Journal of Abnormal Child Psychology

, Volume 47, Issue 8, pp 1367–1377 | Cite as

The Relation between Specific Parenting Behaviors and Toddlers’ Early Anxious Behaviors is Moderated by Toddler Cortisol Reactivity

  • Anne E. KalomirisEmail author
  • Randi A. Phelps
  • Elizabeth J. Kiel


Differential susceptibility theory posits that neurobiological reactivity (e.g., cortisol levels) should be considered as an individual index of susceptibility to both positive and negative environments. The current investigation separately examines cortisol reactivity and total concentration in toddlerhood as moderators of the longitudinal relation between maternal protection and encouragement of independence and increases or decreases in observed anxious behaviors, respectively. A total of 119 mother-toddler dyads participated in a laboratory visit when toddlers were 12- to 18-months-old. Mothers reported on their parenting behaviors and toddlers participated in a novelty episode from which their anxious behaviors were coded. Toddlers provided three saliva samples, yielding measures of cortisol reactivity and total cortisol concentration. One year later, dyads returned to the laboratory where toddlers participated in another novelty episode to observationally assess anxious behaviors. Results revealed that maternal protection tended to relate to greater increases in anxious behaviors one year later only for toddlers who displayed high cortisol reactivity. Cortisol reactivity also moderated the relation between maternal encouragement of independence and change in toddler anxious behaviors, with this parenting behavior relating to greater decreases in anxious behaviors only for toddlers with high cortisol reactivity. Results examining total cortisol concentration as a moderator were not significant. Results suggest the importance of considering toddler cortisol reactivity a context of susceptibility when examining the longitudinal relation between parenting behaviors and the development of anxious behaviors in toddlerhood.


Anxiety risk Parenting Cortisol Toddlers Differential susceptibility 



We express our appreciation to the staff of the Behavior, Emotions, and Relationship laboratory that assisted with data collection and coding, and the families and toddlers who participated in this project.


The project from which these data were derived was supported by a grant from the National Institute for Child Health and Human Development (R15 HD076158).

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no 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.


