Skip to main content
SpringerLink
Log in

Positive Affect Processing and Joint Attention in Infants at High Risk for Autism: An Exploratory Study

  • Original Paper
  • Published:
Journal of Autism and Developmental Disorders Aims and scope Submit manuscript

An Erratum to this article was published on 14 August 2014

Abstract

Few behavioral indices of risk for autism spectrum disorders (ASD) are present before 12 months, and potential biomarkers remain largely unexamined. This prospective study of infant siblings of children with ASD (n = 16) and low-risk comparison infants (n = 15) examined group differences in event-related potentials (ERPs) indexing processing of facial positive affect (N290/P400, Nc) at 9 months and their relation to joint attention at 15 months. Group differences were most pronounced for subtle facial expressions, in that the low-risk group exhibited relatively longer processing (P400 latency) and greater attention resource allocation (Nc amplitude). Exploratory analyses found associations between ERP responses and later joint attention, suggesting that attention to positive affect cues may support the development of other social competencies.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Notes

  1. Consistency in the recruitment procedures and inclusion/exclusion criteria as well as in data acquisition procedures was ensured by joint in-person training on all study procedures for the research staff at the three sites. Standardized behavioral assessments at each site were administered by trained clinical psychologists, ensuring strict adherence to the established procedural guidelines. All EEG data were processed and analyzed by the single lab, ensuring consistency in artifact detection procedures.

References

  • American Psychiatric Association. (2000). Diagnostic and statistical manual of mental disorders-IV-text revision. Washington, DC: Author.

    Google Scholar 

  • Berument, S., Rutter, M., Lord, C., Pickles, A., & Bailey, A. (1999). Autism screening questionnaire: Diagnostic validity. The British Journal of Psychiatry, 175, 444–451.

    Article  PubMed  Google Scholar 

  • Boccia, M., & Campos, J. J. (1989). Maternal emotional signals, social referencing, and infants’ reactions to strangers. New Directions for Child Development, 44, 25–49.

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Campos, J., & Stenberg, C. (1981). Perception, appraisal and emotion: The onset of social referencing. In M. E. Lamb & L. R. Sherrod (Eds.), Infant social cognition. Hillsdale, NJ: Erlbaum.

    Google Scholar 

  • Centers for Disease Control and Prevention. (2014). Autism. http://www.cdc.gov/ncbddd/autism/addm.html.

  • 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.

    Article  PubMed Central  PubMed  Google Scholar 

  • Csibra, G., Kushnerenko, E., & Grossmann, T. (2008). Electrophysiological methods in studying infant cognitive development. In C.A. Nelson & M. Luciana (Eds.), Handbook of Developmental Cognitive Neuroscience (2nd ed., pp. 247–262). MIT Press.

  • Dawson, G., Jones, E. J. H., Merkle, K., Venema, K., Lowy, R., Faja, S., et al. (2012). Early behavioral intervention is associated with normalized brain activity in young children with autism. Journal of the American Academy of Child and Adolescent Psychiatry, 51(11), 1150–1159. doi:10.1016/j.jaac.2012.08.018.

    Article  PubMed Central  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Dawson, G., Webb, S. J., Wijsman, E., Schellenberg, G., Estes, A., Munson, J., et al. (2005). Neurocognitive and electrophysiological evidence of altered face processing in parents of children with autism: implications for a model of abnormal development of social brain circuitry in autism. Development and Psychopathology, 17(3), 679–697. doi:10.1017/S0954579405050327.

    Article  PubMed  Google Scholar 

  • de Haan, M., Belsky, J., Reid, V., Volein, A., & Johnson, M. H. (2004). Maternal personality and infants’ neural and visual responsivity to facial expressions of emotion. Journal of Child Psychology and Psychiatry, 45, 1209–1218.

    Article  PubMed  Google Scholar 

  • de Haan, M., Johnson, M. H., & Halit, H. (2003). Development of face-sensitive event-related potentials during infancy: A review. International Journal of Psychophysiology, 51(1), 45–58.

    Article  PubMed  Google Scholar 

  • de Haan, M., & Nelson, C. A. (1997). Recognition of the mother’s face by six-month-old infants: A neurobehavioral study. Child Development, 68(2), 187–210.

    Article  PubMed  Google Scholar 

  • de Haan, M., & Nelson, C. A. (1999). Brain activity differentiates face and object processing in 6-month-old infants. Developmental Psychology, 35(4), 1113–1121.

    Article  PubMed  Google Scholar 

  • Dereu, M., Roeyers, H., & Raymaekers, R. (2012). Exploring individual trajectories of social communicative development in toddlers at risk for autism spectrum disorders. Research in Autism Spectrum Disorders, 6(3), 1038–1052.

    Article  Google Scholar 

  • Eimer, M., & Holmes, A. (2002). An ERP study on the time course of emotional face processing. NeuroReport, 13(4), 427–431.

    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(1), 31–38. doi:10.1016/j.biopsych.2008.09.034.

