Psychophysiological Arousal to Social Stress in Autism Spectrum Disorders

  • Todd P. Levine
  • Elisabeth Conradt
  • Matthew S. Goodwin
  • Stephen J. Sheinkopf
  • Barry Lester


Individuals with autism spectrum disorders (ASDs) have social deficits which can lead to academic, occupational, and psychiatric difficulties. These individuals face multiple social challenges during the course of their lives which are exacerbated by difficulties understanding, processing, and describing social and emotional content in themselves and others. Self-report of such experiences is challenging for many individuals with ASD. As a result, there has been increasing interest in observing responses to social and nonsocial experiences across multiple levels of analysis, including measurement of psychophysiological systems related to homeostatic regulation. The study of psychophysiological arousal patterns in children and adults with ASDs during social stress provides information about the nature of, and individual differences in, emotional reactivity that is difficult, if not impossible, to achieve via self-report. However, psychophysiological markers of social stress in children and adults with ASDs (including sympathetic, parasympathetic, and hormonal) have yielded inconsistent results. In this chapter, we attempt to disentangle why these inconsistencies have emerged, within the context of the complex relations between these markers.


Autism Spectrum Disorder Heart Rate Variability Salivary Cortisol Social Stress Respiratory Sinus Arrhythmia 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. American Psychiatric Association. Diagnostic and statistical manual of mental disorders. Text revision (DSM-IVTR). 4th ed. Washington, DC: American Psychiatric Publishing; 2000.CrossRefGoogle Scholar
  2. Bal E, Harden E, Lamb D, et al. Emotion recognition in children with autism spectrum disorders: relations to eye gaze and autonomic state. J Autism Dev Disord. 2010;40:358–70.PubMedCrossRefGoogle Scholar
  3. Baron-Cohen S, Leslie AM, Frith U. Does the autistic child have a “theory of mind”? Cognition. 1985;21:37–46.PubMedCrossRefGoogle Scholar
  4. Beauchaine T. Vagal tone, development, and Gray’s motivational theory: toward an integrated model of autonomic nervous system functioning in psychopathology. Dev Psychopathol. 2001;13:183–214.PubMedCrossRefGoogle Scholar
  5. Ben Shalom D, Mostofsky SH, Hazlett RL, et al. Normal physiological emotions but differences in expression of conscious feelings in children with high-functioning autism. J Autism Dev Disord. 2006;36:395–400.PubMedCrossRefGoogle Scholar
  6. Berntson GG, Cacioppo JT, Quigley KS. Autonomic determinism: the modes of autonomic control, the doctrine of autonomic space, and the laws of autonomic constraint. Psychol Rev. 1991;98:459–87.PubMedCrossRefGoogle Scholar
  7. Bosch JA, de Geus EJ, Carroll D, et al. A general enhancement of autonomic and cortisol responses during social evaluative threat. Psychosom Med. 2009;71:877–85.PubMedCrossRefGoogle Scholar
  8. Buske-Kirschbaum A, Jobst S, Psych D, et al. Attenuated free cortisol response to psychosocial stress in children with atopic dermatitis. Psychosom Med. 1997;59:419–26.PubMedGoogle Scholar
  9. Carlson M, Earls F. Psychological and neuroendocrinological sequelae of early social deprivation in institutionalized children in Romania. Ann N Y Acad Sci. 1997;807:419–28.PubMedCrossRefGoogle Scholar
  10. Carpenter LL, Carvalho JP, Tyrka AR, et al. Decreased adrenocorticotropic hormone and cortisol responses to stress in healthy adults reporting significant childhood maltreatment. Biol Psychiatry. 2007;62:1080–7.PubMedCrossRefGoogle Scholar