  1. Aiken, L. S., & West, S. G. (1991). Multiple regression testing and interpreting interactions. Newbury Park, CA: Sage.Google Scholar
  2. Ainsworth, M. D. S., & Bell, S. M. (1970). Attachment, exploration, and separation: Illustrated by the behavior of one-year-olds in a strange situation. Child Development, 41, 49–67.PubMedCrossRefGoogle Scholar
  3. Badanes, L. S., Watamura, S. E., & Hankin, B. L. (2011). Hypocortisolism as a potential marker of allostatic load in children: Associations with family risk and internalizing disorders. Development and Psychopathology, 23(3), 881–896.PubMedPubMedCentralCrossRefGoogle Scholar
  4. Barrios, C. S., Bufferd, S. J., Klein, D. N., & Dougherty, L. R. (2017). The interaction between parenting and children's cortisol reactivity at age 3 predicts increases in children's internalizing and externalizing symptoms at age 6. Development and Psychopathology, 29(4), 1319–1331.PubMedPubMedCentralCrossRefGoogle Scholar
  5. Bayer, J. K., Sanson, A. V., & Hemphill, S. A. (2006). Parent influences on early childhood internalizing difficulties. Journal of Applied Developmental Psychology, 27(6), 542–559.CrossRefGoogle Scholar
  6. Bayer, J. K., Ukoumunne, O. C., Mathers, M., Wake, M., Abdi, N., & Hiscock, H. (2012). Development of children’s internalising and externalising problems from infancy to five years of age. The Australian and New Zealand Journal of Psychiatry, 46(7), 659–668.PubMedCrossRefGoogle Scholar
  7. Belsky, J., & Pluess, M. (2009). Beyond diathesis stress: Differential susceptibility to environmental influences. Psychological Bulletin, 135(6), 885–908.PubMedCrossRefGoogle Scholar
  8. Belsky, J., Bakermans-Kranenburg, M. J., & van IJzendoorn, M. H. (2007). For better and for worse: Differential susceptibility to environmental influences. Current Directions in Psychological Science, 16(6), 300–304.CrossRefGoogle Scholar
  9. Bittner, A., Egger, H. L., Erkanli, A., Costello, E. J., Foley, D. L., & Angold, A. (2007). What do childhood anxiety disorders predict? Journal of Child Psychology and Psychiatry, 48(12), 1174–1183.PubMedCrossRefGoogle Scholar
  10. Blair, C., Granger, D. A., Kivlighan, K. T., Mills-Koonce, R., Willoughby, M., Greenberg, M. T., et al. (2008). Maternal and child contributions to cortisol response to emotional arousal in young children from low income, rural communities. Developmental Psychology, 44(4), 1095–1109.PubMedCrossRefGoogle Scholar
  11. Bögels, S., & Phares, V. (2008). Fathers' role in the etiology, prevention and treatment of child anxiety: A review and new model. Clinical Psychology Review, 28(4), 539–558.PubMedCrossRefGoogle Scholar
  12. Bosquet, M., & Egeland, B. (2006). The development and maintenance of anxiety symptoms from infancy through adolescence in a longitudinal sample. Development and Psychopathology, 18(2), 517–550.PubMedCrossRefGoogle Scholar
  13. Boyce, W. T., & Ellis, B. J. (2005). Biological sensitivity to context: I. An evolutionary–developmental theory of the origins and functions of stress reactivity. Development and Psychopathology, 17(2), 271–301.PubMedCrossRefGoogle Scholar
  14. Buss, K. A. (2011). Which fearful toddlers should we worry about? Context, fear regulation, and anxiety risk. Developmental Psychology, 47(3), 804–819.PubMedPubMedCentralCrossRefGoogle Scholar
  15. Buss, K. A., & Goldsmith, H. H. (2000). Manual and normative data for the laboratory temperament assessment battery—Toddler version. In University of Wisconsin. Madison: Psychology Department Technical Report.Google Scholar
  16. Calkins, S. D., Propper, C., & Mills-Koonce, W. R. (2013). A biopsychosocial perspective on parenting and developmental psychopathology. Development and Psychopathology, 25(4pt2), 1399–1414.PubMedCrossRefGoogle Scholar
  17. Chen, X., Hastings, P. D., Rubin, K. H., Chen, H., Cen, G., & Stewart, S. L. (1998). Child-rearing attitudes and behavioral inhibition in Chinese and Canadian toddlers: A cross-cultural study. Developmental Psychology, 34(4), 677–686.PubMedCrossRefGoogle Scholar
  18. Chorpita, B. F., & Barlow, D. H. (1998). The development of anxiety: The role of control in the early environment. Psychological Bulletin, 124(1), 3–21.PubMedCrossRefGoogle Scholar
  19. Degnan, K. A., Almas, A. N., & Fox, N. A. (2010). Temperament and the environment in the etiology of childhood anxiety. Journal of Child Psychology and Psychiatry, 51(4), 497–517.PubMedCrossRefGoogle Scholar
