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Sympathetic nervous system dominance during stress recovery mediates associations between stress sensitivity and social anxiety symptoms in female adolescents

Published online by Cambridge University Press:  11 January 2021

Tiffany C. Ho ,
Holly T. Pham ,
Jonas G. Miller ,
Katharina Kircanski  and
Ian H. Gotlib
Tiffany C. Ho*
Affiliation:
Department of Psychiatry and Behavioral Sciences; Weill Institute for Neurosciences, University of California, San Francisco, San Francisco, CA, USA Department of Psychology, Stanford University, Stanford, CA, USA
Holly T. Pham
Affiliation:
Department of Psychology, Pennsylvania State University, University Park, PA, USA
Jonas G. Miller
Affiliation:
Department of Psychology, Stanford University, Stanford, CA, USA
Katharina Kircanski
Affiliation:
Emotion and Development Branch, National Institute of Mental Health, Bethesda, MD, USA
Ian H. Gotlib
Affiliation:
Department of Psychology, Stanford University, Stanford, CA, USA
*
Author for Correspondence: Tiffany C. Ho, Ph.D., Department of Psychiatry and Weill Institute for Neurosciences, University of California, San Francisco, 401, Parnassus Avenue, San Francisco, CA94143USA; E-mail: [email protected]
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Abstract

Social anxiety disorder (SAD) is commonly diagnosed during adolescence and is associated with psychological stress reactivity and heightened physiological arousal. No study, however, has systematically examined which aspects of autonomic nervous system function mediate likely links between stress sensitivity and social anxiety symptoms in adolescents. Here, we assessed 163 adolescents (90 females; 12.29 ± 1.39 years) with respect to life stress and social anxiety symptoms, and measured respiratory sinus arrhythmia (RSA) and skin conductance levels (SCL) during a psychosocial stress paradigm. We operationalized stress sensitivity as the residual variance in subjective stress severity after accounting for objective severity and changes in autonomic regulation using standardized change scores in RSA and SCL. In females only, stress sensitivity and social anxiety symptoms were significantly correlated with each other (p < .001) and with autonomic regulation during both reactivity and recovery (all ps < 0.04). Further, sympathetic nervous system dominance during recovery specifically mediated associations between stress sensitivity and social anxiety symptoms (B = 1.06, 95% CI: 0.02–2.64). In contrast, in males, stress sensitivity, autonomic regulation during reactivity or recovery, and social anxiety symptoms were not significantly associated (all ps > 0.1). We interpret these results in the context of psychobiological models of SAD and discuss implications for interventions targeting autonomic processes.

Keywords

adolescencerespiratory sinus arrhythmiaskin conductance level stresssocial anxiety disorder
Type
Special Section 2: Early Adversity and Development: Contributions from the Field
Information
Development and Psychopathology , Volume 32 , Special Issue 5: Early Adversity, Stress, and Neurobehavioral Development: Honoring Megan R. Gunnar's Contributions to Developmental Science , December 2020 , pp. 1914 - 1925
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Copyright
Copyright © Cambridge University Press 2020

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Footnotes

†

Equal contribution.