  11. Cautela J, Groden J. Relaxation: a comprehensive manual for adults, children and children with special needs. Champaign: Research Press; 1978.Google Scholar
  12. Cervantes Blasquez JC, Rodas Font G, Capdevila Ortis L. Heart-rate variability and precompetitive anxiety in swimmers. Psicothema. 2009;21:531–6.PubMedGoogle Scholar
  13. Corbett BA, Mendoza S, Abdullah M, et al. Cortisol circadian rhythms and response to stress in children with autism. Psychoneuroendocrinology. 2006;31:59–68.PubMedCrossRefGoogle Scholar
  14. Corbett BA, Mendoza S, Wegelin JA, et al. Variable cortisol circadian rhythms in children with autism and anticipatory stress. J Psychiatry Neurosci. 2008;33:227–34.PubMedGoogle Scholar
  15. Corbett BA, Schupp CW, Levine S, et al. Comparing cortisol, stress, and sensory sensitivity in children with autism. Autism Res. 2009;2:39–49.PubMedCrossRefGoogle Scholar
  16. Corbett BA, Schupp CW, Simon D, et al. Elevated cortisol during play is associated with age and social engagement in children with autism. Mol Autism. 2010;1:13.PubMedCrossRefGoogle Scholar
  17. Corona R, Dissanayake C, Arbelle S, et al. Is affect aversive to young children with autism? Behavioral and cardiac responses to experimenter distress. Child Dev. 1998;69:1494–502.PubMedGoogle Scholar
  18. Critchley HD. Electrodermal responses: what happens in the brain. Neuroscientist. 2002;8:132–42.PubMedCrossRefGoogle Scholar
  19. Dawson G. A psychobiological perspective on the early socio-emotional development of children with autism. In: Cicchetti D, Toth SL, editors. Rochester symposium on developmental psychopathology: vol. 3. Models and integrations. Rochester: University of Rochester Press; 1991. p. 207–34.Google Scholar
  20. Dawson G, Lewy A. Arousal, attention, and the socioemotional impairments of individuals with autism. In: Dawson G, editor. Autism: nature, diagnosis, and treatment. New York: Guilford Press; 1989. p. 49–74.Google Scholar
  21. DesLauriers AM, Carlson CF. Your child is asleep: early infantile autism. Homewood: Dorsey Press; 1969.Google Scholar
  22. Elzinga BM, Roelofs K, Tollenaar MS, et al. Diminished cortisol responses to psychosocial stress associated with lifetime adverse events a study among healthy young subjects. Psychoneuroendocrinology. 2008;33:227–37.PubMedCrossRefGoogle Scholar
  23. Fernald LC, Burke HM, Gunnar MR. Salivary cortisol levels in children of low-income women with high depressive symptomatology. Dev Psychopathol. 2008;20:423–36.PubMedCrossRefGoogle Scholar
  24. Field T, Diego M. Vagal activity, early growth and emotional development. Infant Behav Dev. 2008;31:361–73.PubMedCrossRefGoogle Scholar
  25. Fisher PA, Gunnar MR, Dozier M, et al. Effects of therapeutic interventions for foster children on behavioral problems, caregiver attachment, and stress regulatory neural systems. Ann N Y Acad Sci. 2006;1094:215–25.PubMedCrossRefGoogle Scholar
  26. Fisher PA, Stoolmiller M, Gunnar MR, et al. Effects of a therapeutic intervention for foster preschoolers on diurnal cortisol activity. Psychoneuroendocrinology. 2007;32:892–905.PubMedCrossRefGoogle Scholar
  27. Fletcher RR, Dobson K, Goodwin MS, et al. iCalm: wearable sensor and network architecture for wirelessly communicating and logging autonomic activity. IEEE Trans Inf Technol Biomed. 2010;14:215–23.PubMedCrossRefGoogle Scholar
  28. Fries E, Hesse J, Hellhammer J, et al. A new view on hypocortisolism. Psychoneuroendocrinology. 2005;30:1010–6.PubMedCrossRefGoogle Scholar
  29. Goenjian AK, Yehuda R, Pynoos RS, et al. Basal cortisol, dexamethasone suppression of cortisol, and MHPG in adolescents after the 1988 earthquake in Armenia. Am J Psychiatry. 1996;153:929–34.PubMedGoogle Scholar
