Abstract
Early behavioral inhibition (BI) is a known risk factor for later anxiety disorder. Variability in children’s parasympathetic nervous system (PNS) functioning may provide insight into the substantial heterogeneity in anxiety outcomes for children high in BI. However, gaps persist due to an over-reliance on static measures of functioning, which limits our ability to leverage PNS functioning to identify risk for anxiety. We address these gaps using baseline data from an early intervention study of inhibited preschoolers by characterizing vagal flexibility (VF), an index of non-linear change in PNS functioning, across social stressor tasks and by examining the associations between VF and anxiety. One hundred and fifty-one parents and their 3.5- to 5-year-old children were selected on the basis of BI to participate in an early intervention program (ClinicalTrials.gov registration: NCT02308826). A structural equation modeling framework was used to model children’s VF across tasks designed to mimic exposure to novel social interactions and to test the predictive links between VF and anxiety. Children who showed less VF, characterized by less suppression and flatter recovery, were rated by both parents and clinicians as more anxious. Moreover, a multiple group model showed that children meeting diagnostic criteria for social anxiety disorder demonstrated significantly less VF across social stressor tasks. Among inhibited youth, reduced VF is a risk factor for anxiety and may reflect an individual’s reduced capacity to actively cope with external demands. Study results contribute to our understanding of the regulatory processes underlying risk for anxiety in early childhood.
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References
Achenbach, T. M. (1991). Manual for the child behavior checklist/ 4–18 and 1991 profile. Burlington VT.
Asher, M., Asnaani, A., & Aderka, I. M. (2017). Gender differences in social anxiety disorder: A review. Clinical Psychology Review, 56, 1–12.
Beauchaine, T. (2001). Vagal tone, development, and Gray’s motivational theory: toward an integrated model of autonomic nervous system functioning in psychopathology. Development and Psychopathology, 13, 183–214. https://doi.org/10.1017/S0954579401002012
Beauchaine, T. P. (2012). Physiological markers of emotional and behavioral dysregulation in externalizing psychopathology. Monographs of the Society for Research in Child Development, 77(2), 79–86. https://doi.org/10.1111/j.1540-5834.2011.00665.x
Beauchaine, T. P. (2015). Respiratory sinus arrhythmia: A transdiagnostic biomarker of emotion dysregulation and psychopathology. Current opinion in Psychology, 3, 43–47.
Beauchaine, T. P., Bell, Z., Knapton, E., McDonough-Caplan, H., Shader, T., & Zisner, A. (2019). Respiratory sinus arrhythmia reactivity across empirically based structural dimensions of psychopathology: a meta-analysis. Psychophysiology, 56(5), e13329. https://doi.org/10.1111/psyp.13329
Beauchaine, T. P., & Hinshaw, S. P. (2020). RDoC and psychopathology among youth: misplaced assumptions and an agenda for future research. Journal of Clinical Child & Adolescent Psychology, 49(3), 322–340. https://doi.org/10.1080/15374416.2020.1750022
Bentler, P. M. (1990). Comparative fit indexes in structural models. Psychological Bulletin, 107(2), 238.
Bertalanffy, L. V. (1972). The history and statm of general systems theory. Academy of Management Journal, 15, 407–426.
