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Journal of Autism and Developmental Disorders

, Volume 46, Issue 12, pp 3688–3699 | Cite as

Autonomic Arousal Response Habituation to Social Stimuli Among Children with Asd

  • Miia Kaartinen
  • Kaija Puura
  • Sari-Leena Himanen
  • Jaakko Nevalainen
  • Jari K. Hietanen
Original Paper

Abstract

Sustained autonomic arousal during eye contact could cause the impairments in eye contact behavior commonly seen in autism. The aim of the present study was to re-analyze the data from a study by Kaartinen et al. (J Autism Develop Disord 42(9):1917–1927, 2012) to investigate the habituation of autonomic arousal responses to repeated facial stimuli and the correlations between response habituation and social impairments among children with and without ASD. The results showed that among children with ASD, the smaller the habituation was, specifically in responses to a direct gaze, the more the child showed social impairments. The results imply that decreased autonomic arousal habituation to a direct gaze might play a role in the development of social impairments in autism.

Keywords

Autism ASD Autonomic arousal Habituation Gaze 

Notes

Acknowledgments

This study was financially supported by the European Union (The GEBACO Project), the Medical Research Fund of Tampere University Hospital, The Child Psychiatric Research Foundation (Finland), The Emil Aaltonen Foundation, The Finnish Medical Foundation, the Competitive Research financing of the Expert Responsibility area of Tampere University Hospital (Grant No. 9R007 and 9PO13 to S-LH), and the Academy of Finland (MIND program Grant, Project No. #266187 to JKH). We are very grateful to all the parents and children who participated in this study and made it possible.

Author Contributions

Miia Kaartinen has made substantial contributions to conception and design, and acquisition of data, and analysis and interpretation of data, participated in drafting and revising the article and has given final approval of the version to be submitted. Kaija Puura has made substantial contributions to conception and design, and analysis and interpretation of data, participated in drafting and revising the article and has given final approval of the version to be submitted. Sari-Leena Himanen has made substantial contributions to acquisition of data, has participated in revising the article and has given final approval of the version to be submitted. Jaakko Nevalainen has made substantial contributions to analysis and interpretation of data, participated in drafting and revising the article and has given final approval of the version to be submitted. Jari Hietanen has made substantial contributions to conception and design, and acquisition of data, and analysis and interpretation of data, participated in drafting and revising the article and has given final approval of the version to be submitted.

Funding

This study was financially supported by the European Union (The GEBACO Project), the Medical Research Fund of Tampere University Hospital, The Child Psychiatric Research Foundation (Finland), the Competitive Research financing of the Expert Responsibility area of Tampere University Hospital (Grant No. 9R007 and 9PO13), The Emil Aaltonen Foundation, The Finnish Medical Foundation, and the Academy of Finland (MIND program Grant, Project No. 266187).

Compliance with Ethical Standards

Conflict of Interest

Author Miia Kaartinen has received research grants from the European Union (The GEBACO Project), the Medical Research Fund of Tampere University Hospital, The Child Psychiatric Research Foundation (Finland), The Emil Aaltonen Foundation and The Finnish Medical Foundation, but declares that she has no other conflict of interest. Author Kaija Puura declares that she has no conflict of interest. Author Sari-Leena Himanen is a shareholder in the company Neurotest and has received research grant from Competitive Research financing of the Expert Responsibility area of Tampere University Hospital (Grant No. 9R007 and 9PO13), but declares that she has no other conflict of interest. Author Jaakko Nevalainen declares that he has no conflict of interest. Author Jari Hietanen has received research grant from the Academy of Finland (MIND program Grant, Project No. #266187), but declares that he has no other conflict of interest.

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.

Informed Consent

Informed consent was obtained from all individual participants included in the study.

