998). Five primate species follow the visual gaze of conspecifics. Animal Behavior, 55, 1063–1069.

    Article  Google Scholar 

  • Tomasello, M., Carpenter, M., Call, J., Behne, T., & Moll, H. (2005). Understanding sharing intentions: The origins of cultural cognition. Brain and Behavior Sciences, 28, 675–690.

    Google Scholar 

  • Vivanti, G., McCormick, C., Young, G. S., Abucayan, F., Hatt, N., Nadig, A., et al. (2011). Intact and impaired mechanisms of action understanding in autism. Developmental Psychology, 47, 841–856.

    Article  PubMed  Google Scholar 

  • World Health Organization. (1993). The ICD-10 classification of mental and behavioural disorders. Diagnostic criteria for research. Geneva: WHO.

  • Yirmiya, N., & Charman, T. (2010). The prodrome of autism: Early behavioral and biological signs, regression, peri- and post-natal development and genetics. Journal of Child Psychology and Psychiatry, 51, 432–458.

    Article  PubMed  Google Scholar 

  • Yirmiya, N., Gamliel, I., Pilowsky, T., Feldman, R., Baron-Cohen, S., & Sigman, M. (2006). The development of siblings of children with autism at 4 and 14 months: Social engagement, communication, and cognition. Journal of Child Psychology and Psychiatry, 47, 511–523.

    Article  PubMed  Google Scholar 

  • Yoder, P., Stone, W. L., Walden, T., & Malesa, E. (2009). Predicting social impairment and ASD diagnosis in younger siblings of children with autism spectrum disorder. Journal of Autism and Developmental Disorders, 39, 1381–1391.

    Article  PubMed  Google Scholar 

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Acknowledgments

This work has been supported by, a Bloomsbury Colleges Scholarship to R. Bedford, a Leverhulme Early Career Fellowship to M. Elsabbagh, and the BASIS funding consortium led by Autistica (www.basisnetwork.org) and a UK Medical Research Council Programme Grant (G0701484) to M.H. Johnson. The Centre for Research in Autism and Education is supported by The Clothworkers’ Foundation and Pears Foundation. T. Charman and M. Elsabbagh are supported by the COST Action BM1004. We thank all the families who participated in this study and Liz Pellicano for helpful discussions.

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Correspondence to Rachael Bedford.

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The BASIS Team in alphabetical order: S. Baron-Cohen, P. Bolton, S. Chandler, J. Fernandes, H. Garwood, K. Hudry, L. Tucker, A. Volein.

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Bedford, R., Elsabbagh, M., Gliga, T. et al. Precursors to Social and Communication Difficulties in Infants At-Risk for Autism: Gaze Following and Attentional Engagement. J Autism Dev Disord 42, 2208–2218 (2012). https://doi.org/10.1007/s10803-012-1450-y

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