European Child & Adolescent Psychiatry

, Volume 26, Issue 12, pp 1423–1432 | Cite as

Autonomic arousal in anxious and typically developing youth during a stressor involving error feedback

  • Michelle Rozenman
  • Alexandra Sturm
  • James T. McCracken
  • John Piacentini
Original Contribution


Anxiety has been proposed to influence psychophysiological reactivity in children and adolescents. However, the extant empirical literature has not always found physiological reactivity to be associated with anxiety in youth. Further, most investigations have not examined psychophysiological reactivity in real time over the course of acute stress. To test the impact of anxiety disorder status on autonomic arousal in youth, we compared youth with primary anxiety disorders (N = 24) to typically developing (TD) youth (N = 22) on heart rate (HR), heart rate variability (HRV), and respiratory sinus arrhythmia (RSA) during an acute stressor in which youth received error-related feedback. We also conducted exploratory analyses on youth performance during the task. Youth ages 9–17 participated in the arithmetic portion of the Trier Social Stress Test for Children (Buske-Kirschbaum et al., Psychosom 59:419–426, 1997), during which time they received consecutive, standardized feedback that they made calculation errors. Results indicated that, compared to their TD counterparts, the anxious group demonstrated elevated HR and suppressed HRV during initial provision of error feedback and during the recovery period. No group differences were found for RSA. Additionally, overall TD youth made a greater proportion of errors than anxious youth. Clinically, these findings may provide preliminary support for anxious youth exhibiting physiological reactivity in response to receipt of error-related feedback, and may have implications for understanding biological processes during stress. This work underscores the need for further study of when and how anxiety may influence autonomic reactivity over the course of stress.


Anxiety Child Adolescent Psychophysiology Heart rate Stress 



This work was supported by the UCLA Research Program for Psychobiological Sciences T32 MH 17140 (Leuchter) and the UCLA Clinical Translational Science Institute UL1TR000124 (Rozenman). The authors would like to acknowledge and thank the children and their parents who participated in this research.

Compliance with ethical standards

Conflict of interest

The authors report no conflicts of interest for the current work.