References

  1. American Psychiatric Association. (2013). Diagnostic and statistical manual of mental disorders (5th ed.). Washington, DC: American Psychiatric Association.CrossRefGoogle Scholar
  2. Batki, A., Baron-Cohen, S., Wheelwright, S., Connellan, J., & Ahluwalia, J. (2002). Is there an innate gaze module? Evidence from human neonates. Infant Behavior and Development, 23(2), 223–229.CrossRefGoogle Scholar
  3. Bedford R, Pickles A, Gliga T, Elsabbagh M, Charman T, & Johnson MH, BASIS Team. (2014). Additive effects of social and non-social attention during infancy relate to later autism spectrum disorder. Developmental Science, 17(4), 612–620.CrossRefPubMedPubMedCentralGoogle Scholar
  4. Breiter, H. C., Etcoff, N. L., Whalen, P. J., Kennedy, W. A., Rauch, S. L., Buckner, R. L., Strauss, M. M., Hyman, S. E., & Rosen, B. R. (1996). Response and habituation of the human amygdala during visual processing of facial expression. Neuron, 17(5), 875–887.CrossRefPubMedGoogle Scholar
  5. Bruno, J. L., Garrett, A. S., Quintin, E. M., Mazaika, P. K., & Reiss, A. L. (2014). Aberrant face and gaze habituation in fragile x syndrome. The American Journal of Psychiatry, 171(10), 1099–1106.CrossRefPubMedPubMedCentralGoogle Scholar
  6. Bryson, S. E., Zwaigenbaum, L., Brian, J., Roberts, W., Szatmari, P., Rombough, V., & McDermott, C. (2007). A prospective case series of high-risk infants who developed autism. Journal of Autism and Developmental Disorders, 37(1), 12–24.CrossRefPubMedGoogle Scholar
  7. Büchel, C., Morris, J., Dolan, R. J., & Friston, K. J. (1998). Brain systems mediating aversive conditioning: An event-related fMRI study. Neuron, 20(5), 947–957.CrossRefPubMedGoogle Scholar
  8. 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(2), 431–442.CrossRefPubMedPubMedCentralGoogle Scholar
  9. Cassel, T. D., Messinger, D. S., Ibanez, 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.CrossRefPubMedGoogle Scholar
  10. Cherulnik, P. D., Neely, W. T., Flanagan, M., & Zachau, M. (1978). Social skill and visual interaction. Journal of Social Psychology, 104(2), 263–270.CrossRefGoogle Scholar
  11. Conzelmann, A., Gerdes, A. B., Mucha, R. F., Weyers, P., Lesch, K. P., Bähne, C. G., Fallgatter, A. J., Renner, T. J., Warnke, A., Romanos, M., & Pauli, P. (2014). Autonomic hypoactivity in boys with attention-deficit/hyperactivity disorder and the influence of methylphenidate. The World Journal of Biological Psychiatry, 15(1), 56–65.CrossRefPubMedGoogle Scholar
  12. Corden, B., Chilvers, R., & Skuse, D. (2008). Avoidance of emotionally arousing stimuli predicts social-perceptual impairment in Asperger’s syndrome. Neuropsychologia, 46(1), 137–147.CrossRefPubMedGoogle Scholar
  13. Critchley, H. D. (2002). Electrodermal responses: What happens in the brain. The Neuroscientist: A Review Journal Bringing Neurobiology, Neurology and Psychiatry, 8(2), 132–142.CrossRefGoogle Scholar
  14. Critchley, H. D. (2009). Psychophysiology of neural, cognitive and affective integration: fMRI and autonomic indicants. International Journal of Psychophysiology, 73(2), 88–94.CrossRefPubMedPubMedCentralGoogle Scholar
  15. Dalton, K. M., Nacewicz, B. M., Alexander, A. L., & Davidson, R. J. (2007). Gaze-fixation, brain activation, and amygdala volume in unaffected siblings of individuals with autism. Biological Psychiatry, 61(4), 512–520.CrossRefPubMedGoogle Scholar
  16. Dalton, K. M., Nacewicz, B. M., Johnstone, T., Schaefer, H. S., Gernsbacher, M. A., Goldsmith, H. H., Alexander, A. L., & Davidson, R. J. (2005). Gaze fixation and the neural circuitry of face processing in autism. Nature Neuroscience, 8(4), 519–526.PubMedPubMedCentralGoogle Scholar