  30. Granger DA, Kivlighan KT, el-Sheikh M, et al. Salivary alpha-amylase in biobehavioral research: recent developments and applications. Ann N Y Acad Sci. 2007;1098:122–44.PubMedCrossRefGoogle Scholar
  31. Groden J, LeVasseur P, Diller A, Cautela J. Coping with stress through picture rehearsal: a how-to manual for working with individuals with autism and developmental disabilities. Providence: The Groden Center; 1989.Google Scholar
  32. Gunnar MR, Talge NM, Herrera A. Stressor paradigms in developmental studies: what does and does not work to produce mean increases in salivary cortisol. Psychoneuroendocrinology. 2009a;34:953–67.PubMedCrossRefGoogle Scholar
  33. Gunnar MR, Wewerka S, Frenn K, et al. Developmental changes in hypothalamus-pituitary-adrenal activity over the transition to adolescence: normative changes and associations with puberty. Dev Psychopathol. 2009b;21:69–85.PubMedCrossRefGoogle Scholar
  34. Hammel JC, Smitherman TA, McGlynn FD, et al. Vagal influence during worry and cognitive challenge. Anxiety Stress Coping. 2010;24:1–16.Google Scholar
  35. Heim C, Ehlert U, Hellhammer DH. The potential role of hypocortisolism in the pathophysiology of stress-related bodily disorders. Psychoneuroendocrinology. 2000;25:1–35.PubMedCrossRefGoogle Scholar
  36. Hill E, Berthoz S, Frith U. Brief report: cognitive processing of own emotions in individuals with autistic spectrum disorder and in their relatives. J Autism Dev Disord. 2004;34:229–35.PubMedCrossRefGoogle Scholar
  37. Hinnant JB, El-Sheikh M. Children’s externalizing and internalizing symptoms over time: the role of individual differences in patterns of RSA responding. J Abnorm Child Psychol. 2009;37:1049–61.PubMedCrossRefGoogle Scholar
  38. Hirstein W, Iversen P, Ramachandran VS. Autonomic responses of autistic children to people and objects. Proc Biol Sci. 2001;268:1883–8.PubMedCrossRefGoogle Scholar
  39. Hutt C, Hutt SJ, Lee D, et al. Arousal and childhood autism. Nature. 1964;204:908–9.PubMedCrossRefGoogle Scholar
  40. Jansen LM, Gispen-de Wied CC, van der Gaag RJ, et al. Differentiation between autism and multiple complex developmental disorder in response to psychosocial stress. Neuropsychopharmacology. 2003;28:582–90.PubMedCrossRefGoogle Scholar
  41. Jessop DS, Turner-Cobb JM. Measurement and meaning of salivary cortisol: a focus on health and disease in children. Stress. 2008;11:1–14.PubMedCrossRefGoogle Scholar
  42. Kaartinen M, Puura K, Makela T, et al. Autonomic arousal to direct gaze correlates with social impairments among children with ASD. J Autism Dev Disord. 2012;42(9):1917–27.PubMedCrossRefGoogle Scholar
  43. Kaufman J. Depressive disorders in maltreated children. J Am Acad Child Adolesc Psychiatry. 1991;30:257–65.PubMedCrossRefGoogle Scholar
  44. Kennedy DP, Courchesne E. The intrinsic functional organization of the brain is altered in autism. Neuroimage. 2008;39:1877–85.PubMedCrossRefGoogle Scholar
  45. Kinsbourne M. Cerebral brainstem relations in infantile autism. In: Schopler E, Mesibov GB, editors. Neurobiological issues in autism. New York: Plenum Press; 1987. p. 107–25.CrossRefGoogle Scholar
  46. Kirschbaum C, Pirke KM, Hellhammer DH. The ‘Trier Social Stress Test’–a tool for investigating psychobiological stress responses in a laboratory setting. Neuropsychobiology. 1993;28:76–81.PubMedCrossRefGoogle Scholar
  47. Klaassens ER, van Noorden MS, Giltay EJ, et al. Effects of childhood trauma on HPA-axis reactivity in women free of lifetime psychopathology. Prog Neuropsychopharmacol Biol Psychiatry. 2009;33:889–94.PubMedCrossRefGoogle Scholar