  1. 1.
    Costello EJ, Egger H, Angold A (2005) 10-year research update review: the epidemiology of child and adolescent psychiatric disorders: I. Methods and public health burden. J Am Acad Child Adolesc Psychiatry 44:972–986. doi: 10.1097/01.chi.0000172552.041596.6f CrossRefPubMedGoogle Scholar
  2. 2.
    Bittner A, Egger HL, Erkanli A, Costello JE, Foley DL, Angold A (2007) What do childhood anxiety disorders predict? J Child Psychol Psychiatr 48:1174–1183. doi: 10.1111/j.1469-7610.2007.01812.x CrossRefGoogle Scholar
  3. 3.
    Sherrill JT (2008) Commentary: expanding the research agenda on interventions for child and adolescent anxiety disorders. Cogn Behav Pract 15:166–171. doi: 10.1016/j.cbpra.2007.11.002 CrossRefGoogle Scholar
  4. 4.
    Beesdo K, Knappe S, Pine DS (2009) Anxiety and anxiety disorders in children and adolescents: devleopmental issues and implications for DSM-V. Psychiatr Clin North Am 32:483–542. doi: 10.1016/j.psc.2009.06.002 CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Pine DS, Cohen P, Gurley D, Brook J, Ma Y (1998) The risk for early-adulthood anxiety and depressive disorders in adolescents with anxiety and depressive disorders. Arch Gen Psychiatr 55:56–64. doi: 10.1001/archpsyc.55.1.56 CrossRefPubMedGoogle Scholar
  6. 6.
    March JS (2011) Looking to the future of research in pediatric anxiety disorders. Depress Anxiety 28:88–98. doi: 10.1002/da.20754 CrossRefPubMedGoogle Scholar
  7. 7.
    Pine DS (2007) Research review: a neuroscience framework for pediatric anxiety disorders. J Child Psychol Psychiatr Allied Discip 48:631–648. doi: 10.1111/j.1469-7610.2007.01751.x CrossRefGoogle Scholar
  8. 8.
    Barlow DH (2000) Unraveling the mysteries of anxiety and its disorders from the perspective of emotion theory. Am Psychol 55:1247–1263. doi: 10.1037/0003-066x.55.11.1247 CrossRefPubMedGoogle Scholar
  9. 9.
    Clarke LA, Watson D (1991) Tripartite model of anxiety and depression: psychometric evidence and taxonomic implications. J Abnorm Psychol 100:316–336. doi: 10.1037/0021-843x.100.3.316 CrossRefGoogle Scholar
  10. 10.
    Weems CF (2008) Developmental trajectories of childhood anxiety: identifying continuity and change in anxious emotion. Dev Rev 28:488–502. doi: 10.1016/j:dr.2008.01.001 CrossRefGoogle Scholar
  11. 11.
    Blechert J, Michael T, Williams SL, Purkis HM, Wilhelm FH (2008) When two paradigms meet: does evaluative learning extinguish in differential fear conditioning? Learn Motivation 39:58–70. doi: 10.1016/j.lmot.2007.03.003 CrossRefGoogle Scholar
  12. 12.
    Craske MG, Kircanski K, Zelikowsky M, Mystkowski J, Chowdhury N, Baker A (2008) Optimizing inhibitory learning during exposure therapy. Behav Res Ther 46:5–27. doi: 10.1016/j.brat.2007.10.003 CrossRefPubMedGoogle Scholar
  13. 13.
    Lau JYF, Lissek S, Nelson EE, Lee Y, Roberson-Nay R, Poeth K et al (2008) Fear conditioning in adolescents with anxiety disorders: results from a novel experimental paradigm. J Am Acad Child Adolesc Psychiatr 47:94–102. doi: 10.1097/chi.0b01e31815a5f01 CrossRefGoogle Scholar
  14. 14.
    Kossowsky J, Wilhelm FH, Roth WT, Schneider S (2012) Separation anxiety disorder in children: disorder-specific responses to experimental separation from the mother. J Child Psychol Psychiatr 53:178–187. doi: 10.1111/j.1469-7610.2011.02465.x CrossRefGoogle Scholar
  15. 15.
    Rozenman M, Vreeland A, Piacentini J (2017) Thinking anxious, feeling anxious, or both? Cognitive bias moderates the relationship between anxiety disorder status and sympathetic arousal in youth. J Anx Disord 45:34–42. doi: 10.1016/j.janxdis.2016.11.004 CrossRefGoogle Scholar
  16. 16.
    Kramer M, Seefeldt WL, Heinrichs N, Tuschen-Caffier B, Schmitz J, Wolf OT et al (2011) Subjective, autonomic, and endocrine reactivity during social stress in children with social phobia. J Abnorm Child Psychol 40:95–104. doi: 10.1007/s10802-011-9548-9 CrossRefGoogle Scholar
  17. 17.
    Schmitz J, Kramer M, Tuschen-Caffier B, Heinrichs N, Blechert J (2011) Restricted autonomic flexibility in children with social phobia. J Child Psychol Psychiatr 52:1203–1211. doi: 10.1111/j.1469-7610.2011.02417.x CrossRefGoogle Scholar
