Skip to main content
Log in

Infants at Risk for Autism Spectrum Disorder: Frequency, Quality, and Variety of Joint Attention Behaviors

  • Published:
Journal of Abnormal Child Psychology Aims and scope Submit manuscript

Abstract

Initiation of joint attention is a critical developmental function related to further social communicative development in infancy. Joint attention appears to be impaired very early in life for children with autism spectrum disorder (ASD), well before a formal diagnosis is established. To observe the early development of joint attention, we prospectively followed infant siblings at high risk for ASD (HR) and low-risk (LR) infants. Initiations of joint attention behaviors were coded with respect to frequency, quality, and variety from videos taken during the administration of the Autism Observation Schedule for Infants. Participants were further stratified based on the presence of ASD (n = 17) or language delay (n = 19) at 3 years of age. Our results revealed that initiations of joint attention are impaired from 12 months of age in both children with ASD and those with language delay, especially for use of gestures (i.e., showing and pointing). At 18 months, fewer initiations of joint attention in all three dimensions distinguished infants with ASD, compared to infants with language delay and HR and LR infants without a diagnosis. Beyond the definition of initiation of joint attention as an early sign for ASD, clinical implications of these results concern the importance of intervening on frequency, quality, and variety of joint attention as early as possible in infants at heightened risk for ASD.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • American Psychiatric Association. (2000). Diagnostic and statistical manual of mental disorders (4th ed text rev; DSM-IV-TR). Washington, DC: Author.

    Google Scholar 

  • American Psychiatric Association. (2013). Cautionary statement for forensic use of DSM-5. In Diagnostic and statistical manual of mental disorders (5th ed.). doi:https://doi.org/10.1176/appi.books.9780890425596.744053

  • Bakeman, R., & Adamson, L. B. (1984). Coordinating attention to people and objects in mother-infant and peer-infant interaction. Child Development, 55(4), 1278–1289. https://doi.org/10.2307/1129997.

    Article  PubMed  Google Scholar 

  • Baron-Cohen, S., Cox, A., Baird, G., & Swettenham, J. (1996). Psychological markers in the detection of autism in infancy. The British Journal of Psychiatry, 168, 158–163.

    Article  Google Scholar 

  • Begus, K., & Southgate, V. (2012). Infant pointing serves an interrogative function. Developmental Science, 15(5), 611–617. https://doi.org/10.1111/j.1467-7687.2012.01160.x.

    Article  PubMed  Google Scholar 

  • Benjamini, Y., & Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society, 57, 289–300.

    Google Scholar 

  • Bhat, A. N., Galloway, J. C., & Landa, R. J. (2010). Social and non-social visual attention patterns and associative learning in infants at risk for autism. Journal of Child Psychology and Psychiatry, 51(9), 989–997.

    Article  Google Scholar 

  • Bradshaw, J., Steiner, A. M., Gengoux, G., & Koegel, L. K. (2015). Feasibility and effectiveness of very early intervention for infants at-risk for autism spectrum disorder: A systematic review. Journal of Autism and Developmental Disorders, 45(3), 778–794. https://doi.org/10.1007/s10803-014-2235-2.

    Article  PubMed  Google Scholar 

  • Bryson, S. E., Zwaigenbaum, L., McDermott, C., Rombough, V., & Brian, J. (2008). The autism observation scale for infants: Scale development and reliability data. Journal of Autism and Developmental Disorders, 38(4), 731–738. https://doi.org/10.1007/s10803-007-0440-y.

    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), 1–143. https://doi.org/10.2307/1166214.

    Article  Google Scholar 

  • Carter, A. S., Messinger, D. S., Stone, W. L., Celimli, S., Nahmias, A. S., & Yoder, P. (2011). A randomized controlled trial of Hanen’s “more than words” in toddlers with early autism symptoms. Journal of Child Psychology and Psychiatry, 52(7), 741–752. https://doi.org/10.1111/j.1469-7610.2011.02395.x.

    Article  PubMed  Google Scholar 

  • Cassel, T. D., Messinger, D. S., Ibañez, 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(1), 122–132. https://doi.org/10.1007/s10803-006-0337-1.