  17. Dawson, G., Webb, S. J., Wijsman, E., Schellenberg, G., Estes, A., Munson, J., & Faja, S. (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.CrossRefPubMedGoogle Scholar
  18. Elison, J. T., Paterson, S. J., Wolff, J. J., Reznick, J. S., Sasson, N. J., Gu, H., Botteron, K. N., Dager, S. R., Estes, A. M., Evans, A. C., Gerig, G., Hazlett, H. C., Schultz, R. T., Styner, M., Zwaigenbaum, L., Piven, J., & IBIS Network. (2013). White matter microstructure and atypical visual orienting in 7-month-olds at risk for autism. The American Journal of Psychiatry, 170(8), 899–908.CrossRefPubMedGoogle Scholar
  19. Elsabbagh, M., Fernandes, J., Jane Webb, S., Dawson, G., Charman, T., Johnson, M. H., & British Autism Study of Infant Siblings Team. (2013). Disengagement of visual attention in infancy is associated with emerging autism in toddlerhood. Biological Psychiatry, 74(3), 189–194.CrossRefPubMedPubMedCentralGoogle Scholar
  20. Elsabbagh, M., & Johnson, M. H. (2010). Getting answers from babies about autism. Trends in Cognitive Sciences, 14(2), 81–87.CrossRefPubMedGoogle Scholar
  21. Ewbank, M. P., Rhodes, G., von dem Hagen EA, Powell, T. E., Bright, N., Stoyanova, R. S., Baron-Cohen, S., & Calder, A. J. (2015). Repetition suppression in ventral visual cortex is diminished as a function of increasing autistic traits. Cerebral Cortex, 25(10), 3381–3393.CrossRefPubMedGoogle Scholar
  22. Falck-Ytter, T., Carlström, C., & Johansson, M. (2015). Eye contact modulates cognitive processing differently in children with autism. Child Development, 86(1), 37–47.CrossRefPubMedGoogle Scholar
  23. Farroni, T., Menon, E., & Johnson, M. H. (2006). Factors influencing newborns’ preference for faces with eye contact. Journal of Experimental Child Psychology, 95(4), 298–308.CrossRefPubMedGoogle Scholar
  24. Frischen, A., Bayliss, A. P., & Tipper, S. P. (2007). Gaze cueing of attention: Visual attention, social cognition, and individual differences. Psychological Bulletin, 133(4), 694–724.CrossRefPubMedPubMedCentralGoogle Scholar
  25. Gaigg, S. B. (2012). The interplay between emotion and cognition in Autism spectrum disorder: implications for developmental theory. Frontiers in Integrative Neuroscience, 6, 113. doi: 10.3389/fnint.2012.00113.CrossRefPubMedPubMedCentralGoogle Scholar
  26. George, N., & Conty, L. (2008). Facing the gaze of others. Clinical Neurophysiology, 38(3), 197–207.CrossRefPubMedGoogle Scholar
  27. Green, M. F., Nuechterlein, K. H., & Satz, P. (1989). The relationship of symptomatology and medication to electrodermal activity in schizophrenia. Psychophysiology, 26(2), 148–157.CrossRefPubMedGoogle Scholar
  28. Guiraud, J. A., Kushnerenko, E., Tomalski, P., Davies, K., Ribeiro, H., Johnson, M. H., & BASIS team (2011). Differential habituation to repeated sounds in infants at high risk for autism. Neuroreport, 22(16), 845–849.PubMedGoogle Scholar
  29. Hadjikhani, N., Hoge, R., Snyder, J., & de Gelder, B. (2008). Pointing with the eyes: The role of gaze in communicating danger. Brain and Cognition, 68(1), 1–8.CrossRefPubMedPubMedCentralGoogle Scholar
  30. Harding, G. B., & Rundle, G. R. (1969). Long-term retention of modality- and nonmodality-specific habituation of the GSR. Journal of Experimental Psychology, 82(2), 390–392.CrossRefPubMedGoogle Scholar
  31. Hutt, C., & Ounsted, C. (1966). The biological significance of gaze aversion with particular reference to the syndrome of infantile autism. Behavioral Sciences, 11(5), 346–356.CrossRefGoogle Scholar
  32. Iarocci, G., & McDonald, J. (2006). Sensory integration and the perceptual experience of persons with autism. Journal of Autism and Developmental Disorders, 36(1), 77–90.CrossRefPubMedGoogle Scholar