  18. 18.
    Alkozei A, Cresswell C, Cooper P, Allen J (2015) Autonomic arousal in childhood anxiety disorders: associations with state anxiety and social anxiety disorder. J Affect Disord 175:25–33. doi: 10.1016/j.jad.2014.11.056 CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Anderson E, Hope D (2009) The relationship among social phobia, objective and perceived physiological reactivity, and anxiety sensitivity in an adolescent population. J Anx Disord 23:18–26. doi: 10.1016/j.janxdis.2008.03.011 CrossRefGoogle Scholar
  20. 20.
    Dorn L, Campo J, Thato S, Dahl R, Lewin D (2003) Psychological comorbidity and stress reactivity in children and adolescents with recurrent abdominal pain and anxiety disorders. J Am Acad Child Adolesc Psychiatr 42:66–75. doi: 10.1097/00004583-200301000-00012 CrossRefGoogle Scholar
  21. 21.
    Schmitz J, Tuschen-Caffier B, Wilhelm F, Blechert J (2013) Eur Child Adolesc Psychiatr 22:631–640. doi: 10.1007/s00787-013-0405-y CrossRefGoogle Scholar
  22. 22.
    Miers A, Blote A, Sumter S, Kallen V (2011) Subjective and objective arousal correspondence and the role of self-monitoring processes in high and low socially anxious youth. J Exp Psychopathol 18:322–333. doi: 10.5127/jep.019411 Google Scholar
  23. 23.
    Schmitz J, Blechert J, Kramer M, Asbrand J, Tuschen-Caffier B (2012) Biased perception and interpretation of bodily anxiety symptoms in childhood social anxiety. J Clin Child Adolesc Psychol 41:92–102. doi: 10.1080/15374416.2012.632349 CrossRefPubMedGoogle Scholar
  24. 24.
    Buske-Kirschbaum A, Jobst S, Wustmans A (1997) Attenuated free cortisol response to psychosocial stress in children with atopic dermatitis. Psychosom 59:419–426. doi: 10.1087/00006842-199707000-00012 CrossRefGoogle Scholar
  25. 25.
    Reynolds G, Field A, Askew C (2014) Effect of vicarious fear learning on children’s heart rate responses and attentional bias for novel animals. Emot 14:995–1006. doi: 10.1037/a0037225 CrossRefGoogle Scholar
  26. 26.
    Askew C, Hagel A, Morgan J (2015) Vicarious learning of children’s social-anxiety-related fear beliefs and emotional Stroop bias. Emot 15:501–510. doi: 10.1037/emo00000083 CrossRefGoogle Scholar
  27. 27.
    Kramer M, Schmitz J, Heinrichs N, Tuschen-Caffier B (2011) Self-evaluation, social and cognitive performance in children with social phobia. J Exp Psychopathol 2:586–600. doi: 10.5127/jep.0016311 Google Scholar
  28. 28.
    Miers AC, Blote AW, de Rooij M, Bokhorst CL, Westenberg PM (2013) Trajectories of social anxiety during adolescence: relations with cognition, social competence, and temperament. J Abnorm Child Psychol 41:97–110. doi: 10.1007/s10802-012-9651-6 CrossRefPubMedGoogle Scholar
  29. 29.
    Ashcraft MH, Faust MW (1994) Mathematics anxiety and mental arithmetic performance: an exploratory investigation. Cog Emot 8:97–125. doi: 10.1080/02699939408408931 CrossRefGoogle Scholar
  30. 30.
    Eysenck MW, Calvo MG (1992) Anxiety and performance: the processing efficiency theory. Cog Emot 6:409–434. doi: 10.1080/02699939208409696 CrossRefGoogle Scholar
  31. 31.
    Owens M, Stevenson J, Norgate R, Hadwin JA (2008) Processing efficiency theory in children: working memory as a mediator between trait anxiety and academic performance. Anx Stress Coping 21:417–430. doi: 10.1080/10615800701847823 CrossRefGoogle Scholar
  32. 32.
    Chalmers JA, Quintana DS, Abott MJA, Kemp AH (2014) Anxiety disorders are associated with reduced heart rate variability: a meta-analysis. Front Psychiatr 5:80. doi: 10.3389/fpsyct.2014.00080 CrossRefGoogle Scholar
  33. 33.
    Friedman BH (2007) An autonomic flexibility-neurovisceral integration model of anxiety and cardiac vagal tone. Biol Psychol 74:185–199. doi: 10.1016/j.biopsycho.2005.08.009 CrossRefPubMedGoogle Scholar
  34. 34.