    Article  PubMed  Google Scholar 

  • Centers for Disease Control and Prevention. (2014). Prevalence of autism spectrum disorders among children aged 8 years- autism and developmental disabilities monitoring network, eleven sites, United States, 2010. Morbidity and Mortality Weekly Report, 63(2), 1–24.

    Google Scholar 

  • Charman, T. (2003). Why is joint attention a pivotal skill in autism? Philosophical Transactions of the Royal Society of London. Biological Sciences, 358(1430), 315–324. https://doi.org/10.1098/rstb.2002.1199.

    Article  PubMed  Google Scholar 

  • Charman, T., Swettenham, J., & Baron-Cohen, S. (1997). Infants with autism: An investigation of empathy, pretend play, joint attention, and imitation. Developmental Psychology, 33(5), 781–789.

    Article  Google Scholar 

  • Chawarska, K., Macari, S., & Shic, F. (2013). Decreased spontaneous attention to social scenes in 6-month-old infants later diagnosed with autism spectrum disorders. Biological Psychiatry, 74(3), 195–203. https://doi.org/10.1016/j.biopsych.2012.11.022.

    Article  PubMed  PubMed Central  Google Scholar 

  • Chevallier, C., Kohls, G., Troiani, V., Brodkin, E. S., & Schultz, R. T. (2012). The social motivation theory of autism. Trends in Cognitive Sciences, 16(4), 231–239. https://doi.org/10.1016/j.tics.2012.02.007.

    Article  PubMed  PubMed Central  Google Scholar 

  • Cohen, J. (1988). Statistical power analyses for the behavioral sciences (2nd ed.). Hillsdale, NJ: Lawrence Erlbaum Associates.

    Google Scholar 

  • Daniels, A. M., & Mandell, D. S. (2014). Explaining differences in age at autism spectrum disorder diagnosis: A critical review. Autism, 18(5), 583–597. https://doi.org/10.1177/1362361313480277.

    Article  PubMed  Google Scholar 

  • Dawson, G., Toth, K., Abbott, R., Osterling, J., Munson, J., Estes, A., & Liaw, J. (2004). Early social attention impairments in autism: Social orienting, joint attention, and attention to distress. Developmental Psycholgy, 40, 271–283.

    Article  Google Scholar 

  • Drew, A., Baird, G., Baron-Cohen, S., Cox, A., Slonims, V., Wheelwright, S., Swettenham, J., Berry, B., & Charman, T. (2002). A pilot randomised control trial of a parent training intervention for pre-school children with autism. European Child & Adolescent Psychiatry, 11(6), 266–272. https://doi.org/10.1007/s00787-002-0299-6.

    Article  Google Scholar 

  • Franchini, M., Armstrong, V., Schaer, M. & Smith, I. (2018). Spontaneous joint attention and related visual attention processes in infants with autism Spectrum disorder: Literature review. Child Neuropsychology, e1-e31.

  • Gangi, D. N., Ibañez, L. V., & Messinger, D. S. (2014). Joint attention initiation with and without positive affect: Risk group differences and associations with ASD symptoms. Journal of Autism and Developmental Disorders, 44(6), 1414–1424. https://doi.org/10.1007/s10803-013-2002-9.

    Article  PubMed  PubMed Central  Google Scholar 

  • Gillespie-Lynch, K. (2013). Response to and initiation of joint attention: overlapping but distinct roots of development in autism? OA Autism, 1(2). doi: https://doi.org/10.13172/2052-7810-1-2-596

  • Goldberg, W. A., Jarvis, K. L., Osann, K., Laulhere, T. M., Straub, C., Thomas, E., Filipek, P., & Spence, M. A. (2005). Brief report: Early social communication behaviors in the younger siblings of children with autism. Journal of Autism and Developmental Disorders, 35(5), 657–664. https://doi.org/10.1007/s10803-005-0009-6.

    Article  PubMed  Google Scholar 

  • Gotham, K., Pickles, A., & Lord, C. (2009). Standardizing ADOS scores for a measure of severity in autism spectrum disorders. Journal of Autism and Developmental Disorders, 39(5), 693–705.

