Skip to main content
SpringerLink
Log in

The Relationship Between Early Neural Responses to Emotional Faces at Age 3 and Later Autism and Anxiety Symptoms in Adolescents with Autism

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

Abstract

Both autism spectrum (ASD) and anxiety disorders are associated with atypical neural and attentional responses to emotional faces, differing in affective face processing from typically developing peers. Within a longitudinal study of children with ASD (23 male, 3 female), we hypothesized that early ERPs to emotional faces would predict concurrent and later ASD and anxiety symptoms. Greater response amplitude to fearful faces corresponded to greater social communication difficulties at age 3, and less improvement by age 14. Faster ERPs to neutral faces predicted greater ASD symptom improvement over time, lower ASD severity in adolescence, and lower anxiety in adolescence. Early individual differences in processing of emotional stimuli likely reflect a unique predictive contribution from social brain circuitry early in life.

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

Similar content being viewed by others

References

  • Amaral, D. G., Behniea, H., & Kelly, J. L. (2003). Topographic organization of projections from the amygdala to the visual cortex in the macaque monkey. Neuroscience, 188, 1099–1120.

    Article  Google Scholar 

  • Ashwin, C., Baron-Cohen, S., Wheelwright, S., O’Riordan, M., & Bullmore, E. T. (2007). Differential activation of the amygdala and the ‘social brain’ during fearful face-processing in Asperger Syndrome. Neuropsychologia, 45(1), 2–14.

    Article  PubMed  Google Scholar 

  • Bar-Haim, Y., Lamy, D., & Glickman, S. (2005). Attentional bias in anxiety: A behavioral and ERP study. Brain and Cognition, 59, 11–22.

    Article  PubMed  Google Scholar 

  • Baron-Cohen, S. (2005). Mindblindness: An essay on autism and theory of mind. Cambridge, MA: MIT Press.

    Google Scholar 

  • Baron-Cohen, S., Baldwin, D. A., & Crowson, M. (1997). Do children with autism use the speaker’s direction of gaze strategy to crack the code of language? Child Development, 68(1), 48–57.

    Article  PubMed  Google Scholar 

  • Beauchaine, T. P., & Webb, S. J. (in press). Developmental processes and psychophysiology. In J. T. Cacioppo, L. G. Tassinary, & G. G. Berntson (Eds.), Handbook of psychophysiology (4th ed.). Newyork: Cambridge University Press.

  • Bentin, S., Allison, T., Puce, A., Perez, E., & McCarthy, G. (1996). Electrophysiological studies of face perception in humans. Journal of Cognitive Neuroscience, 8(6), 551–565. doi:10.1162/jocn.1996.8.6.551.

    Article  PubMed  PubMed Central  Google Scholar 

  • Blakeley-Smith, A., Reaven, J., Ridge, K., & Hepburn, S. (2012). Parent-child agreement of anxiety symptoms in youth with autism spectrum disorders. Research in Autism Spectrum Disorders, 6, 707–716.

    Article  Google Scholar 

  • Bryk, A. S., & Raudenbush, S. W. (1992). Hierarchical linear models. Newbury Park, CA: Sage.

    Google Scholar 

  • Campbell, D. J., Shic, F., Macari, S., & Chawarska, K. (2014). Gaze response to dyadic bids at 2 years related to outcomes at 3 years in autism spectrum disorders: A subtyping analysis. Journal of Autism and Developmental Disorders, 44, 431–442.

    Article  PubMed  PubMed Central  Google Scholar 

  • Dawson, G., & Bernier, R. A. (2007). Social brain circuitry in autism. In D. Coch, G. Dawson, & K. Fischer (Eds.), Human behavior and the developing brain (2nd ed.). New York, NY: Guilford Press.

    Google Scholar 

  • Dawson, G., Webb, S. J., Carver, L., Panagiotides, H., & McPartland, J. (2004). Young children with autism show atypical brain responses to fearful versus neutral facial expressions of emotion. Developmental Science, 7(3), 340–359.