    Graziano P, Derefinko K (2013) Cardiac vagal control and children’s adaptive functioning: a meta-analysis. Biol Psychol 94:22–37. doi: 10.1016/j.biopsycho.2013.04.011 CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Walkup J, Albano A, Piacentini J, Birmaher B, Compton SN, Sherrill JT et al (2008) Cognitive behavioral therapy, sertraline, or a combination in childhood anxiety. New Engl J Med 359:2753–2766. doi: 10.1056/NEJMoa0804633 CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Silverman W, Albano A (1996) Anxiety disorders interview schedule for children-IV. Psychological Corporation, San AntonioGoogle Scholar
  37. 37.
    Silverman W, Saavedra L, Pina A (2001) Test-retest reliability of anxiety symptoms and diagnoses with the anxiety disorders interview schedule for DSM-IV: child and parent versions. J Am Acad Child Adolesc Psychiatr 40:937–944. doi: 10.1097/00004583-200108000-00016 CrossRefGoogle Scholar
  38. 38.
    Wood JJ, Piacentini JC, Bergman RL, McCracken J, Barrios V (2002) Concurrent validity of the anxiety disorders section of the anxiety disorders interview schedule for DSM-IV: child and parent versions. J Clin Child Adolesc Psychol 31:335–342. doi: 10.1207/S15374424JCCP3103_05 CrossRefPubMedGoogle Scholar
  39. 39.
    Kirschbaum C, Pirke KM, Helhammer DH (1993) The ‘Trier Social Stress Test’—a tool for investigating psychobiological stress responses in a laboratory setting. Neuropsychobio 28:76–81. doi: 10.1159/000119004 CrossRefGoogle Scholar
  40. 40.
    Aldao A, McLaughlin KA, Hatzenbuehler ML, Sheridan MA (2014) The relationship between rumination and affective, cognitive, and physiological responses to stress in adolescents. J Exp Pscychopathol 5:272–288. doi: 10.5127/jep.039113 CrossRefGoogle Scholar
  41. 41.
    Gilissen R, Bakermans-Kranenburg MJ, van Ijzendoorn MH, Linting M (2008) Electrodermal reactivity during the Trier Social Stress Test for children: interaction between the serotonin transporter polymorphism and children’s attachment representation. Dev Psychobio 50:615–625. doi: 10.1002/dev.20314 CrossRefGoogle Scholar
  42. 42.
    Kudielka BM, Buske-Kirschbaum A, Hellhammer DH, Kurschbaum C (2004) HPA axis responses to laboratory psychosocial stress in healthy adults, younger adults, and children: impact of age and gender. Psychoneuroendocrinol 29:83–98. doi: 10.1016/S0306-4530(02)00146-4 CrossRefGoogle Scholar
  43. 43.
    Silvetti MS, Drago F, Ragonese P (2001) Heart rate variability in healthy children and adolescents is partially related to age and gender. Int J Cardiol 81:169–174. doi: 10.1016/S0167-5273(01)00537-x CrossRefPubMedGoogle Scholar
  44. 44.
    Burkholder AR, Koss KJ, Hostinar CE, Johnson AE, Gunnar MR (2016) Early life stress: effects on the regulation of anxiety expression in children and adolescents. Soc Dev 25:777–793. doi: 10.1111/sode.12170 CrossRefPubMedGoogle Scholar
  45. 45.
    Lang PJ, Davis M, Öhman A (2000) Fear and anxiety: animal models and human cognitive psychophysiology. J Affect Disord 61:137–159. doi: 10.1016/S0165-0327(00)00343-8 CrossRefPubMedGoogle Scholar
  46. 46.
    Steimer T (2002) State of the art: the biology of fear- and anxiety-related behavior. Dialogues Clin Neurosci 4:231–249PubMedPubMedCentralGoogle Scholar
  47. 47.
    Gentzler AL, Snatucci AK, Kovacs M, Fox NA (2009) Respiratory sinus arrhythmia reactivity predicts emotion regulation and depressive symptoms in at-risk and control children. Biol Psychol 82:156–163. doi: 10.1016/j.biopsycho.2009.07.002 CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Field AP, Schorah H (2007) The verbal information pathway to fear and heart rate changes in children. J Child Psychol Psychiatr 48:1088–1093. doi: 10.1111/j.1469-7610.2007.01772.x CrossRefGoogle Scholar
  49. 49.
    Kudielka BM, Hellhammer DH, Kirschbaum C, Harmon-Jones E, Winkielman P (2007) Ten years of research with the Trier Social Stress Test—revisited. Social neuroscience: Integrating biological and psychological explanations of social behavior, pp 56–83Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Michelle Rozenman
    • 1
  • Alexandra Sturm
    • 1
  • James T. McCracken
    • 1
  • John Piacentini
    • 1
  1. 1.Division of Child and Adolescent PsychiatryUCLA Semel Institute for Neuroscience and Human BehaviorLos AngelesUSA

Personalised recommendations