Bishop, G., Spence, S. H., & McDonald, C. (2003). Can Parents and Teachers Provide a Reliable and Valid Report of Behavioral Inhibition? Child Development, 74, 1899–1917. https://doi.org/10.1046/j.1467-8624.2003.00645.x
Bornas, X., Balle, M., De la Torre-Luque, A., Fiol-Veny, A., & Llabrés, J. (2015). Ecological assessment of heart rate complexity: differences between high- and low-anxious adolescents. International Journal of Psychophysiology, 98(1), 112–118. https://doi.org/10.1016/j.ijpsycho.2015.07.007
Brooker, R. J., & Buss, K. A. (2010). Dynamic measures of RSA predict distress and regulation in toddlers. Developmental Psychobiology, 52(4), 372–382. https://doi.org/10.1002/dev.20432
Brooker, R. J., Buss, K. A., Lemery-Chalfant, K., Aksan, N., Davidson, R. J., & Goldsmith, H. H. (2013). The development of stranger fear in infancy and toddlerhood: normative development, individual differences, antecedents, and outcomes. Developmental Science., 16, 864–878. https://doi.org/10.1111/desc.12058
Browne, M. W., & Cudeck, R. (1993). Alternative ways of assessing model fit. In K. A. Bollen, & J. S. Long (Eds.), Testing structural equation models (pp. 136–162). Newbury Park, CA: Sage.
Burt, K. B., & Obradović, J. (2013). The construct of psychophysiological reactivity: statistical and psychometric issues. Developmental Review, 33(1), 29–57. https://doi.org/10.1016/j.dr.2012.10.002
Buss, K. A., Davis, E. L., Kiel, E. J., Brooker, R. J., Beekman, C., & Early, M. C. (2013). Dysregulated fear predicts social wariness and social anxiety symptoms during kindergarten. Journal of Clinical Child and Adolescent Psychology, 42, 603–616. https://doi.org/10.1080/15374416.2013.769170
Buss, K. A., Davis, E. L., Ram, N., & Coccia, M. (2017). Dysregulated fear, social inhibition, and respiratory sinus arrhythmia: a replication and extension. Child Development, 00, 1–15. https://doi.org/10.1111/cdev.12774
Buss, K. A., Davis, E. L., Ram, N., & Coccia, M. (2018). Dysregulated fear, social inhibition, and respiratory sinus arrhythmia: a replication and extension. Child Development, 89(3), e214–e228. https://doi.org/10.1111/cdev.12774
Cacioppo, J. T., Tassinary, L. G., & Berntson, G. (2007). Handbook of psychophysiology. Cambridge University Press.
Carter, C. S., & Porges, S. W. (2013). The biochemistry of love: an oxytocin hypothesis. EMBO Reports, 14, 12–16. https://doi.org/10.1038/embor.2012.191
Chronis-Tuscano, A., Danko, C. M., Rubin, K. H., Coplan, R. J., Novick, R., & D. (2018). Future directions for research on early intervention for young children at risk for social anxiety. Journal of Clinical Child & Adolescent Psychology, 00, 1–13. https://doi.org/10.1080/15374416.2018.1426006
Chronis-Tuscano, A., Degnan, K. A., Pine, D. S., Perez-Edgar, K., Henderson, H. A., Diaz, Y., et al. (2009). Stable early maternal report of behavioral inhibition predicts lifetime social anxiety disorder in adolescence. Journal of the American Academy of Child and Adolescent Psychiatry, 48, 928–935. https://doi.org/10.1097/CHI.0b013e3181ae09df
Chronis-Tuscano, A., Novick, D. R., Danko, C. M., Smith, K. A., Wagner, N. J., Wang, C. H., et al. (2021). Early intervention for inhibited young children: a randomized controlled trial comparing the Turtle Program and Cool Little Kids. Journal of Child Psychology and Psychiatry, 63(3), 273–281. https://doi.org/10.1111/jcpp.13475
Cui, L., Morris, A. S., Harrist, A. W., Larzelere, R. E., Criss, M. M., & Houltberg, B. J. (2015). Adolescent RSA responses during an anger discussion task: relations to emotion regulation and adjustment. Emotion, 15(3), 360–372. https://doi.org/10.1037/emo0000040
Cui, L., Zhang, X., Houltberg, B. J., Criss, M. M., & Morris, A. S. (2019). RSA reactivity in response to viewing bullying film and adolescent social adjustment. Developmental Psychobiology, 61(4), 592–604. https://doi.org/10.1002/dev.21835
Darling, L. N., Holochwost, S. J., Coffman, J., Propper, C. B., & Wagner, N. J. (2022). Context is key: parasympathetic regulation in the classroom differentially predicts preschoolers’ socially competent behaviors. Developmental Psychobiology, 64(2), e22246. https://doi.org/10.1002/dev.22246
Eisenberg, J., Natella Ben-Daniel, M., & Mei-Tal, G. (2004). An autonomic nervous system biofeedback modality for the treatment of attention deficit hyperactivity. The Israel Journal of Psychiatry and Related Sciences, 41(1), 45–53.