    Article  PubMed  Google Scholar 

  • Dawson, G., Webb, S. J., & McPartland, J. (2005). Understanding the nature of face processing impairment in autism: Insights from behavioral and electrophysiological studies. Developmental Neuropsychology, 27(3), 403–424.

    Article  PubMed  Google Scholar 

  • Deely, Q., Daly, E. M., Surguladze, S., Page, L., Toal, F., Robertson, D., et al. (2007). An event related functional magnetic resonance imaging study of facial emotion processing Asperger Syndrome. Biological Psychiatry, 62, 207–217.

    Article  Google Scholar 

  • de Klerk, C. C. J. M., Gliga, T., Charman, T., Johnson, M. H., & The BASIS Team. (2014). Face engagement during infancy predicts later face recognition ability in younger siblings of children with autism. Developmental Science, 17(4), 596–611.

    Google Scholar 

  • Ekman, P., & Friesen, W. V. (1976). Pictures of facial affect. Palo Alto, CA: Consulting Psychologists Press.

    Google Scholar 

  • Eldar, S., Yankelevitch, R., Lamy, D., & Bar-Haim, Y. (2010). Enhanced neural reactivity and selective attention to threat in anxiety. Biological Psychology, 85, 252–257.

    Article  PubMed  Google Scholar 

  • Elsabbagh, M., Mercure, E., Hudry, K., Chandler, S., Pasco, G., Charman, T., et al. (2012). Infant neural sensitivity to dynamic eye gaze is associated with later emerging autism. Current Biology, 22(4), 338–342.

    Article  PubMed  PubMed Central  Google Scholar 

  • Fox, E., Russo, R., Bowles, R., & Dutton, K. (2007). Do threatening stimuli draw or hold visual attention in subclinical anxiety? Journal of Experimental Psychology: General, 130(4), 681–700.

    Article  Google Scholar 

  • Gauthier, I., Curran, T., Curby, K. M., & Collins, D. (2003). Perceptual interference supports a non-modular account of face processing. Nature Neuroscience, 6(4), 428–432.

    Article  PubMed  Google Scholar 

  • Golarai, G., Grill-Spector, K., & Reiss, A. L. (2006). Autism and the development of face processing. Clinical Neuroscience Research, 6, 145–160.

    Article  PubMed  PubMed Central  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  PubMed  Google Scholar 

  • Gotham, K., Risi, S., Pickles, A., & Lord, C. (2007). The Autism Diagnostic Observation Schedule: Revised algorithms for improved diagnostic validity. Journal of Autism and Developmental Disorders, 37(4), 613–627.

    Article  PubMed  Google Scholar 

  • Hankin, B. L., Gibb, B. E., Abela, J. R. Z., & Flory, K. (2010). Selective attention to affective stimuli and clinical depression among youth: Role of anxiety and specificity of emotion. Journal of Abnormal Psychology, 119(3), 491–501.

    Article  PubMed  PubMed Central  Google Scholar 

  • Hileman, C. M., Henderson, H., Mundy, P., Newell, L., & Jaime, M. (2011). Developmental and individual differences on the P1 and N170 ERP components in children with and without autism. Developmental Neuropsychology, 36, 214–236.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ingersoll, B., & Wainer, A. (2013). Initial efficacy of Project ImPACT: A parent-mediated social communication intervention for young children with ASD. Journal of Autism and Developmental Disorders, 43, 2943–2952.

    Article  PubMed  Google Scholar 

  • Johnson, M. H., Senju, A., & Tomalski, P. (2015). The two-process theory of face processing: modifications based on two decades of data from infants and adults. Neuroscience and Biobehavioral Reviews, 50, 169–179. doi:10.1016/j.neubiorev.2014.10.009.

    Article  PubMed  Google Scholar 

  • Jones, W., & Klin, A. (2013). Attention to eyes is present but in decline in 2–6-month-old infants later diagnosed with autism. Nature, 504, 427–431.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kanwisher, N. (2000). Domain specificity in face perception. Nature Neuroscience, 3(8), 759–763.

