Advertisement

Journal of Abnormal Child Psychology

, Volume 47, Issue 5, pp 907–920 | Cite as

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

  • Martina FranchiniEmail author
  • T. Hamodat
  • V. L. Armstrong
  • L.-A. R. Sacrey
  • J. Brian
  • S. E. Bryson
  • N. Garon
  • W. Roberts
  • L. Zwaigenbaum
  • I. M. Smith
Article

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.

Keywords

Autism spectrum disorder High-risk infants Joint attention Prospective Longitudinal 

Notes

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.

Compliance with Ethical Standards

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.

References

  1. American Psychiatric Association. (2000). Diagnostic and statistical manual of mental disorders (4th ed text rev; DSM-IV-TR). Washington, DC: Author.Google Scholar
  2. 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
  3. 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.Google Scholar
  4. 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.Google Scholar
  5. 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.Google Scholar
  6. 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
  7. 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.Google Scholar
  8. 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.Google Scholar
  9. 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.Google Scholar
  10. 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.Google Scholar
  11. 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.Google Scholar
  12. 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.Google Scholar
  13. 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
  14. 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.Google Scholar
  15. 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.Google Scholar
  16. 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.Google Scholar
  17. 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.Google Scholar
  18. Cohen, J. (1988). Statistical power analyses for the behavioral sciences (2nd ed.). Hillsdale, NJ: Lawrence Erlbaum Associates.Google Scholar
  19. 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.Google Scholar
  20. 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.Google Scholar
  21. 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.Google Scholar
  22. 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.Google Scholar
  23. 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.Google Scholar
  24. 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
  25. 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.Google Scholar
  26. 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.Google Scholar
  27. 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.Google Scholar
  28. 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.Google Scholar
  29. 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.Google Scholar
  30. 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.Google Scholar
  31. 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.Google Scholar
  32. 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.Google Scholar
  33. 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.Google Scholar
  34. 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.Google Scholar
  35. 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.Google Scholar
  36. McHugh, M. L. (2012). Interrater reliability: The kappa statistic. Biochemia medica, 22(3), 276–282.Google Scholar
  37. 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.Google Scholar
  38. 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.Google Scholar
  39. Mullen, E. M. (1995). Mullen scales of early learning. Circle Pines, MN: American Guidance.Google Scholar
  40. Mundy, P. (2016). Autism and joint attention: Development, neuroscience, and clinical fundamentals. New York: Guilford Press.Google Scholar
  41. 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.Google Scholar
  42. 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.Google Scholar
  43. 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.Google Scholar
  44. 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.Google Scholar
  45. Mundy, P., Delgado, C., Block, J., & Venezia, M. (2003). Early social communication scales (ESCS). Coral Gables.Google Scholar
  46. 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.Google Scholar
  47. 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.Google Scholar
  48. 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.Google Scholar
  49. 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.Google Scholar
  50. 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.
  51. 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.Google Scholar
  52. 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.Google Scholar
  53. 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.Google Scholar
  54. Rutter, M., Le Couteur, A., & Lord, C. (2003). ADI-R: Autism diagnostic interview revised manual. Los Angeles, CA: Western Psychological Services.Google Scholar
  55. 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.Google Scholar
  56. 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.Google Scholar
  57. 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.Google Scholar
  58. 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.Google Scholar
  59. 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.Google Scholar
  60. 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.Google Scholar
  61. 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.Google Scholar
  62. 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.Google Scholar
  63. 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.

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Martina Franchini
    • 1
    • 2
    Email author
  • T. Hamodat
    • 3
  • V. L. Armstrong
    • 1
  • L.-A. R. Sacrey
    • 4
  • J. Brian
    • 5
    • 6
  • S. E. Bryson
    • 1
    • 2
  • N. Garon
    • 7
  • W. Roberts
    • 8
  • L. Zwaigenbaum
    • 4
  • I. M. Smith
    • 1
    • 2
    • 3
  1. 1.Autism Research Centre, IWK Health CentreHalifaxCanada
  2. 2.Department of PediatricsDalhousie UniversityHalifaxCanada
  3. 3.Department of Psychology & NeuroscienceDalhousie UniversityHalifaxCanada
  4. 4.Department of PediatricsUniversity of AlbertaEdmontonCanada
  5. 5.Bloorview Research InstituteTorontoCanada
  6. 6.Department of PediatricsUniversity of TorontoTorontoCanada
  7. 7.Department of PsychologyMount Allison UniversitySackvilleCanada
  8. 8.Integrated Services for Autism and Neurodevelopmental DisordersTorontoCanada

Personalised recommendations