Enders, C. K. (2001). A primer on maximum likelihood algorithms available for use with missing data. Structural Equation Modeling: A Multidisciplinary Journal, 8, 128–141. https://doi.org/10.1207/S15328007SEM0801
Eaves, L. C., Wingert, H. D., Ho, H. H., & Mickelson, E. C. (2006). Screening for autism spectrum disorders with the social communication questionnaire. Journal of Developmental & Behavioral Pediatrics, 27(2), S95–S103.
Fox, N., Henderson, H. A., & Rubin, K. H. (2001). Continuity and discontinuity of behavioral inhibition and exuberance: psychophysiological and behavioral influences across the first four years of life. Child Development, 72(1), 1–21.
Fox, N. A., Buzzell, G. A., Morales, S., Valadez, E. A., Wilson, M., & Henderson, H. A. (2021). Understanding the emergence of social anxiety in children with behavioral inhibition. Biological Psychiatry, 89(7), 681–689. https://doi.org/10.1016/j.biopsych.2020.10.004
Fox, N. A., Henderson, H. A., Marshall, P. J., Nichols, K. E., & Ghera, M. M. (2005). Behavioral inhibition: linking biology and behavior within a developmental framework. Annual Review of Psychology, 56, 235–262. https://doi.org/10.1146/annurev.psych.55.090902.141532
Friedman, B. H. (2007). An autonomic flexibility–neurovisceral integration model of anxiety and cardiac vagal tone. Biological Psychology, 74(2), 185–199.
Friedman, B. H., & Thayer, J. F. (1998). Anxiety and autonomic flexibility: a cardiovascular approach. Biological Psychology, 47(3), 243–263.
Ginsburg, G. S., Drake, K. L., Tein, J. Y., Teetsel, R., & Riddle, M. A. (2015). Preventing onset of anxiety disorders in offspring of anxious parents: a randomized controlled trial of a family-based intervention. American Journal of Psychiatry, 172(12), 1207–1214.
Granic, I. (2014). The role of anxiety in the development, maintenance, and treatment of childhood aggression. Development and Psychopathology, 26, 1515–1530. https://doi.org/10.1017/S0954579414001175
Greaves-Lord, K., Tulen, J., Dietrich, A., Sondeijker, F., van Roon, A., Oldehinkel, A., et al. (2010). Reduced autonomic flexibility as a predictor for future anxiety in girls from the general population: the TRAILS study. Psychiatry Research, 179(2), 187–193. https://doi.org/10.1016/j.psychres.2009.04.014
Hastings, P. D., Kahle, S., Fleming, C., Lohr, M. J., Katz, L. F., & Oxford, M. L. (2019). An intervention that increases parental sensitivity in families referred to Child Protective Services also changes toddlers’ parasympathetic regulation. Developmental Science, 22(1), e12725. https://doi.org/10.1111/desc.12725
Hastings, P. D., Nuselovici, J. N., Utendale, W. T., Coutya, J., McShane, K. E., & Sullivan, C. (2008). Applying the polyvagal theory to children’s emotion regulation: social context, socialization, and adjustment. Biological Psychology, 79, 299–306. https://doi.org/10.1016/j.biopsycho.2008.07.005
Henderson, H. A., Marshall, P. J., Fox, N. A., & Rubin, K. H. (2004). Psychophysiological and behavioral evidence for varying forms and functions of nonsocial behavior in preschoolers. Child Development, 75, 251–263. https://doi.org/10.1111/j.1467-8624.2004.00667.x
Hinnant, J. B., & El-Sheikh, M. (2009). Children’s externalizing and internalizing symptoms over time: the role of individual differences in patterns of RSA responding. Journal of Abnormal Child Psychology, 37, 1049–1061. https://doi.org/10.1007/s10802-009-9341-1
Hu, L., & Bentler, P. M. (1998). Fit indices in covariance structure modeling: sensitivity to underparameterized model misspecification. Psychological Methods, 3, 424–453. https://doi.org/10.1037//1082-989X.3.4.424
Kagan, J., Reznick, J. S., & Gibbons, J. (1989). Inhibited and uninhibited types of children. Child Development, 60, 838–845.