  48. Kudielka BM, Buske-Kirschbaum A, Hellhammer DH, et al. Differential heart rate reactivity and recovery after psychosocial stress (TSST) in healthy children, younger adults, and elderly adults: the impact of age and gender. Int J Behav Med. 2004;11:116–21.PubMedCrossRefGoogle Scholar
  49. Kylliainen A, Hietanen JK. Skin conductance responses to another person’s gaze in children with autism. J Autism Dev Disord. 2006;36:517–25.PubMedCrossRefGoogle Scholar
  50. Kylliainen A, Wallace S, Coutanche MN, et al. Affective-motivational brain responses to direct gaze in children with autism spectrum disorder. J Child Psychol Psychiatry. 2012;53:790–7.PubMedCrossRefGoogle Scholar
  51. Lanni KE, Schupp CW, Simon D, et al. Verbal ability, social stress, and anxiety in children with autistic disorder. Autism. 2012;16:123–38.PubMedCrossRefGoogle Scholar
  52. Lester BM, Lagasse LL, Shankaran S, et al. Prenatal cocaine exposure related to cortisol stress reactivity in 11-year-old children. J Pediatr. 2010;157:288–95. e281.PubMedCrossRefGoogle Scholar
  53. Lazarus RS, Folkman S. Stress, appraisal, and coping. New York: Springer; 1984.Google Scholar
  54. Levine TP, Sheinkopf SJ, Pescosolido M, et al. Physiologic arousal to social stress in children with autism spectrum disorders: a pilot study. Res Autism Spectr Disord. 2012;6:177–83.PubMedCrossRefGoogle Scholar
  55. Lopata C, Volker MA, Putnam SK, et al. Effect of social familiarity on salivary cortisol and self-reports of social anxiety and stress in children with high functioning autism spectrum disorders. J Autism Dev Disord. 2008;38:1866–77.PubMedCrossRefGoogle Scholar
  56. Lord C, McGee JP. Educating children with autism. Washington, DC: National Academy Press; 2001.Google Scholar
  57. Losh M, Capps L. Understanding of emotional experience in autism: insights from the personal accounts of high-functioning children with autism. Dev Psychol. 2006;42:809–18.PubMedCrossRefGoogle Scholar
  58. Ming X, Julu PO, Brimacombe M, et al. Reduced cardiac parasympathetic activity in children with autism. Brain Dev. 2005;27:509–16.PubMedCrossRefGoogle Scholar
  59. Ornitz EM. Autism at the interface between sensory and information processing. In: Dawson G, editor. Autism: nature, diagnosis, and treatment. New York: Guilford Press; 1989. p. 174–297.Google Scholar
  60. Ornitz EM, Ritvo ER. Perceptual inconstancy in early infantile autism. Arch Gen Psychiatry. 1968;18:76–98.PubMedCrossRefGoogle Scholar
  61. Palkovitz RJ, Wiesenfeld AR. Differential autonomic responses of autistic and normal children. J Autism Dev Disord. 1980;10:347–60.PubMedCrossRefGoogle Scholar
  62. Pieper S, Brosschot JF, van der Leeden R, et al. Cardiac effects of momentary assessed worry episodes and stressful events. Psychosom Med. 2007;69:901–9.PubMedCrossRefGoogle Scholar
  63. Poh MZ, Swenson NC, Picard RW. A wearable sensor for unobtrusive, long-term assessment of electrodermal activity. IEEE Trans Biomed Eng. 2010;57:1243–52.PubMedCrossRefGoogle Scholar
  64. Porges SW. The polyvagal theory: phylogenetic substrates of a social nervous system. Int J Psychophysiol. 2001;42:123–46.PubMedCrossRefGoogle Scholar
  65. Prizant BM, Wetherby AM, Rubin E, Laurent AC. The SCERTS model: a transactional, family-centered approach to enhancing communication and socioemotional abilities of children with autism spectrum disorder. Infants and Young Children. 2003;16:296–316.CrossRefGoogle Scholar
  66. Raison CL, Miller AH. When not enough is too much: the role of insufficient glucocorticoid signaling in the pathophysiology of stress-related disorders. Am J Psychiatry. 2003;160:1554–65.PubMedCrossRefGoogle Scholar