    Article  PubMed  Google Scholar 

  • Lord, C., Rutter, M., DiLavore, P. C., & Risi, S. (2003). Autism Diagnostic Observation Schedule manual. Los Angeles, CA: Western Psychological Services.

    Google Scholar 

  • Lord, C., Rutter, M. L., Goode, S., & Heemsbergen, J. (1989). Autism Diagnostic Observation Schedule: A standardized observation of communicative and social behavior. Journal of Autism and Developmental Disorders, 19, 185–212.

    Article  PubMed  Google Scholar 

  • Lord, C., Rutter, M., & Le Couteur, A. (1994). 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 

  • Lozier, L. M., Vanmeter, J. W., & Marsh, A. A. (2014). Impairments in facial affect recognition associated with autism spectrum disorders: A meta-analysis. Developmental Psychopathology. doi:10.1017/s0954579414000479.

    Google Scholar 

  • May, T., Cornish, K., & Rinehart, N. J. (2015). Parent–child agreement using the Spence Children’s Anxiety Scale and thermometer in children with autism spectrum disorder. Autism Research and Treatment, Article ID 315495.

  • Mogg, K., Garner, M., & Bradley, B. P. (2007). Anxiety and orienting of gaze to angry and fearful faces. Biological Psychology, 76, 163–169.

    Article  PubMed  PubMed Central  Google Scholar 

  • Morton, J., & Johnson, M. H. (1991). CONSPEC and CONLERN: A two-process theory of infant face recognition. Psychological Review, 98(2), 164–181.

    Article  PubMed  Google Scholar 

  • Mullen, E. M. (1997). Mullen scales of early learning. Los Angeles, CA: Western Psychological Services.

    Google Scholar 

  • Neuhaus, E., Beauchaine, T. P., & Bernier, R. (2010). Neurobiological correlates of social functioning in autism. Clinical Psychology Review, 30(6), 733–748.

    Article  PubMed  Google Scholar 

  • Neuhaus, E., Bernier, R., & Beauchaine, T. P. (2014). Social skills, internalizing and externalizing symptoms, and respiratory sinus arrhythmia in autism. Journal of Autism and Developmental Disorders, 44, 730–737.

    Article  PubMed  Google Scholar 

  • O’Toole, L. J., DeCicco, J. M., Berthod, S., & Dennis, T. A. (2013). The N170 to angry faces predicts anxiety in typically developing children over a two-year period. Developmental Neuropsychology, 38(5), 352–363.

    Article  PubMed  PubMed Central  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., Iosif, A. M., Baquio, F., Cook, I. C., Hill, M. M., Rogers, S. J., 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), 256–266.

    PubMed  PubMed Central  Google Scholar 

  • Ozsivadjian, A., Hibberd, C., & Hollocks, M. J. (2014). The use of self-report measures in young people with autism spectrum disorder to access symptoms of anxiety, depression, and negative thoughts. Journal of Autism and Developmental Disorders, 44, 969–974.

    Article  PubMed  Google Scholar 

  • Phelps, E. A., & LeDoux, J. E. (2005). Contributions of the amygdala to emotion processing: From animal models to human behavior. Neuron, 48, 175–187.

    Article  PubMed  Google Scholar 

  • Reynolds, C. R., & Richmond, B. O. (1997). What I think and feel: A revised measure of children’s manifest anxiety. Journal of Abnormal Child Psychology, 25, 15–20.

    Article  PubMed  Google Scholar 

  • Rothbart, M. K., Sheese, B. E., Rueda, M. R., & Posner, M. I. (2011). Developing mechanisms of self-regulation in early life. Emotion Review, 3, 207–213.

    Article  PubMed  PubMed Central  Google Scholar 

  • Siller, M., & Sigman, M. (2008). Modeling longitudinal change in the language abilities of children with autism: Parent behaviors and child characteristics as predictors of change. Developmental Psychology, 44, 1691–1704.