Kagan, J., & Snidman, N. (1999). Early childhood predictors of adult anxiety disorders. Biological Psychiatry, 46(11), 1536–1541.
Kagan, J., Snidman, N., Kahn, V., Towsley, S., Steinberg, L., & Fox, N. A. (2007). The preservation of two infant temperaments into adolescence. Monographs of the Society for Research in Child Development, 72(2), i–95.
Kennedy, S. J., Rapee, R. M., & Edwards, S. L. (2009). A selective intervention program for inhibited preschool-aged children of parents with an anxiety disorder: Effects on current anxiety disorders and temperament. Journal of the American Academy of Child & Adolescent Psychiatry, 48(6), 602–609.
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(1–2), 76–81. https://doi.org/10.1159/000119004
Kotov, R., Krueger, R. F., Watson, D., Achenbach, T. M., Althoff, R. R., Bagby, R. M., et al. (2017). The Hierarchical Taxonomy of Psychopathology (HiTOP): a dimensional alternative to traditional nosologies. Journal of Abnormal Psychology, 126(4), 454–477. https://doi.org/10.1037/abn0000258
Kudielka, B. M., Hellhammer, D. H., & Kirschbaum, C. (2010). Ten years of research with the Trier Social Stress Test - revisited. In E. Harmon-Jones & P. Winkielman (Eds.), Social neuroscience: Integrating biological and psychological explanations for social behavior (pp. 56–83). Guilford.
Lewis, G. F., Furman, S. A., McCool, M. F., & Porges, S. W. (2012). Statistical strategies to quantify respiratory sinus arrhythmia: Are commonly used metrics equivalent? Biological Psychology, 89, 349–364. https://doi.org/10.1016/j.biopsycho.2011.11.009
Lo, Y., Mendell, N. R., & Rubin, D. B. (2001). Testing the number of components in a normal mixture. Biometrika, 88(3), 767–778.
LoBue, V., & Thrasher, C. (2014). The Child Affective Facial Expression (CAFE) set: validity and reliability from untrained adults. Frontiers in Psychology, 5, 1532. https://doi.org/10.3389/fpsyg.2014.01532
Mathewson, K. J., Schmidt, L. A., Miskovic, V., Santesso, D. L., Duku, E., McCabe, R. E., et al. (2013). Does respiratory sinus arrhythmia (RSA) predict anxiety reduction during cognitive behavioral therapy (CBT) for social anxiety disorder (SAD)? International Journal of Psychophysiology, 88(2), 171–181. https://doi.org/10.1016/j.ijpsycho.2013.03.016
Mendes, W. (2019). Emotion and the Autonomic Nervous System. In Handbook of Emotion (4th ed.). The Guilford Press.
Merikangas, K. R., He, J., Burstein, M., Swanson, S. A., Avenevoli, S., Cui, L., et al. (2010). Lifetime prevalence of mental disorders in U.S. adolescents: results from the national comorbidity survey replication– adolescent supplement (NCS-A). Adolescent Psychiatry, 49(10), 10.