    Article  PubMed  Google Scholar 

  • Georgiades, S., Szatmari, P., Zwaigenbaum, L., Bryson, S., Brian, J., Roberts, W., Smith, I., et al. (2012). A prospective study of autistic-like traits in unaffected siblings of probands with autism spectrum disorder. Archives of General Psychiatry, E1–E7. doi:10.1001/2013.jamapsychiatry.1.

  • Halit, H., de Haan, M., & Johnson, M. H. (2003). Cortical specialization for face processing: Face-sensitive event-related potential components in 3- and 12-month-old infants. Neuroimage, 19(3), 1180–1193.

    Article  PubMed  Google Scholar 

  • Hornik, R., & Gunnar, M. R. (1988). A descriptive analysis of infant social referencing. Child Development, 59, 626–634.

    Article  PubMed  Google Scholar 

  • Ibanez, 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.

  • Key, A., & Stone, W. (2012a). Processing of novel and familiar faces in infants at average and high risk for autism. Developmental Cognitive Neuroscience, 2, 244–255.

    Article  PubMed  Google Scholar 

  • Key, A., & Stone, W. (2012b). Same but different: Nine-month-old infants at low and high risk for autism look at the same facial features but process them using different brain mechanisms. Autism Research, 5, 253–266.

    Article  PubMed Central  PubMed  Google Scholar 

  • Key, A., Stone, W., & Williams, S. (2009). What do infants see in faces? ERP evidence of different roles of eyes and mouth for face perception in 9-month-old infants. Infant and Child Development, 18, 149–162.

    Article  PubMed Central  PubMed  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(6), 629–638. doi:10.1111/j.1469-7610.2006.01531.x.

    Article  PubMed  Google Scholar 

  • Leppänen, J., Moulson, M., Vogel-Farley, V., & Nelson, C. (2007). An ERP study of emotional face processing in the adult and infant brain. Child Development, 78(1), 232–245.

    Article  PubMed Central  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 communication deficits associated with the spectrum of autism. Journal of Autism and Developmental Disorders, 30, 205–223.

    Article  PubMed  Google Scholar 

  • Luyster, R., Wagner, J., Vogel-Farley, V., Tager-Flusberg, H., & Nelson, C. (2011). Neural correlates of familiar and unfamiliar face processing in infants at risk for autism spectrum disorders. Brain Topography,. doi:10.1007/s10548-011-0176-z.

    PubMed Central  PubMed  Google Scholar 

  • McCleery, J., Akshoomoff, N., Dobkins, K., & Carver, L. (2009). Atypical face versus object processing and hemispheric asymmetries in 10-month-old infants at risk for autism. Biological Psychiatry, 66, 950–957.

    Article  PubMed Central  PubMed  Google Scholar 

  • Messinger, D., Young, G. S., Ozonoff, S., Dobkins, K., Carter, A., Zwaigenbaum, L., et al. (2013). Beyond ASD: A Baby Siblings Research Consortium study of high-risk siblings at three years of age. Journal of the American Academy of Child and Adolescent Psychiatry, 52, 300–308.

  • Mundy, P., Fox, N., & Card, J. (2003). EEG coherence, joint attention and language development in the second year. Developmental Science, 6, 48–54.

    Article  Google Scholar 

  • Mundy, P. C., Henderson, H. A., Inge, A. P., & Coman, D. C. (2007). The modifier model of autism and social development in higher functioning children with autism. Research and Practice for Persons with Severe Disabilities, 32, 124–139.

    Article  PubMed Central  PubMed  Google Scholar 

  • Mundy, P., & Sigman, M. (2006). Joint attention, social competence, and developmental psychopathology. In Mundy, P., & Sigman, M. (Eds.), Developmental psychopathology, Vol 1: Theory and method (2nd ed., pp. 293–332). Hoboken, NJ, US: Wiley.

  • Nelson, C. A., & de Haan, M. (1996). Neural correlates of infants’ visual responsiveness to facial expressions of emotion. Developmental Psychobiology, 29, 577–595.

    Article  PubMed  Google Scholar 

  • Osterling, J., & Dawson, G. (1994). Early recognition of children with autism: A study of first birthday home videotapes. Journal of Autism and Developmental Disorders, 24(3), 247–257.

    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(3), 488–495.

    Google Scholar 

  • Pelphrey, K. A., Shultz, S., Hudac, C. M., & Vander Wyk, B. C. (2011). Constraining heterogeneity: The social brain and its development in autism spectrum disorder. Journal of Child Psychology and Psychiatry and Allied Disciplines, 52(6), 631–644. doi:10.1111/j.1469-7610.2010.02349.x.

    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(1), 133–144.

    Article  PubMed  Google Scholar 

  • Reynolds, G., & Richards, J. (2005). Familiarization, attention, and recognition memory in infancy: An event-related potential and cortical source localization study. Developmental Psychology, 41(4), 598–615.