  33. Ishai, A., Pessoa, L., Bikle, P. C., & Ungerleider, L. G. (2004). Repetition suppression of faces is modulated by emotion. Proceedings of the National Academy of Sciences of the United States of America, 101(26), 9827–9832.CrossRefPubMedPubMedCentralGoogle Scholar
  34. Jones, E. J., 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.CrossRefGoogle Scholar
  35. Jones W, & Klin A (2013). Attention to eyes is present but in decline in 2–6 month-old later diagnosed with autism. Nature, 504(7480), 427–431.CrossRefPubMedPubMedCentralGoogle Scholar
  36. Jones, W., Carr, K., & Klin, A. (2008). Absence of preferential looking to the eyes of approaching adults predicts level of social disability in 2-year-old toddlers with autism spectrum disorder. Archives of General Psychiatry, 65(8), 946–954.CrossRefPubMedGoogle Scholar
  37. Joseph, R. M., Ehrman, K., McNally, R., & Keehn, B. (2008). Affective response to eye contact and face recognition ability in children with ASD. Journal of the International Neuropsychological Society, 14(6), 947–955.CrossRefPubMedGoogle Scholar
  38. Joseph, R. M., & Tanaka, J. (2003). Holistic and part-based face recognition in children with autism. Journal of Child Psychology and Psychiatry, 44(4), 529–542.CrossRefPubMedGoogle Scholar
  39. Kaartinen, M., Puura, K., Mäkelä, T., Rannisto, M., Lemponen, R., Helminen, M., Salmelin, R., Himanen, S. L., Hietanen, J. K. (2012). Autonomic arousal to direct gaze correlates with social impairments among children with ASD. Journal of Autism and Developmental Disorders, 42(9), 1917–1927.CrossRefPubMedGoogle Scholar
  40. Keehn, B., Müller, R. A., & Townsend, J. (2013). Atypical attentional networks and the emergence of autism. Neuroscience & Biobehavioral Reviews, 37(2), 164–183.CrossRefGoogle Scholar
  41. Keller, H., & Zach, U. (1993). Developmental consequences of early eye contact behaviour. Acta Paedopsychiatrica, 56(1), 31–36.PubMedGoogle Scholar
  42. Kimmel, H. D., & Goldstein, A. J. (1967). Retention of habituation of the GSR to visual and auditory stimulation. Journal of Experimental Psychology, 73(3), 401–404.CrossRefPubMedGoogle Scholar
  43. Kleinhans, N. M., Johnson, L. C., Richards, T., Mahurin, R., Greenson, J., Dawson, G., & Aylward, E. (2009). Reduced neural habituation in the amygdala and social impairments in autism spectrum disorders. The American Journal of Psychiatry, 166(4), 467–475.CrossRefPubMedGoogle Scholar
  44. Kleinke, C. L. (1986). Gaze and eye contact: A research review. Psychological Bulletin, 100(1), 78–100.CrossRefPubMedGoogle Scholar
  45. Kliemann, D., Dziobek, I., Hatri, A., Baudewig, J., & Heekeren, H. R. (2012). The role of the amygdala in atypical gaze on emotional faces in autism spectrum disorders. The Journal of Neuroscience, 32(28), 9469–9476.CrossRefPubMedGoogle Scholar
  46. Klin, A., Jones, W., Schultz, R., Volkmar, F., & Cohen, D. (2002). Visual fixation patterns during viewing of naturalistic social situations as predictors of social competence in individuals with autism. Archives of General Psychiatry, 59(9), 809–816.CrossRefPubMedGoogle Scholar
  47. Klorman, R., & Ryan, R. M. (1980). Heart rate, contingent negative variation, and evoked potentials during anticipation of affective stimulation. Psychophysiology, 17(6), 513–523.CrossRefPubMedGoogle Scholar
  48. Klorman, R., Weissberg, R. P., & Wiesenfeld, A. R. (1977). Individual differences in fear and autonomic reactions to affective stimulation. Psychophysiology, 14(1), 45–51.CrossRefPubMedGoogle Scholar
  49. Klorman, R., Wiesenfeld, A. R., & Austin, M. L. (1975). Autonomic responses to affective visual stimuli. Psychophysiology, 12(5), 553–560.CrossRefPubMedGoogle Scholar