References

American Psychiatric Association. (2013). Diagnostic and statistical manual of mental disorders (5th ed.). Washington, DC: Publisher.Google Scholar
Angold, A., & Costello, E. J. (1995). Developmental epidemiology. Epidemiologic Reviews, 17, 74–82.CrossRefGoogle ScholarPubMed
Aune, T., & Stiles, T. C. (2009). The effects of depression and stressful life events on the development and maintenance of syndromal social anxiety: Sex and age differences. Journal of Clinical Child & Adolescent Psychology, 38, 501–512.CrossRefGoogle ScholarPubMed
Azadeh, S. M., Kazemi-Zahrani, H., & Besharat, M. A. (2016). Effectiveness of acceptance and commitment therapy on interpersonal problems and psychological flexibility in female high school students with social anxiety disorder. Global Journal of Health Science, 8, 131.CrossRefGoogle Scholar
Baldwin, J. S., & Dadds, M. R. (2007). Reliability and validity of parent and child versions of the multidimensional anxiety scale for children in community samples. Journal of the American Academy of Child & Adolescent Psychiatry, 46, 252–260.CrossRefGoogle ScholarPubMed
Baldwin, J. R., Reuben, A., Newbury, J. B., & Danese, A. (2019). Agreement between prospective and retrospective measures of childhood maltreatment: A systematic review and meta-analysis. JAMA Psychiatry, 76, 584–593.CrossRefGoogle ScholarPubMed
Beesdo, K., Bittner, A., Pine, D. S., Stein, M. B., Höfler, M., Lieb, R., & Wittchen, H. U. (2007). Incidence of social anxiety disorder and the consistent risk for secondary depression in the first three decades of life. Archives of General Psychiatry, 64, 903–912.CrossRefGoogle ScholarPubMed
Beesdo, K., Pine, D. S., Lieb, R., & Wittchen, H. U. (2010). Incidence and risk patterns of anxiety and depressive disorders and categorization of generalized anxiety disorder. Archives of General Psychiatry, 67, 47–57.CrossRefGoogle ScholarPubMed
Bergdahl, J., & Bergdahl, M. (2002). Perceived stress in adults: Prevalence and association of depression, anxiety and medication in a Swedish population. Stress and Health: Journal of the International Society for the Investigation of Stress, 18, 235–241.CrossRefGoogle Scholar
Berntson, G. G., Cacioppo, J. T., & Quigley, K. S. (1993). Respiratory sinus arrhythmia: Autonomic origins, physiological mechanisms, and psychophysiological implications. Psychophysiology, 30, 183–196.CrossRefGoogle ScholarPubMed
Berntson, G. G., Norman, G. J., Hawkley, L. C., & Cacioppo, J. T. (2008). Cardiac autonomic balance versus cardiac regulatory capacity. Psychophysiology, 45, 643–652.CrossRefGoogle ScholarPubMed
Blakemore, S. J. (2008). The social brain in adolescence. Nature Reviews Neuroscience, 9, 267.CrossRefGoogle ScholarPubMed
Brosschot, J. F., Pieper, S., & Thayer, J. F. (2005). Expanding stress theory: Prolonged activation and perseverative cognition. Psychoneuroendocrinology, 30, 1043–1049.CrossRefGoogle ScholarPubMed
Brougham, R. R., Zail, C. M., Mendoza, C. M., & Miller, J. R. (2009). Stress, sex differences, and coping strategies among college students. Current Psychology, 28, 85–97.CrossRefGoogle Scholar
Caballo, V. E., Salazar, I. C., Irurtia, M. J., Arias, B., Hofmann, S. G., & CISO-A Research Team. (2008). Social anxiety in 18 nations: Sex and age differences. Behavioral Psychology/Psicología Conductual, 16, 163–187.Google Scholar
Colich, N. L., Williams, E. S., Ho, T. C., King, L. S., Humphreys, K. L., Price, A. N., … Gotlib, I. H. (2017). The association between early life stress and prefrontal cortex activation during implicit emotion regulation is moderated by sex in early adolescence. Development and Psychopathology, 29, 1851–1864.CrossRefGoogle ScholarPubMed
