Journal of Autism and Developmental Disorders

, Volume 46, Issue 7, pp 2450–2463 | Cite as

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

  • Emily Neuhaus
  • Emily J. H. Jones
  • Karen Barnes
  • Lindsey Sterling
  • Annette Estes
  • Jeff Munson
  • Geraldine Dawson
  • Sara J. Webb
Original Paper


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.


Autism Face processing ERP Internalizing Anxiety 



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.

Compliance with Ethical Standards

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.


  1. 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.CrossRefGoogle Scholar
  2. 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.CrossRefPubMedGoogle Scholar
  3. Bar-Haim, Y., Lamy, D., & Glickman, S. (2005). Attentional bias in anxiety: A behavioral and ERP study. Brain and Cognition, 59, 11–22.CrossRefPubMedGoogle Scholar
  4. Baron-Cohen, S. (2005). Mindblindness: An essay on autism and theory of mind. Cambridge, MA: MIT Press.Google Scholar
  5. 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.CrossRefPubMedGoogle Scholar
  6. 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.Google Scholar
  7. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  8. 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.CrossRefGoogle Scholar
  9. Bryk, A. S., & Raudenbush, S. W. (1992). Hierarchical linear models. Newbury Park, CA: Sage.Google Scholar
  10. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  11. 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
  12. 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.CrossRefPubMedGoogle Scholar
  13. 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.CrossRefPubMedGoogle Scholar
  14. 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.CrossRefGoogle Scholar
  15. 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
  16. Ekman, P., & Friesen, W. V. (1976). Pictures of facial affect. Palo Alto, CA: Consulting Psychologists Press.Google Scholar
  17. 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.CrossRefPubMedGoogle Scholar
  18. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 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.CrossRefGoogle Scholar
  20. 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.CrossRefPubMedGoogle Scholar
  21. Golarai, G., Grill-Spector, K., & Reiss, A. L. (2006). Autism and the development of face processing. Clinical Neuroscience Research, 6, 145–160.CrossRefPubMedPubMedCentralGoogle Scholar
  22. 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.CrossRefPubMedGoogle Scholar
  23. 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.CrossRefPubMedGoogle Scholar
  24. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  25. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  26. 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.CrossRefPubMedGoogle Scholar
  27. 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.CrossRefPubMedGoogle Scholar
  28. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  29. Kanwisher, N. (2000). Domain specificity in face perception. Nature Neuroscience, 3(8), 759–763.CrossRefPubMedGoogle Scholar
  30. Lord, C., Rutter, M., DiLavore, P. C., & Risi, S. (2003). Autism Diagnostic Observation Schedule manual. Los Angeles, CA: Western Psychological Services.Google Scholar
  31. 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.CrossRefPubMedGoogle Scholar
  32. 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.CrossRefPubMedGoogle Scholar
  33. 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
  34. 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.Google Scholar
  35. Mogg, K., Garner, M., & Bradley, B. P. (2007). Anxiety and orienting of gaze to angry and fearful faces. Biological Psychology, 76, 163–169.CrossRefPubMedPubMedCentralGoogle Scholar
  36. Morton, J., & Johnson, M. H. (1991). CONSPEC and CONLERN: A two-process theory of infant face recognition. Psychological Review, 98(2), 164–181.CrossRefPubMedGoogle Scholar
  37. Mullen, E. M. (1997). Mullen scales of early learning. Los Angeles, CA: Western Psychological Services.Google Scholar
  38. Neuhaus, E., Beauchaine, T. P., & Bernier, R. (2010). Neurobiological correlates of social functioning in autism. Clinical Psychology Review, 30(6), 733–748.CrossRefPubMedGoogle Scholar
  39. 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.CrossRefPubMedGoogle Scholar
  40. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  41. 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.CrossRefPubMedGoogle Scholar
  42. 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.PubMedPubMedCentralGoogle Scholar
  43. 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.CrossRefPubMedGoogle Scholar
  44. Phelps, E. A., & LeDoux, J. E. (2005). Contributions of the amygdala to emotion processing: From animal models to human behavior. Neuron, 48, 175–187.CrossRefPubMedGoogle Scholar
  45. 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.CrossRefPubMedGoogle Scholar
  46. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  47. 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.CrossRefPubMedGoogle Scholar
  48. 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.CrossRefPubMedGoogle Scholar
  49. 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.CrossRefGoogle Scholar
  50. 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.CrossRefPubMedGoogle Scholar
  51. Tucker, D. (1993). Spatial sampling of head electrical fields, the geodesic sensor net. Electroencephalography and Clinical Neurophysiology, 87, 154–163.CrossRefPubMedGoogle Scholar
  52. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  53. 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.CrossRefGoogle Scholar
  54. 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.

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Emily Neuhaus
    • 1
  • Emily J. H. Jones
    • 2
  • Karen Barnes
    • 1
  • Lindsey Sterling
    • 3
  • Annette Estes
    • 4
  • Jeff Munson
    • 5
  • Geraldine Dawson
    • 6
    • 7
  • Sara J. Webb
    • 1
    • 5
  1. 1.Center on Child Health, Behavior, and DevelopmentSeattle Children’s Research InstituteSeattleUSA
  2. 2.Centre for Brain and Cognitive DevelopmentBirkbeck, University of LondonLondonUK
  3. 3.Department of PsychologyCalifornia State UniversityLong BeachUSA
  4. 4.Department of Speech and Hearing SciencesUniversity of WashingtonSeattleUSA
  5. 5.Department of Psychiatry and Behavioral SciencesUniversity of WashingtonSeattleUSA
  6. 6.Duke Center for Autism and Brain Development, Department of Psychiatry and Behavioral SciencesDuke UniversityDurhamUSA
  7. 7.Department of PsychologyUniversity of WashingtonSeattleUSA

Personalised recommendations