  20. Deković, M., Janssens, J. M., & Gerris, J. R. (1991). Factor structure and construct validity of the Block child rearing practices report (CRPR). Psychological Assessment: A Journal of Consulting and Clinical Psychology, 3(2), 182–187.CrossRefGoogle Scholar
  21. Edwards, S. L., Rapee, R. M., & Kennedy, S. (2010). Prediction of anxiety symptoms in preschool-aged children: Examination of maternal and paternal perspectives. Journal of Child Psychology and Psychiatry, 51(3), 313–321.PubMedCrossRefGoogle Scholar
  22. 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(1), 7–28.PubMedCrossRefGoogle Scholar
  23. Enders, C. K. (2001). The performance of the full information maximum likelihood estimator in multiple regression models with missing data. Educational and Psychological Measurement, 61(5), 713–740.CrossRefGoogle Scholar
  24. Fox, N. A., Nichols, K. E., Henderson, H. A., Rubin, K., Schmidt, L., Hamer, D., Ernst, M., & Pine, D. S. (2005). Evidence for a gene-environment interaction in predicting behavioral inhibition in middle childhood. Psychological Science, 16(12), 921–926.PubMedCrossRefGoogle Scholar
  25. Grabell, A. S., Olson, S. L., Miller, A. L., Kessler, D. A., Felt, B., Kaciroti, N., Wang, L., & Tardif, T. (2015). The impact of culture on physiological processes of emotion regulation: A comparison of US and Chinese preschoolers. Developmental Science, 18(3), 420–435.PubMedCrossRefGoogle Scholar
  26. Grover, R. L., Ginsburg, G. S., & Ialongo, N. (2007). Psychosocial outcomes of anxious first graders: A seven-year follow-up. Depression and Anxiety, 24(6), 410–420.PubMedPubMedCentralCrossRefGoogle Scholar
  27. Gunnar, M. R. (2001). The role of glucocorticoids in anxiety disorders: A critical analysis. In M. V. Vasey & M. R. Dadds (Eds.), The developmental psychopathology of anxiety (pp. 143–159). New York: Oxford University Press.CrossRefGoogle Scholar
  28. Gunnar, M., & Quevedo, K. (2007). The neurobiology of stress and development. Annual Review of Psychology, 58, 145–173.PubMedCrossRefGoogle Scholar
  29. Hagan, M. J., Roubinov, D. S., Mistler, A. K., & Luecken, L. J. (2014). Mental health outcomes in emerging adults exposed to childhood maltreatment: The moderating role of stress reactivity. Child Maltreatment, 19(3–4), 156–167.PubMedCrossRefGoogle Scholar
  30. Hane, A. A., Cheah, C., Rubin, K. H., & Fox, N. A. (2008). The role of maternal behavior in the relation between shyness and social reticence in early childhood and social withdrawal in middle childhood. Social Development, 17(4), 795–811.CrossRefGoogle Scholar
  31. Hastings, P. D., & Rubin, K. H. (1999). Predicting mothers' beliefs about preschool-aged children's social behavior: Evidence for maternal attitudes moderating child effects. Child Development, 70(3), 722–741.PubMedCrossRefGoogle Scholar
  32. Kagan, J., Reznick, J. S., Clarke, C., Snidman, N., & Garcia-Coll, C. (1984). Behavioral inhibition to the unfamiliar. Child Development, 55(6), 2212–2225.CrossRefGoogle Scholar
  33. Kiel, E. J., Premo, J. E., & Buss, K. A. (2016). Maternal encouragement to approach novelty: A curvilinear relation to change in anxiety for inhibited toddlers. Journal of Abnormal Child Psychology, 44(3), 433–444.PubMedPubMedCentralCrossRefGoogle Scholar
  34. Kopala-Sibley, D. C., Dougherty, L. R., Dyson, M. W., Laptook, R. S., Olino, T. M., Bufferd, S. J., & Klein, D. N. (2017). Early childhood cortisol reactivity moderates the effects of parent–child relationship quality on the development of children's temperament in early childhood. Developmental Science, 20(3), e12378.CrossRefGoogle Scholar
  35. Kuhlman, K. R., Geiss, E. G., Vargas, I., & Lopez-Duran, N. (2018). HPA-axis activation as a key moderator of childhood trauma exposure and adolescent mental health. Journal of Abnormal Child Psychology, 46(1), 149–157.PubMedCrossRefGoogle Scholar
  36. Kushner, M. R., Barrios, C., Smith, V. C., & Dougherty, L. R. (2016). Physiological and behavioral vulnerability markers increase risk to early life stress in preschool-aged children. Journal of Abnormal Child Psychology, 44(5), 859–870.PubMedCrossRefGoogle Scholar
  37. Laurent, H. K., Leve, L. D., Neiderhiser, J. M., Natsuaki, M. N., Shaw, D. S., Fisher, P. A., Marceau, K., Harold, G. T., & Reiss, D. (2013). Effects of parental depressive symptoms on child adjustment moderated by hypothalamic pituitary adrenal activity: Within- and between-family risk. Child Development, 84(2), 528–542.PubMedCrossRefGoogle Scholar
  38. Laurin, J. C., Joussemet, M., Tremblay, R. E., & Boivin, M. (2015). Early forms of controlling parenting and the development of childhood anxiety. Journal of Child and Family Studies, 24(11), 3279–3292.CrossRefGoogle Scholar