    Article  Google Scholar 

  • Ibañez, L. V., Grantz, C. J., & Messinger, D. S. (2013). The development of referential communication and autism symptomatology in high-risk infants. Infancy, 18(5), 687–707. https://doi.org/10.1111/j.1532-7078.2012.00142.x.

    Article  Google Scholar 

  • Jones, E. J. H., Gliga, T., Bedford, R., Charman, T., & Johnson, M. H. (2014). Developmental pathways to autism: A review of prospective studies of infants at risk. Neuroscience & Biobehavioral Reviews, 39, 1–33. https://doi.org/10.1016/j.neubiorev.2013.12.001.

    Article  Google Scholar 

  • Kasari, C., Gulsrud, A., Freeman, S., Paparella, T., & Hellemann, G. (2012). Longitudinal follow-up of children with autism receiving targeted interventions on joint attention and play. Journal of the American Academy of Child and Adolescent Psychiatry, 51(5), 487–495. https://doi.org/10.1016/j.jaac.2012.02.019.

    Article  PubMed  PubMed Central  Google Scholar 

  • Landa, R., & Garrett-Mayer, E. (2006). Development in infants with autism spectrum disorders: A prospective study. Journal of Child Psychology and Psychiatry, 47, 629–638.

    Article  Google Scholar 

  • Landa, R. J., Gross, A. L., Stuart, E. A., & Faherty, A. (2013). Developmental trajectories in children with and without autism spectrum disorders: The first 3 years. Child Development, 84(2), 429–442. https://doi.org/10.1111/j.1467-8624.2012.01870.x.

    Article  PubMed  Google Scholar 

  • Leezenbaum, N. B., Campbell, S. B., Butler, D., & Iverson, J. M. (2013). Maternal verbal responses to communication of infants at low and heightened risk of autism. Autism, 18(6), 694–703. https://doi.org/10.1177/1362361313491327.

    Article  PubMed  PubMed Central  Google Scholar 

  • Lord, C., Risi, S., Lambrecht, L., Cook, E. H., 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 and Developmental Disorders, 30, 205–223.

    Article  Google Scholar 

  • Lord C., Rutter M., DiLavore P. C., Risi S., Gotham K. & Bishop S.L. (2012). Autism diagnostic observation schedule, (2nd ed, ADOS-2). Los Angeles, California: Western Psychological Services.

  • Macari, S. L., Campbell, D., Gengoux, G. W., Saulnier, C. A., Klin, A. J., & Chawarska, K. (2012). Predicting developmental status from 12 to 24 months in infants at risk for autism spectrum disorder: A preliminary report. Journal of Autism and Developmental Disorders, 42(12), 2636–2647. https://doi.org/10.1007/s10803-012-1521-0.

    Article  PubMed  PubMed Central  Google Scholar 

  • McHugh, M. L. (2012). Interrater reliability: The kappa statistic. Biochemia medica, 22(3), 276–282.

    Article  Google Scholar 

  • Merin, N., Young, G. S., Ozonoff, S., & Rogers, S. J. (2006). Visual fixation patterns during reciprocal social interaction distinguish a subgroup of 6-month-old infants at-risk for autism from comparison infants. Journal of Autism and Developmental Disorders, 37(1), 108–121. https://doi.org/10.1007/s10803-006-0342-4.

    Article  PubMed  Google Scholar 

  • Morales, M., Mundy, P., Delgado, C. E. F., Yale, M., Messinger, D., Neal, R., & Schwartz, H. K. (2000). Responding to joint attention across the 6- through 24-month age period and early language acquisition. Journal of Applied Developmental Psychology, 21(3), 283–298. https://doi.org/10.1016/S0193-3973(99)00040-4.

    Article  Google Scholar 

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

    Google Scholar 

  • Mundy, P. (2016). Autism and joint attention: Development, neuroscience, and clinical fundamentals. New York: Guilford Press.

    Google Scholar 

  • Mundy, P. (2017). A review of joint attention and social-cognitive brain systems in typical development and autism spectrum disorder. The European Journal of Neuroscience, 27(4), 409–420. https://doi.org/10.1111/ejn.13720.