    Article  PubMed  Google Scholar 

  • Simonoff, E., Pickles, A., Charman, T., Chandler, S., Loucas, T., & Baird, G. (2008). Psychiatric disorders in children with autism spectrum disorders: Prevalence, comorbidity, and associated factors in a population-derived sample. Journal of the American Academy of Child and Adolescent Psychiatry, 47(8), 921–929.

    Article  PubMed  Google Scholar 

  • Taylor, M. J., Batty, M., & Itier, R. J. (2001). The faces of development: A review of early face processing over childhood. Journal of Cognitive Neuroscience, 16, 1426–1442.

    Article  Google Scholar 

  • Thomas, K. M., Drevets, W. C., Dahl, R. E., Ryan, N. D., Birmaher, B., Eccard, C. H., et al. (2001). Amygdala response to fearful faces in anxious and depressed children. Archives of General Psychiatry, 58, 1057–1063.

    Article  PubMed  Google Scholar 

  • Tucker, D. (1993). Spatial sampling of head electrical fields, the geodesic sensor net. Electroencephalography and Clinical Neurophysiology, 87, 154–163.

    Article  PubMed  Google Scholar 

  • Webb, S. J., Dawson, G., Bernier, R., & Panagiotides, H. (2006). ERP evidence of atypical face processing in young children with autism. Journal of Autism and Developmental Disorders, 36, 881–890.

    Article  PubMed  PubMed Central  Google Scholar 

  • Webb, S. J., Jones, E. J. H., Merkle, K., Namkung, J., Toth, K., Greenson, J., et al. (2010). Toddlers with elevated autism symptoms show slowed habituation to faces. Child Neuropsychology: A Journal on Normal and Abnormal Development in Childhood and Adolescence, 16(3), 255–278.

    Article  Google Scholar 

  • Webb, S. J., Neuhaus, E., & Faja, S. (in press). Face perception and learning in autism spectrum disorders. The Quarterly Journal of Experimental Psychology. doi:10.1080/17470218.2016.1151059.

Download references

Acknowledgments

Support for this project was provided by NICHD and NIDCD PO1HD34565 and an Autism Speaks Meixner Translational Postdoctoral Fellowship (Neuhaus).

Author Contributions

Conceptualization: GD, SW, AE; Methodology: GD, SW, AE, JM; Formal Analysis: EJ, EN; Investigation: SW, AE, LS, KB, EN; Writing - Original Draft: EN, SW; Writing - Review & Editing: all authors; Project Administration: GD, AE, SW.

Author information

Authors and Affiliations

  1. Center on Child Health, Behavior, and Development, Seattle Children’s Research Institute, PO Box 5371, Seattle, WA, 98145, USA

    Emily Neuhaus, Karen Barnes & Sara J. Webb

  2. Centre for Brain and Cognitive Development, Birkbeck, University of London, London, UK

    Emily J. H. Jones

  3. Department of Psychology, California State University, Long Beach, CA, USA

    Lindsey Sterling

  4. Department of Speech and Hearing Sciences, University of Washington, Seattle, WA, USA

    Annette Estes

  5. Department of Psychiatry and Behavioral Sciences, University of Washington, Seattle, WA, USA

    Jeff Munson & Sara J. Webb

  6. Duke Center for Autism and Brain Development, Department of Psychiatry and Behavioral Sciences, Duke University, Durham, NC, USA

    Geraldine Dawson

  7. Department of Psychology, University of Washington, Seattle, WA, USA

    Geraldine Dawson

Authors
  1. Emily Neuhaus
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Emily J. H. Jones
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Karen Barnes
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lindsey Sterling
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Annette Estes
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jeff Munson
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Geraldine Dawson
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Sara J. Webb
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sara J. Webb.

Ethics declarations

Ethical Approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Neuhaus, E., Jones, E.J.H., Barnes, K. et al. The Relationship Between Early Neural Responses to Emotional Faces at Age 3 and Later Autism and Anxiety Symptoms in Adolescents with Autism. J Autism Dev Disord 46, 2450–2463 (2016). https://doi.org/10.1007/s10803-016-2780-y

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10803-016-2780-y

Keywords

Search

Navigation