  50. Knight, D. C., Nguyen, H. T., & Bandettini, P. A. (2005). The role of the human amygdala in the production of conditioned fear responses. NeuroImage, 26(4), 1193–1200.CrossRefPubMedGoogle Scholar
  51. Kylliäinen, A., & Hietanen, J. K. (2006). Skin conductance responses to another person’s gaze in children with autism. Journal of Autism and Developmental Disorders, 36(4), 517–525.CrossRefPubMedGoogle Scholar
  52. Kylliäinen, A., Wallace, S., Coutanche, M. N., Leppänen, J. M., Cusack, J., Bailey, A. J., & Hietanen, J. K. (2012). Affective-motivational brain responses to direct gaze in children with autism spectrum disorder. Journal of Child Psychology and Psychiatry, 53(7), 790–797.CrossRefPubMedGoogle Scholar
  53. LaBar, K. S., Gatenby, J. C., Gore, J. C., LeDoux, J. E., & Phelps, E. A. (1998). Human amygdala activation during conditioned fear acquisition and extinction: A mixed-trial fMRI study. Neuron, 20(5), 937–945.CrossRefPubMedGoogle Scholar
  54. Macrae, C. N., Hood, B. M., Milne, A. B., Rowe, A. C., & Mason, M. F. (2002). Are you looking at me? Eye gaze and person perception. Psychological Science, 13(5), 460–464.CrossRefPubMedGoogle Scholar
  55. McIntosh, D. N., Miller, L. J., Shyu, V., & Hagerman, R. J. (1999). Sensory-modulation disruption, electrodermal responses, and functional behaviors. Developmental Medicine & Child Neurology, 41(9), 608–615.CrossRefGoogle Scholar
  56. Nacewicz, B. M., Dalton, K. M., Johnstone, T., Long, M. T., McAuliff, E. M., Oakes, T. R., Alexander, A. L., & Davidson, R. J. (2006). Amygdala volume and nonverbal social impairment in adolescent and adult males with autism. Archives of General Psychiatry, 63(12), 1417–1428.CrossRefPubMedPubMedCentralGoogle Scholar
  57. Negrao, B. L., Bipath, P., van der Westhuizen, D., & Viljoen, M. (2011). Autonomic correlates at rest and during evoked attention in children with attention-deficit/hyperactivity disorder and effects of methylphenidate. Neuropsychobiology, 63(2), 82–91.CrossRefPubMedGoogle Scholar
  58. Nummenmaa, L., & Calder, A. J. (2009). Neural mechanisms of social attention. Trends in Cognitive Sciences, 13(3), 135–143.CrossRefPubMedGoogle Scholar
  59. O’Neill, M., & Jones, R. S. (1997). Sensory-perceptual abnormalities in autism: A case for more research? Journal of Autism and Developmental Disorders, 27(3), 283–293.CrossRefPubMedGoogle Scholar
  60. 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
  61. Pellicano, E., & Macrae, C. N. (2009). Mutual eye gaze facilitates person categorization for typically developing children, but not for children with autism. Psychonomic Bulletin & Review, 16(6), 1094–1099.CrossRefGoogle Scholar
  62. Peltola, M. J., Leppänen, J. M., Mäki, S., & Hietanen, J. K. (2009). Emergence of enhanced attention to fearful faces between 5 and 7 months of age. Social Cognitive and Affective Neuroscience, 4(2), 134–142.CrossRefPubMedPubMedCentralGoogle Scholar
  63. Rice, K., Moriuchi, J. M., Jones, W., & Klin, A. (2012). Parsing heterogeneity in autism spectrum disorders: Visual scanning of dynamic social scenes in school-aged children. Journal of the American Academy of Child and Adolescent Psychiatry, 51(3), 238–248.CrossRefPubMedPubMedCentralGoogle Scholar
  64. Robson, K. S., Pedersen, F. A., & Moss, H. A. (1969). Developmental observations of diadic gazing in relation to the fear of strangers and social approach behavior. Child Development, 40(2), 619–627.CrossRefPubMedGoogle Scholar
  65. Rogers, S. J., & Ozonoff, S. (2005). Annotation: what do we know about sensory dysfunction in autism? A critical review of the empirical evidence. Journal of Child Psychology and Psychiatry, 46(12), 1255–1268.CrossRefPubMedGoogle Scholar
  66. 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.CrossRefPubMedGoogle Scholar