  39. Lindhout, I. E., Markus, M. T., Hoogendijk, T. H., & Boer, F. (2009). Temperament and parental child-rearing style: Unique contributions to clinical anxiety disorders in childhood. European Child & Adolescent Psychiatry, 18(7), 439–446.CrossRefGoogle Scholar
  40. McLeod, B. D., Wood, J. J., & Weisz, J. R. (2007). Examining the association between parenting and childhood anxiety: A meta-analysis. Clinical Psychology Review, 27(2), 155–172.PubMedCrossRefGoogle Scholar
  41. Monroe, S. M., & Simons, A. D. (1991). Diathesis-stress theories in the context of life stress research: Implications for the depressive disorders. Psychological Bulletin, 110, 406–425.PubMedCrossRefGoogle Scholar
  42. Paschall, K. W., & Mastergeorge, A. M. (2016). A review of 25 years of research in bidirectionality in parent–child relationships: An examination of methodological approaches. International Journal of Behavioral Development, 40(5), 442–451.CrossRefGoogle Scholar
  43. Pérez-Edgar, K. E., & Guyer, A. E. (2014). Behavioral inhibition: Temperament or prodrome? Current Behavioral Neuroscience Reports, 1(3), 182–190.PubMedPubMedCentralCrossRefGoogle Scholar
  44. Pruessner, J. C., Kirschbaum, C., Meinlschmid, G., & Hellhammer, D. H. (2003). Two formulas for computation of the area under the curve represent measures of total hormone concentration versus time-dependent change. Psychoneuroendocrinology, 28, 916–931.PubMedCrossRefGoogle Scholar
  45. Roberts, G. C., Block, J. H., & Block, J. (1984). Continuity and change in parents' child-rearing practices. Child Development, 55(2), 586–597.CrossRefGoogle Scholar
  46. Roisman, G. I., Newman, D. A., Fraley, R. C., Haltigan, J. D., Groh, A. M., & Haydon, K. C. (2012). Distinguishing differential susceptibility from diathesis–stress: Recommendations for evaluating interaction effects. Development and Psychopathology, 24(2), 389–409.PubMedCrossRefGoogle Scholar
  47. Rubin, K. H., Burgess, K. B., & Hastings, P. D. (2002). Stability and social–behavioral consequences of toddlers’ inhibited temperament and parenting behaviors. Child Development, 73(2), 483–495.PubMedCrossRefGoogle Scholar
  48. Shirtcliff, E. A., Peres, J. C., Dismukes, A. R., Lee, Y., & Phan, J. M. (2014). Hormones: Commentary: Riding the physiological roller coaster: Adaptive significance of cortisol stress reactivity to social contexts. Journal of Personality Disorders, 28(1), 40–51.PubMedCrossRefGoogle Scholar
  49. Silk, J. S., Morris, A. S., Kanaya, T., & Steinberg, L. (2003). Psychological control and autonomy granting: Opposite ends of a continuum or distinct constructs? Journal of Research on Adolescence, 13(1), 113–128.CrossRefGoogle Scholar
  50. Slagt, M., Dubas, J. S., Deković, M., & van Aken, M. A. (2016). Differences in sensitivity to parenting depending on child temperament: A meta-analysis. Psychological Bulletin, 142(10), 1068–1110.PubMedCrossRefGoogle Scholar
  51. van de Weil, N. M. H., van Goozen, S. H., Matthys, W., Snoek, H., & van Engeland, H. (2004). Cortisol and treatment effect in children with disruptive behavior disorders: A preliminary study. Journal of the American Academy of Child & Adolescent Psychiatry, 43(8), 1011–1018.CrossRefGoogle Scholar
  52. von Klitzing, K., Perren, S., Klein, A. M., Stadelmann, S., White, L. O., Groeben, M., et al. (2012). The interaction of social risk factors and HPA axis dysregulation in predicting emotional symptoms of five- and six-year-old children. Journal of Psychiatric Research, 46, 290–297.CrossRefGoogle Scholar
  53. Wagner, N. J., Propper, C., Gueron-Sela, N., & Mills-Koonce, W. R. (2016). Dimensions of maternal parenting and infants’ autonomic functioning interactively predict early internalizing behavior problems. Journal of Abnormal Child Psychology, 44(3), 459–470.PubMedPubMedCentralCrossRefGoogle Scholar
  54. Wagner, N. J., Mills-Koonce, W. R., Willoughby, M. T., & Cox, M. J. (2019). Parenting and cortisol in infancy interactively predict conduct problems and callous–unemotional behaviors in childhood. Child Development, 90, 279–297.PubMedCrossRefGoogle Scholar
  55. Xing, X., & Wang, M. (2018). The moderating role of HPA activity in the relations between parental corporal punishment and executive function in Chinese school-aged children. Psychology of Violence, 8(4), 418–426.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Psychology DepartmentMiami UniversityOxfordUSA

Personalised recommendations