Crişan, L. G., Vulturar, R., Miclea, M., & Miu, A. C. (2016). Reactivity to social stress in subclinical social anxiety: Emotional experience, cognitive appraisals, behavior, and physiology. Frontiers in Psychiatry, 7, 5.CrossRefGoogle Scholar
Critchley, H., & Nagai, Y. (2013). Electrodermal activity (EDA). Encyclopedia of Behavioral Medicine, 78, 666–669.Google Scholar
Dorn, L. D., Dahl, R. E., Woodward, H. R., & Biro, F. (2006). Defining the boundaries of early adolescence: A user's guide to assessing pubertal status and pubertal timing in research with adolescents. Applied Developmental Science, 10, 30–56.CrossRefGoogle Scholar
Ellis, B. J., Boyce, W. T., Belsky, J., Bakermans-Kranenburg, M. J., & Van IJzendoorn, M. H. (2011). Differential susceptibility to the environment: An evolutionary–neurodevelopmental theory. Development and Psychopathology, 23, 7–28.CrossRefGoogle Scholar
Farmer, A. S., & Kashdan, T. B. (2015). Stress sensitivity and stress generation in social anxiety disorder: A temporal process approach. Journal of Abnormal Psychology, 124, 102.CrossRefGoogle ScholarPubMed
Goldin, P. R., & Gross, J. J. (2010). Effects of mindfulness-based stress reduction (MBSR) on emotion regulation in social anxiety disorder. Emotion, 10, 83.CrossRefGoogle ScholarPubMed
Green, J. G., McLaughlin, K. A., Berglund, P. A., Gruber, M. J., Sampson, N. A., Zaslavsky, A. M., & Kessler, R. C. (2010). Childhood adversities and adult psychiatric disorders in the national comorbidity survey replication I: Associations with first onset of DSM-IV disorders. Archives of General Psychiatry, 67, 113–123.CrossRefGoogle ScholarPubMed
Hamilton, J. L., Stange, J. P., Abramson, L. Y., & Alloy, L. B. (2015). Stress and the development of cognitive vulnerabilities to depression explain sex differences in depressive symptoms during adolescence. Clinical Psychological Science, 3, 702–714.CrossRefGoogle ScholarPubMed
Hammen, C. (2015). Stress sensitivity in psychopathology: Mechanisms and consequences. Journal of Abnormal Psychology, 124, 152.CrossRefGoogle ScholarPubMed
Ho, T. C., King, L. S., Leong, J. K., Colich, N. L., Humphreys, K. L., Ordaz, S. J., & Gotlib, I. H. (2017). Effects of sensitivity to life stress on uncinate fasciculus segments in early adolescence. Social Cognitive and Affective Neuroscience, 12, 1460–1469.CrossRefGoogle ScholarPubMed
Kahle, S., Miller, J. G., Helm, J. L., & Hastings, P. D. (2018). Linking autonomic physiology and emotion regulation in preschoolers: The role of reactivity and recovery. Developmental Psychobiology, 60, 775–788.CrossRefGoogle ScholarPubMed
Kahle, S., Miller, J. G., Lopez, M., & Hastings, P. D. (2016). Sympathetic recovery from anger is associated with emotion regulation. Journal of Experimental Child Psychology, 142, 359–371.CrossRefGoogle ScholarPubMed
Kessler, R. C., McLaughlin, K. A., Green, J. G., Gruber, M. J., Sampson, N. A., Zaslavsky, A. M., … Benjet, C. (2010). Childhood adversities and adult psychopathology in the WHO World Mental Health Surveys. The British Journal of Psychiatry, 197, 378–385.CrossRefGoogle ScholarPubMed
Kilford, E. J., Garrett, E., & Blakemore, S. J. (2016). The development of social cognition in adolescence: An integrated perspective. Neuroscience & Biobehavioral Reviews, 70, 106–120.CrossRefGoogle Scholar
King, L. S., Colich, N. L., LeMoult, J., Humphreys, K. L., Ordaz, S. J., Price, A. N., & Gotlib, I. H. (2017). The impact of the severity of early life stress on diurnal cortisol: The role of puberty. Psychoneuroendocrinology, 77, 68–74.CrossRefGoogle ScholarPubMed