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. https://doi.org/10.1016/j.biopsycho.2012.12.005
Miller, J. G., Kahle, S., & Hastings, P. D. (2016). Moderate baseline vagal tone predicts greater prosociality in children. Developmental Psychology, 53, 274–289. https://doi.org/10.1037/dev0000238
Muhtadie, L., Akinola, M., Koslov, K., & Mendes, W. B. (2015). Vagal flexibility: a physiological predictor of social sensitivity. Journal of Personality and Social Psychology, 109(1), 106–120. https://doi.org/10.1037/pspp0000016
Muthén, L. K., & Muthen, B. (2017). Mplus user’s guide: statistical analysis with latent variables, user’s guide. Muthén & Muthén.
Paniccia, M., Paniccia, D., Thomas, S., Taha, T., & Reed, N. (2017). Clinical and non-clinical depression and anxiety in young people: A scoping review on heart rate variability. Autonomic Neuroscience, 208, 1–14. https://doi.org/10.1016/j.autneu.2017.08.008
Porges, S. W. (1992). Vagal tone: a physiologic marker of stress vulnerability. Pediatrics, 90, 498–504.
Porges, S. W. (2007). A phylogenetic journey through the vague and ambiguous Xth cranial nerve: a commentary on contemporary heart rate variability research. Biological Psychology, 74(2), 301–307. https://doi.org/10.1016/j.biopsycho.2006.08.007
Porges, S. W. (2009). The polyvagal theory: new insights into adaptive reactions of the autonomic nervous system. Cleveland Clinic Journal of Medicine, 76, S86. https://doi.org/10.3949/ccjm.76.s2.17
Porges, S. W. (1985). Method and apparatus for evaluating rhythmic oscillations in aperiodic physiological response systems. Washington DC: U.S. Patent Office. Patent Number: 4,510,944.
Porges, S. W., & Bohrer, R. E. (1990). The analysis of periodic processes in psychophysiological research. Principles of psychophysiology: Physical, social, and inferential elements (pp. 708–753). Cambridge University Press.
Porges, S. W., & Byrne, E. A. (1992). Research methods for measurement of heart rate and respiration. Biological psychology, 34(2–3), 93–130.
Ramsawh, H. J., Weisberg, R. B., Dyck, I., Stout, R., & Keller, M. B. (2011). Age of onset, clinical characteristics, and 15-year course of anxiety disorders in a prospective, longitudinal, observational study. Journal of Affective Disorders, 132(1–2), 260–264.
Rubin, K. H., & Chronis-Tuscano, A. (2021). Perspectives on social withdrawal in childhood: past, present, and prospects. Child Development Perspectives, 15(3), 160–167. https://doi.org/10.1111/cdep.12417
Rubin, K. H., Coplan, R. J., & Bowker, J. C. (2009). Social withdrawal in childhood. Annual Review of Psychology, 60(1), 141–171. https://doi.org/10.1146/annurev.psych.60.110707.163642
Schmitz, J., Krämer, M., Tuschen-Caffier, B., Heinrichs, N., & Blechert, J. (2011). Restricted autonomic flexibility in children with social phobia: autonomic nervous system in children. Journal of Child Psychology and Psychiatry, 52(11), 1203–1211. https://doi.org/10.1111/j.1469-7610.2011.02417.x
Silverman, W. K., & Albano, A. M. (1996). The anxiety disorders interview schedule for DSM–IV—child and parent versions. San Antonio, TX: Physiological Corporation.