    Article  Google Scholar 

  • Mundy, P., & Newell, L. (2007). Attention, joint attention, and social cognition. Current Directions in Psychological Science, 16(5), 269–274. https://doi.org/10.1111/j.1467-8721.2007.00518.x.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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(5), 657–669. https://doi.org/10.1111/j.1469-7610.1986.tb00190.x.

    Article  PubMed  Google Scholar 

  • Mundy, P., Sigman, M., & Kasari, C. (1990). A longitudinal study of joint attention and language development in autistic children. Journal of Autism and Developmental Disorders, 20(1), 115–128.

    Article  Google Scholar 

  • Mundy, P., Delgado, C., Block, J., & Venezia, M. (2003). Early social communication scales (ESCS). Coral Gables.

    Google Scholar 

  • Mundy, P., Block, J., Delgado, C., Pomares, Y., Van Hecke, A. V., & Parlade, M. V. (2007). Individual differences and the development of joint attention in infancy. Child Development, 78(3), 938–954. https://doi.org/10.1111/j.1467-8624.2007.01042.x.

    Article  PubMed  PubMed Central  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(1), 2–21. https://doi.org/10.1002/aur.61.

    Article  PubMed  PubMed Central  Google Scholar 

  • Noldus Observer XT (2013). http://www.noldus.com/human-behavior-research/products/the-observer-xt.

  • Ozonoff, S., Iosif, A.-M., Baguio, F., Cook, I. C., Hill, M. M., Hutman, T., et al. (2010). A prospective study of the emergence of early behavioral signs of autism. Journal of the American Academy of Child and Adolescent Psychiatry, 49(3), 256–66.e1–2.

  • Ozonoff, S., Young, G. S., Carter, A., Messinger, D., Yirmiya, N., Zwaigenbaum, L., Bryson, S., Carver, L. J., Constantino, J. N., Dobkins, K., Hutman, T., Iverson, J. M., Landa, R., Rogers, S. J., Sigman, M., & Stone, W. L. (2011). Recurrence risk for autism spectrum disorders: A baby siblings research consortium study. Pediatrics, 128(3), e488–e495. https://doi.org/10.1542/peds.2010-2825.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ozonoff, S., Young, G. S., Belding, A., Hill, M., Hill, A., Hutman, T., et al. (2014). The broader autism phenotype in infancy: When does it emerge? Journal of the American Academy of Child and Adolescent Psychiatry, 53(4), 398–407.e2. https://doi.org/10.1016/j.jaac.2013.12.020.

  • Parlade, M. V., & Iverson, J. M. (2015). The development of coordinated communication in infants at heightened risk for autism spectrum disorder. Journal of Autism and Developmental Disorders, 45(7), 2218–2234. https://doi.org/10.1007/s10803-015-2391-z.

    Article  PubMed  PubMed Central  Google Scholar 

  • Rogers, S. J., Estes, A., Lord, C., Vismara, L., Winter, J., Fitzpatrick, A., Guo, M., & Dawson, G. (2012). Effects of a brief early start Denver model (ESDM)–based parent intervention on toddlers at risk for autism spectrum disorders: A randomized controlled trial. Journal of the American Academy of Child and Adolescent Psychiatry, 51(10), 1052–1065. https://doi.org/10.1016/j.jaac.2012.08.003.

    Article  PubMed  PubMed Central  Google Scholar 

  • Rozga, A., Hutman, T., Young, G. S., Rogers, S. J., Ozonoff, S., Dapretto, M., & Sigman, M. (2011). Behavioral profiles of affected and unaffected siblings of children with autism: Contribution of measures of mother-infant interaction and nonverbal communication. Journal of Autism and Developmental Disorders, 41(3), 287–301. https://doi.org/10.1007/s10803-010-1051-6.

    Article  PubMed  Google Scholar 

  • Rutter, M., Le Couteur, A., & Lord, C. (2003). ADI-R: Autism diagnostic interview revised manual. Los Angeles, CA: Western Psychological Services.

    Google Scholar 

  • Sacrey, L.-A. R., Zwaigenbaum, L., Bryson, S., Brian, J., Smith, I. M., Roberts, W., Szatmari, P., Roncadin, C., Garon, N., Novak, C., Vaillancourt, T., McCormick, T., MacKinnon, B., Jilderda, S., & Armstrong, V. (2015). Can parents' concerns predict autism spectrum disorder? A prospective study of high-risk siblings from 6 to 36 months of age. Journal of the American Academy of Child and Adolescent Psychiatry, 54(6), 470–478. https://doi.org/10.1016/j.jaac.2015.03.014.