    Article  PubMed Central  PubMed  Google Scholar 

  • Rosen, W. D., Adamson, L. B., & Bakeman, R. (1992). An experimental investigation of infant social referencing: Mother’s messages and gender differences. Developmental Psychology, 28, 1172–1178.

    Article  Google Scholar 

  • Rozga, A., Hutman, T., Young, G. S., Rogers, S. J., Ozonoff, S., Dapretto, M., et al. (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.

    Article  PubMed Central  PubMed  Google Scholar 

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

    Google Scholar 

  • Scott, L., & Nelson, C. (2006). Featural and configural face processing in adults and infants: A behavioral and electrophysiological investigation. Perception, 35, 1107–1128.

    Article  PubMed  Google Scholar 

  • Sepeta, L., Tsuchiya, N., Davies, M. S., Sigman, M., Bookheimer, S. Y., & Dapretto, M. (2012). Abnormal social reward processing in autism as indexed by pupillary responses to happy faces. Journal of Neurodevelopmental Disorders, 4, 17.

    Article  PubMed Central  PubMed  Google Scholar 

  • Stone, W. L., McMahon, C. R., Yoder, P. J., & Walden, T. A. (2007). Early social communicative and cognitive development of younger sibling of children with autism spectrum disorders. Archive of Pediatrics and Adolescent Medicine, 161, 384–390.

    Article  Google Scholar 

  • Tabachnick, B. G., Fidell, L. S., & Osterlind, S. J. (2001). Using multivariate statistics. Allyn and Bacon.

  • Thomas, D., Grice, J., Najm-Briscoe, R., & Miller, J. (2004). The influence of unequal numbers of trials on comparisons of average event-related potentials. Developmental Neuropsychology, 26, 753–774.

    Article  PubMed  Google Scholar 

  • Tierney, A. L., Gabard-Durnam, L., Vogel-Farley, V., Tager-Flusberg, H., & Nelson, C. A. (2012). Developmental trajectories of resting EEG power: An endophenotype of autism spectrum disorder. PLoS One, 7(6), e39127. doi:10.1371/journal.pone.0039127.

    Article  PubMed Central  PubMed  Google Scholar 

  • Tomasello, M. (1992). The social bases of language acquisition. Social Development, 1, 67–87.

    Article  Google Scholar 

  • Trevarthen, C., & Hubley, P. (1978). Secondary intersubjectivity: confidence, confiding and acts of meaning in the first year. In A. Lock (Ed.), Action, gesture and symbol: The emergence of language. New York and London: Academic Press.

    Google Scholar 

  • Wetherby, A. M., Woods, J., Allen, L., Cleary, J., Dickinson, H., & Lord, C. (2004). Early indicators of autism spectrum disorders in the second year of life. Journal of Autism and Development Disorders, 34(5), 473–493.

    Article  Google Scholar 

  • Wong, N., Beidel, D. C., Sarver, D. E., & Sims, V. (2012). Facial emotion recognition in children with high functioning autism and children with social phobia. Child Psychiatry and Human Development, 43(5), 775–794. doi:10.1007/s10578-012-0296-z.

    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(5), 511–523.

    Article  PubMed  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, 23(2–3), 143–152.

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This research was supported by National Institute of Child Health and Human Development Grant R01 HD057284 to Wendy L. Stone and Daniel S. Messinger. We would like to thank the participants and their families for their support of the study. We are grateful to Amber Vinson, Dorita Jones, Michelle Fong, Kim Ono, Devon Gangi, and Nicole Coman for their help with acquisition and processing of the ERP data.

Author information

Authors and Affiliations

  1. Vanderbilt Kennedy Center for Research on Human Development and Department of Hearing and Speech Sciences, Vanderbilt University, 230 Appleton Place, PMB 74, Nashville, TN, 37203, USA

    Alexandra P. Key

  2. University of Washington Autism Center, Box 357920, Seattle, WA, 98195, USA

    Lisa V. Ibanez

  3. Department of Psychology, University of Waterloo, Waterloo, ON, N2L 3G1, Canada

    Heather A. Henderson

  4. Treatment and Research Institute for Autism Spectrum Disorders (TRIAD), Vanderbilt Kennedy Center, 230 Appleton Place, PMB 74, Nashville, TN, 37203-5721, USA

    Zachary Warren

  5. University of Miami, P.O. Box 249229, Coral Gables, FL, 33101-0721, USA

    Daniel S. Messinger

  6. Center on Human Development and Disability, University of Washington, Box 357920, Seattle, WA, 98195-7920, USA

    Wendy L. Stone

Authors
  1. Alexandra P. Key
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lisa V. Ibanez
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Heather A. Henderson
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zachary Warren
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Daniel S. Messinger
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Wendy L. Stone
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alexandra P. Key.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Key, A.P., Ibanez, L.V., Henderson, H.A. et al. Positive Affect Processing and Joint Attention in Infants at High Risk for Autism: An Exploratory Study. J Autism Dev Disord 45, 4051–4062 (2015). https://doi.org/10.1007/s10803-014-2191-x

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10803-014-2191-x

Keywords

Search

Navigation