Smith, K. A., Hastings, P. D., Henderson, H. A., & Rubin, K. H. (2019). Multidimensional emotion regulation moderates the relation between behavioral inhibition at age 2 and social reticence with unfamiliar peers at age 4. Journal of Abnormal Child Psychology, 47(7), 1239–1251. https://doi.org/10.1007/s10802-018-00509-y
Towe-Goodman, N. R., Franz, L., Copeland, W., Angold, A., & Egger, H. (2014). Perceived family impact of preschool anxiety disorders. Journal of the American Academy of Child & Adolescent Psychiatry, 53(4), 437–446. https://doi.org/10.1016/j.jaac.2013.12.017
Ugarte, E., Liu, S., & Hastings, P. D. (2021a). Parasympathetic activity, emotion socialization, and internalizing and externalizing problems in children: longitudinal associations between and within families. Developmental Psychology, 57(9), 1525–1539. https://doi.org/10.1037/dev0001039
Ugarte, E., Miller, J. G., Weissman, D. G., & Hastings, P. D. (2021b). Vagal flexibility to negative emotions moderates the relations between environmental risk and adjustment problems in childhood. Development and Psychopathology, 1–18. https://doi.org/10.1017/S0954579421000912
Viana, A. G., Palmer, C. A., Zvolensky, M. J., Alfano, C. A., Dixon, L. J., & Raines, E. M. (2017). Children’s behavioral inhibition and anxiety disorder symptom severity: the role of individual differences in respiratory sinus arrhythmia. Behaviour Research and Therapy, 93, 38–46. https://doi.org/10.1016/j.brat.2017.03.012
Viana, A. G., Trent, E. S., Raines, E. M., Woodward, E. C., Storch, E. A., & Zvolensky, M. J. (2021). Childhood anxiety sensitivity, fear downregulation, and anxious behaviors: vagal suppression as a moderator of risk. Emotion, 21(2), 430–441. https://doi.org/10.1037/emo0000713
Wagner, N. J., Holochwost, S., Lynch, S., Mills-Koonce, R., & Propper, C. (2021). Characterizing change in vagal tone during the first three years of life: a systematic review and empirical examination across two longitudinal samples. Neuroscience & Biobehavioral Reviews, 129, 282–295. https://doi.org/10.1016/j.neubiorev.2021.07.025
Wagner, N. J., Propper, C., Gueron-Sela, N., & Mills-Koonce, W. R. (2015). Dimensions of maternal parenting and infants’ autonomic functioning interactively predict early internalizing behavior problems. Journal of Abnormal Child Psychology. https://doi.org/10.1007/s10802-015-0039-2
Wagner, N. J., & Waller, R. (2020). Leveraging parasympathetic nervous system activity to study risk for psychopathology: the special case of callous-unemotional traits. Neuroscience & Biobehavioral Reviews, 118, 175–185.
Waldman, I., King, C., Poore, H., Luningham, J., Zinbarg, R., Krueger, R., et al. (2022, October 20). Recommendations for adjudicating among alternative structural models of psychopathology. PsyArXiv. https://doi.org/10.31234/osf.io/bksm7
West, K. B., Shaffer, A., Wickrama, Kandauda, A. S., Han, Z. R., & Suveg, C. (2020). Preschoolers’ dynamic respiratory sinus arrhythmia (RSA) change during a challenging parent-child interactive task: relations with preschoolers’ socioemotional health. Developmental Psychobiology, 63(5), 1132–1145. https://doi.org/10.1002/dev.22054
Yaroslavsky, I., Rottenberg, J., & Kovacs, M. (2014). Atypical patterns of respiratory sinus arrhythmia index an endophenotype for depression. Development and Psychopathology, 26, 1337–1352. https://doi.org/10.1017/S0954579414001060
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This project was funded by NIH R01MH103253 awarded to A.C-T. and K.H.R. Manuscript preparation was partially supported by NIH R03MH123762 awarded to N.J.W.
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Wagner, N.J., Shakiba, N., Bui, H.N. et al. Examining the Relations Between Children’s Vagal Flexibility Across Social Stressor Tasks and Parent- and Clinician-Rated Anxiety Using Baseline Data from an Early Intervention for Inhibited Preschoolers. Res Child Adolesc Psychopathol 51, 1213–1224 (2023). https://doi.org/10.1007/s10802-023-01050-3
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DOI: https://doi.org/10.1007/s10802-023-01050-3