    Article  PubMed  Google Scholar 

  • Schertz, H. H., & Odom, S. L. (2007). Promoting joint attention in toddlers with autism: A parent-mediated developmental model. Journal of Autism and Developmental Disorders, 37(8), 1562–1575. https://doi.org/10.1007/s10803-006-0290-z.

    Article  PubMed  Google Scholar 

  • Wetherby, A. M., & Woods, J. J. (2016). Early social interaction project for children with autism spectrum disorders beginning in the second year of life: A preliminary study. Topics in Early Childhood Special Education, 26(2), 67–82. https://doi.org/10.1177/02711214060260020201.

    Article  Google Scholar 

  • Winder, B. M., Wozniak, R. H., Parlade, M. V., & Iverson, J. M. (2013). Spontaneous initiation of communication in infants at low and heightened risk for autism spectrum disorders. Developmental Psychology, 49(10), 1931–1942. https://doi.org/10.1037/a0031061.

    Article  PubMed  Google Scholar 

  • Young, G. S., Merin, N., Rogers, S. J., & Ozonoff, S. (2009). Gaze behavior and affect at 6 months: Predicting clinical outcomes and language development in typically developing infants and infants at risk for autism. Developmental Science, 12(5), 798–814. https://doi.org/10.1111/j.1467-7687.2009.00833.x.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zwaigenbaum, L., Bryson, S., Rogers, T., Roberts, W., Brian, J., & Szatmari, P. (2005). Behavioral manifestations of autism in the first year of life. International Journal of Developmental Neuroscience : the Official Journal of the International Society for Developmental Neuroscience, 23(2–3), 143–152. https://doi.org/10.1016/j.ijdevneu.2004.05.001.

    Article  Google Scholar 

  • Zwaigenbaum, L., Bryson, S. E., Szatmari, P., Brian, J., Smith, I. M., Roberts, W., Vaillancourt, T., & Roncadin, C. (2012). Sex differences in children with autism spectrum disorder identified within a high-risk infant cohort. Journal of Autism and Developmental Disorders, 42(12), 2585–2596. https://doi.org/10.1007/s10803-012-1515-y.

    Article  PubMed  Google Scholar 

  • Zwaigenbaum, L., Bryson, S., & Garon, N. (2013). Early identification of autism spectrum disorders. Behavioural Brain Research, 251, 133–146. https://doi.org/10.1016/j.bbr.2013.04.004.

    Article  PubMed  Google Scholar 

  • Zwaigenbaum, L., Bauman, M. L., Fein, D., Pierce, K., Buie, T., Davis, P. A., et al. (2015). Early screening of autism spectrum disorder: Recommendations for practice and research. Pediatrics, 136 Suppl 1(supplement), S41–59. https://doi.org/10.1542/peds.2014-3667D.

Download references

Acknowledgments

The authors would like to thank all the families who kindly volunteered to participate as well as everyone involved in data collection. This work was supported by the Canadian Institutes of Health Research [grant number MOP102655], and Autism Speaks Canada [grant number ASCanada-2010-01]. MF was supported by an individual grant from the Swiss National Science Foundation (grant number P2GEP1_171686). SEB and IMS were supported by the Joan and Jack Craig Chair in Autism Research. The authors declare no conflicts of interest. LZ was supported by the Stollery Childrens Hospital Foundation Chair in Autism.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Martina Franchini.

Ethics declarations

Conflict of Interest

The authors declare no conflicts of interest.

Ethical Approval

Research Ethics Boards approved the study protocol at each site.

Informed Consent

Participants’ parents gave their informed consent.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Franchini, M., Hamodat, T., Armstrong, V.L. et al. Infants at Risk for Autism Spectrum Disorder: Frequency, Quality, and Variety of Joint Attention Behaviors. J Abnorm Child Psychol 47, 907–920 (2019). https://doi.org/10.1007/s10802-018-0471-1

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10802-018-0471-1

Keywords

Navigation