  67. Rieffe C, Meerum Terwogt M, Kotronopoulou K. Awareness of single and multiple emotions in high-functioning children with autism. J Autism Dev Disord. 2007;37:455–65.PubMedCrossRefGoogle Scholar
  68. Rimmele U, Seiler R, Marti B, et al. The level of physical activity affects adrenal and cardiovascular reactivity to psychosocial stress. Psychoneuroendocrinology. 2009;34:190–8.PubMedCrossRefGoogle Scholar
  69. Rohleder N, Joksimovic L, Wolf JM, et al. Hypocortisolism and increased glucocorticoid sensitivity of pro-Inflammatory cytokine production in Bosnian war refugees with posttraumatic stress disorder. Biol Psychiatry. 2004;55:745–51.PubMedCrossRefGoogle Scholar
  70. Sato K, Kang WH, Saga K, et al. Biology of sweat glands and their disorders. I. Normal sweat gland function. J Am Acad Dermatol. 1989;20:537–63.PubMedCrossRefGoogle Scholar
  71. Schmitz J, Kramer M, Tuschen-Caffier B, et al. Restricted autonomic flexibility in children with social phobia. J Child Psychol Psychiatry. 2011;52:1203–11.PubMedCrossRefGoogle Scholar
  72. Schultz RT. Developmental deficits in social perception in autism: the role of the amygdala and fusiform face area. Int J Dev Neurosci. 2005;23:125–41.PubMedCrossRefGoogle Scholar
  73. Siegel B. When atypical development and typical development cross paths. In: Siegel B, editor. Helping children with autism learn. New York: Oxford University Press; 2003. p. 40–76.Google Scholar
  74. Sigman M, Dissanayake C, Corona R, et al. Social and cardiac responses of young children with autism. Autism. 2003;7:205–16.PubMedCrossRefGoogle Scholar
  75. Smeets T. Autonomic and hypothalamic-pituitary-adrenal stress resilience: Impact of cardiac vagal tone. Biol Psychol. 2010;84:290–5.PubMedCrossRefGoogle Scholar
  76. Susman EJ, Dockray S, Schiefelbein VL, et al. Morningness/eveningness, morning-to-afternoon cortisol ratio, and antisocial behavior problems during puberty. Dev Psychol. 2007;43:811–22.PubMedCrossRefGoogle Scholar
  77. Thayer JF, Friedman BH, Borkovec TD. Autonomic characteristics of generalized anxiety disorder and worry. Biol Psychiatry. 1996;39:255–66.PubMedCrossRefGoogle Scholar
  78. Thayer JF, Brosschot JF. Psychosomatics and psychopathology: looking up and down from the brain. Psychoneuroendocrinology. 2005;30:1050–8.PubMedCrossRefGoogle Scholar
  79. Tornhage CJ. Salivary cortisol for assessment of hypothalamic-pituitary-adrenal axis function. Neuroimmunomodulation. 2009;16:284–9.PubMedCrossRefGoogle Scholar
  80. Van Hecke Vaughan A, Lebow J, Bal E, et al. Electroencephalogram and heart rate regulation to familiar and unfamiliar people in children with autism spectrum disorders. Child Dev. 2009;80:1118–33.CrossRefGoogle Scholar
  81. Yoshie M, Kudo K, Murakoshi T, et al. Music performance anxiety in skilled pianists: effects of social-evaluative performance situation on subjective, autonomic, and electromyographic reactions. Exp Brain Res. 2009;199:117–26.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Todd P. Levine
    • 1
  • Elisabeth Conradt
    • 2
  • Matthew S. Goodwin
    • 3
  • Stephen J. Sheinkopf
    • 2
  • Barry Lester
    • 2
  1. 1.Brown Center for the Study of Children at RiskWomen and Infants’ Hospital of Rhode IslandProvidenceUSA
  2. 2.Departments of Psychiatry and Human Behavior and PediatricsAlpert Medical School of Brown University, Brown Center for the Study of Children at RiskProvidenceUSA
  3. 3.Department of Health SciencesNortheastern University, Bouvé; College of Health Science & College of Computer and Information ScienceBostonUSA

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