Kircanski, K., Waugh, C. E., Camacho, M. C., & Gotlib, I. H. (2016). Aberrant parasympathetic stress responsivity in pure and co-occurring major depressive disorder and generalized anxiety disorder. Journal of Psychopathology and Behavioral Assessment, 38, 5–19.CrossRefGoogle Scholar
Kirschbaum, C., Pirke, K. M., & Hellhammer, D. H. (1993). The ‘Trier Social Stress Test’–a tool for investigating psychobiological stress responses in a laboratory setting. Neuropsychobiology, 28, 76–81.CrossRefGoogle Scholar
Kudielka, B. M., Buske-Kirschbaum, A., Hellhammer, D. H., & Kirschbaum, C. (2004). HPA axis responses to laboratory psychosocial stress in healthy elderly adults, younger adults, and children: Impact of age and gender. Psychoneuroendocrinology, 29, 83–98.CrossRefGoogle ScholarPubMed
Kudielka, B. M., & Kirschbaum, C. (2005). Sex differences in HPA axis responses to stress: A review. Biological Psychology, 69, 113–132.CrossRefGoogle ScholarPubMed
LeMoult, J., Humphreys, K. L., Tracy, A., Hoffmeister, J. A., Ip, E., & Gotlib, I. H. (2019). Meta-analysis: Exposure to early life stress and risk for depression in childhood and adolescence. Journal of the American Academy of Child & Adolescent Psychiatry, 59, 842–855.CrossRefGoogle ScholarPubMed
March, J. S., Parker, J. D., Sullivan, K., Stallings, P., & Conners, C. K. (1997). The Multidimensional Anxiety Scale for Children (MASC): Factor structure, reliability, and validity. Journal of the American Academy of Child & Adolescent Psychiatry, 36, 554–565.CrossRefGoogle ScholarPubMed
March, J. S., Sullivan, K., & Parker, J. (1999). Test-retest reliability of the Multidimensional Anxiety Scale for Children. Journal of Anxiety Disorders, 13, 349–358.CrossRefGoogle ScholarPubMed
Marshall, W. A., & Tanner, J. M. (1968). Growth and physiological development during adolescence. Annual Review of Medicine, 19, 283–300.CrossRefGoogle ScholarPubMed
Marshall, W. A., & Tanner, J. M. (1970). Variations in the pattern of pubertal changes in boys. Archives of Disease in Childhood, 45, 13–23.CrossRefGoogle ScholarPubMed
McLaughlin, K. A., Conron, K. J., Koenen, K. C., & Gilman, S. E. (2010a). Childhood adversity, adult stressful life events, and risk of past-year psychiatric disorder: A test of the stress sensitization hypothesis in a population-based sample of adults. Psychological Medicine, 40, 1647–1658.CrossRefGoogle Scholar
McLaughlin, K. A., Green, J. G., Gruber, M. J., Sampson, N. A., Zaslavsky, A. M., & Kessler, R. C. (2010b). Childhood adversities and adult psychiatric disorders in the national comorbidity survey replication II: Associations with persistence of DSM-IV disorders. Archives of General Psychiatry, 67, 124–132.CrossRefGoogle Scholar
McLaughlin, K. A., Sheridan, M. A., & Nelson, C. A. (2017). Neglect as a violation of species-expectant experience: Neurodevelopmental consequences. Biological Psychiatry, 82, 462–471.CrossRefGoogle ScholarPubMed
Merikangas, K. R., He, J. P., Burstein, M., Swanson, S. A., Avenevoli, S., Cui, L., … Swendsen, J. (2010). Lifetime prevalence of mental disorders in US adolescents: Results from the National Comorbidity Survey Replication–Adolescent Supplement (NCS-A). Journal of the American Academy of Child & Adolescent Psychiatry, 49, 980–989.CrossRefGoogle Scholar
Mezzacappa, E. S., Kelsey, R. M., Katkin, E. S., & Sloan, R. P. (2001). Vagal rebound and recovery from psychological stress. Psychosomatic Medicine, 63, 650–657.CrossRefGoogle ScholarPubMed
Miller, J. G., Chocol, C., Nuselovici, J. N., Utendale, W. T., Simard, M., & Hastings, P. D. (2013). Children's dynamic RSA change during anger and its relations with parenting, temperament, and control of aggression. Biological Psychology, 92, 417–425.CrossRefGoogle ScholarPubMed