  67. Senju, A., & Hasegawa, T. (2006). Do the upright eyes have it? Psychonomic Bulletin & Review, 13(2), 223–228.CrossRefGoogle Scholar
  68. Senju, A., & Johnson, M. H. (2009). The eye contact effect: Mechanisms and development. Trends in Cognitive Sciences, 13(3), 127–134.CrossRefPubMedGoogle Scholar
  69. Senju, A., Yaguchi, K., Tojo, Y., & Hasegawa, T. (2003). Eye contact does not facilitate detection in children with autism. Cognition, 89(1), B43–B851.CrossRefPubMedGoogle Scholar
  70. Sequeira, H., Hot, P., Silvert, L., & Delplanque, S. (2009). Electrical autonomic correlates of emotion. International Journal of Psychophysiology, 71(1), 50–56.CrossRefPubMedGoogle Scholar
  71. Skuse, D. (2003). Fear recognition and the neural basis of social cognition. Child and Adolescent Mental Health, 8(2), 50–60.CrossRefGoogle Scholar
  72. Skuse, D., Warrington, R., Bishop, D., Chowdhury, U., Lau, J., Mandy, W., & Place, M. (2004). The developmental, dimensional and diagnostic interview (3di): A novel computerized assessment for autism spectrum disorders. Journal of the American Academy of Child and Adolescent Psychiatry, 43(5), 548–558.CrossRefPubMedGoogle Scholar
  73. Spezio, M. L., Adolphs, R., Hurley, R. S., & Piven, J. (2007). Analysis of face gaze in autism using “Bubbles”. Neuropsychologia, 45(1), 144–151.CrossRefPubMedGoogle Scholar
  74. Spohn, H. E., Thetford, P. E., & Cancro, R. (1971). The effects of phenothiazine medication on skin conductance and heart rate in schizophrenic patients. The Journal of Nervous and Mental Disease, 152(2), 129–139.CrossRefPubMedGoogle Scholar
  75. Swartz, J. R., Wiggins, J. L., Carrasco, M., Lord, C., & Monk, C. S. (2013). Amygdala habituation and prefrontal functional connectivity in youth with autism spectrum disorders. Journal of the American Academy of Child and Adolescent Psychiatry, 52(1), 84–93.CrossRefPubMedGoogle Scholar
  76. Tanaka, J. W., & Sung, A. (2016). The “Eye Avoidance” hypothesis of autism face processing. Journal of Autism and Developmental Disorders, 46(5), 1538–1552.CrossRefPubMedGoogle Scholar
  77. Thompson, R. F., & Spencer, W. A. (1966). Habituation: A model phenomenon for the study of neuronal substrates of behavior. Psychological Review, 73(1), 16–43.CrossRefPubMedGoogle Scholar
  78. Tottenham, N., Hertzig, M. E., Gillespie-Lynch, K., Gilhooly, T., Millner, A. J., & Casey, B. J. (2014). Elevated amygdala response to faces and gaze aversion in autism spectrum disorder. Social Cognitive & Affective Neuroscience, 9(1), 106–117.CrossRefGoogle Scholar
  79. Webb, S. J., Jones, E. J., Merkle, K., Namkung, J., Toth, K., Greenson, J., Murias, M., & Dawson, G. (2010). Toddlers with elevated autism symptoms show slowed habituation to faces. Child Neuropsychology, 16(3), 255–278.CrossRefPubMedPubMedCentralGoogle Scholar
  80. 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.CrossRefPubMedGoogle Scholar
  81. Zalla, T., & Sperduti, M. (2013). The amygdala and the relevance detection theory of autism: An evolutionary perspective. Frontiers in Integrative Neuroscience, 7, 894. doi: 10.3389/fnhum.2013.00894.Google Scholar
  82. 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.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  1. 1.Department of Child PsychiatryTampere University Hospital and University of TampereTampereFinland
  2. 2.Human Information Processing Laboratory, School of Social Sciences and Humanities/PsychologyUniversity of TampereTampereFinland
  3. 3.Tampere School of Health SciencesUniversity of TampereTampereFinland
  4. 4.Department of Clinical NeurophysiologyTampere University HospitalTampereFinland

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