Miller, J. G., Gillette, J. S., Manczak, E. M., Kircanski, K., & Gotlib, I. H. (2019). Fine particle air pollution and physiological reactivity to social stress in adolescence: The moderating role of anxiety and depression. Psychosomatic Medicine, 81, 641–648.CrossRefGoogle ScholarPubMed
Morris, N. M., & Udry, J. R. (1980). Validation of a self-administered instrument to assess stage of adolescent development. Journal of Youth and Adolescence, 9, 271–280.CrossRefGoogle ScholarPubMed
Nelemans, S. A., Hale, W. W. III, Branje, S. J., van Lier, P. A. C., Koot, H. M., & Meeus, W. H. J. (2017). The role of stress reactivity in the long-term persistence of adolescent social anxiety symptoms. Biological Psychology, 125, 91–104.CrossRefGoogle ScholarPubMed
Ordaz, S., & Luna, B. (2012). Sex differences in physiological reactivity to acute psychosocial stress in adolescence. Psychoneuroendocrinology, 37, 1135–1157.CrossRefGoogle ScholarPubMed
Perugini, M., Gallucci, M., & Costantini, G. (2018). A practical primer to power analysis for simple experimental designs. International Review of Social Psychology, 31, 20.CrossRefGoogle Scholar
Porges, S. W. (2007). The polyvagal perspective. Biological Psychology, 74, 116–143.CrossRefGoogle ScholarPubMed
Ribbe, D. (1996). Psychometric review of Traumatic Event Screening Instrument for Children (TESI-C). In B.H. Stamm (Ed.), Measurement of stress, trauma, and adaptation (pp. 386–387). Lutherville, MD: Sidran Press.Google Scholar
Rudolph, K. D., Hammen, C., Burge, D., Lindberg, N., Herzberg, D., & Daley, S. E. (2000). Toward an interpersonal life-stress model of depression: The developmental context of stress generation. Developmental Psychopathology, 12, 215–234.CrossRefGoogle ScholarPubMed
Scott, K. M., McLaughlin, K. A., Smith, D. A., & Ellis, P. M. (2012). Childhood maltreatment and DSM-IV adult mental disorders: Comparison of prospective and retrospective findings. The British Journal of Psychiatry, 200, 469–475.CrossRefGoogle ScholarPubMed
Shirtcliff, E. A., Dahl, R. E., & Pollak, S. D. (2009). Pubertal development: Correspondence between hormonal and physical development. Child Development, 80, 327–337.CrossRefGoogle ScholarPubMed
Spear, L. P. (2009). Heightened stress responsivity and emotional reactivity during pubertal maturation: Implications for psychopathology. Development and Psychopathology, 21, 87–97.CrossRefGoogle ScholarPubMed
Stein, M. B. (2006). An epidemiologic perspective on social anxiety disorder. The Journal of Clinical Psychiatry, 67, 3–8.Google ScholarPubMed
Stein, M. B., Fuetsch, M., Müller, N., Höfler, M., Lieb, R., & Wittchen, H. U. (2001). Social anxiety disorder and the risk of depression: A prospective community study of adolescents and young adults. Archives of General Psychiatry, 58, 251–256.CrossRefGoogle ScholarPubMed
Swain, J., Hancock, K., Dixon, A., Koo, S., & Bowman, J. (2013). Acceptance and commitment therapy for anxious children and adolescents: Study protocol for a randomized controlled trial. Trials, 14, 140.CrossRefGoogle ScholarPubMed
Tofighi, D., & MacKinnon, D. P. (2011). RMediation: An R package for mediation analysis confidence intervals. Behavior Research Methods, 43, 692–700.CrossRefGoogle Scholar
Van Roy, B., Kristensen, H., Groholt, B., & Clench-Aas, J. (2009). Prevalence and characteristics of significant social anxiety in children aged 8–13 years. Social Psychiatry and Psychiatric Epidemiology, 44, 407–415.CrossRefGoogle ScholarPubMed
Wilhelm, F. H., & Peyk, P. (2005). ANSLab: Autonomic nervous system laboratory (Version 2.4) (Computer software). Retrieved from the SPR Software Repository: http://www.sprweb.org.+.Google Scholar