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Physiological attunement in mother–infant dyads at clinical high risk: The influence of maternal depression and positive parenting

Published online by Cambridge University Press:  19 September 2017

Cassandra L. Hendrix*
Affiliation:
Emory University
Zachary N. Stowe
Affiliation:
University of Wisconsin
D. Jeffrey Newport
Affiliation:
University of Miami Miller School of Medicine
Patricia A. Brennan
Affiliation:
Emory University
*
Address correspondence and reprint requests to: Cassandra L. Hendrix, 36 Eagle Row, Emory University, Atlanta, GA 30322; E-mail: [email protected].

Abstract

A growing number of research studies have examined the intradyadic coregulation (or attunement) of hypothalamus–pituitary–adrenal axis functioning in mothers and their children. However, it is unclear how early this coregulation may be present in dyads at clinical high risk and whether certain factors, such as maternal depression or positive parenting, are associated with the strength of this coregulation. The present study examined cortisol attunement within mother–infant dyads in a high-risk sample of 233 mothers who received treatment for psychiatric illness during pregnancy and whose infants were 6 months old at the study visit. Results showed that maternal and infant cortisol covaried across four time points that included a stressor paradigm and a mother–infant interaction task. Greater maternal positive affect, but not depression, predicted stronger cortisol attunement. In addition, infants’ cortisol level following separation from the mother predicted mothers’ cortisol level at the next time point. Mothers’ cortisol level following the separation and the laboratory stress paradigm predicted infants’ cortisol levels at each successive time point, over and above infants’ own cortisol at the previous time point. These findings suggest that maternal and infant cortisol levels influence one another in a bidirectional fashion that may be temporally and context dependent.

Type
Regular Articles
Copyright
Copyright © Cambridge University Press 2017 

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Footnotes

This research was supported by a NARSAD Young Investigator Grant (to P.A.B.) as well as NIH Grants MD009746, MH088609, MH58922, and MH68036. The first author is supported by the National Science Foundation Graduate Research Fellowship Program under Grant DGE-1444932. Dr. Brennan and Ms. Hendrix declare no conflicts of interest. Dr. Stowe has received research support from the National Institutes of Health, GlaxoSmithKline, Pfizer, and Wyeth; served on speakers or advisory boards for Pfizer, Eli Lilly, Wyeth, Bristol-Myers Squibb, and GlaxoSmithKline; and received honoraria from Eli Lilly, GlaxoSmithKline, Pfizer, and Wyeth. Dr. Newport has received research support from Eli Lilly, GlaxoSmithKline, Janssen, the National Institutes of Health, NARSAD, Takeda Pharmaceuticals, and Wyeth; served on speakers or advisory boards for AstraZeneca, Eli Lilly, GlaxoSmithKline, Pfizer, and Wyeth; and received honoraria from AstraZeneca, Eli Lilly, GlaxoSmithKline, Pfizer, and Wyeth.

References

Atkinson, L., Gonzalez, A., Kashy, D. A., Basile, V. S., Masellis, M., Pereira, J., … Levitan, R. (2013). Maternal sensitivity and infant and mother adrenocortical function across challenges. Psychoneuroendocrinology, 38, 29432951. doi:10.1016/j.psyneuen.2013.08.001Google Scholar
Atkinson, L., Khoury, J., Ludmer, J., Jamieson, B., & Gonzalez, A. (2016). Stress physiology in infancy and early childhood: Cortisol flexibility, attunement, and coordination. Journal of Neuroendocrinology. Advance online publication. doi:10.1111/jne.12408Google Scholar
Bale, T. L. (2006). Stress sensitivity and the development of affective disorders. Hormones and Behavior, 50, 529533.Google Scholar
Beck, A. T., Steer, R. A., & Carbin, M. G. (1988). Psychometric properties of the Beck Depression Inventory: Twenty-five years of evaluation. Clinical Psychology Review, 8, 77100. doi:10.1016/0272-7358(88)90050-5Google Scholar
Beck, A. T., Ward, C. H., Mendelson, M., Mock, J., Erbaugh, J., Comrey, A. L., … Wittenborn, J. R. (1961). An inventory for measuring depression. Archives of General Psychiatry, 4, 561571. doi:10.1001/archpsyc.1961.01710120031004Google Scholar
Beebe, B., Jaffe, J., Markese, S., Buck, K., Chen, H., Cohen, P., … Feldstein, S. (2010). The origins of 12-month attachment: A microanalysis of 4-month mother-infant interaction. Attachment and Human Development, 12, 3141. doi:10.1080/14616730903338985Google Scholar
Belsky, J., & Pluess, M. (2009). Beyond diathesis stress: Differential susceptibility to environmental influences. Psychological Bulletin, 135, 885908. doi:10.1037/a0017376Google Scholar
Blair, C., Granger, D., Willoughby, M., & Kivlighan, K. (2006). Maternal sensitivity is related to hypothalamic-pituitary-adrenal axis stress reactivity and regulation in response to emotion challenge in 6-month-old onfants. Annals of the New York Academy of Sciences, 1094, 263267.10.1196/annals.1376.031Google Scholar
Brandtstädter, J., Baltes-Götz, B., Kirschbaum, C., & Hellhammer, D. (1991). Developmental and personality correlates of adrenocortical activity as indexed by salivary cortisol: Observations in the age range of 35 to 65 years. Journal of Psychosomatic Research, 35, 173185. doi:10.1016/0022-3999(91)90072-VGoogle Scholar
Burke, H. M., Davis, M. C., Otte, C., & Mohr, D. C. (2005). Depression and cortisol responses to psychological stress: A meta-analysis. Psychoneuroendocrinology, 30, 846856.Google Scholar
Butzlaff, R. L., & Hooley, J. M. (1998). Expressed emotion and psychiatric relapse. Archives of General Psychiatry, 55, 547. doi:10.1001/archpsyc.55.6.547Google Scholar
Centola, D. (2010). The spread of behavior in an online social network experiment. Science, 329(5996), 11941197.Google Scholar
Clearfield, M. W., Carter-Rodriguez, A., Merali, A.-R., & Shober, R. (2014). The effects of SES on infant and maternal diurnal salivary cortisol output. Infant Behavior and Development, 37, 298304. doi:10.1016/j.infbeh.2014.04.008Google Scholar
Coviello, L., Sohn, Y., Kramer, A. D. I., Marlow, C., Franceschetti, M., Christakis, N. A., & Fowler, J. H. (2014). Detecting emotional contagion in massive social networks. PLOS ONE, 9, e90315. doi:10.1371/journal.pone.0090315Google Scholar
Davis, E. P., & Granger, D. A. (2009). Developmental differences in infant salivary alpha-amylase and cortisol responses to stress. Psychoneuroendocrinology, 34, 795804.Google Scholar
De Waal, F. B. (2008). Putting the altruism back into altruism: The evolution of empathy. Annual Reviews of Psychology, 59, 279300.Google Scholar
Feldman, R. (2003). Infant-mother and infant-father synchrony: The coregulation of positive arousal. Infant Mental Health Journal, 24, 123. doi:10.1002/imhj.10041Google Scholar
Feldman, R. (2007). Parent–infant synchrony and the construction of shared timing: Physiological precursors, developmental outcomes, and risk conditions. Journal of Child Psychology and Psychiatry, 48, 329354.10.1111/j.1469-7610.2006.01701.xGoogle Scholar
Field, T., Healy, B. T., Goldstein, S., & Guthertz, M. (1990). Behavior-state matching and synchrony in mother-infant interactions of nondepressed versus depressed dyads. Developmental Psychology, 26, 7.Google Scholar
First, M. B., Spitzer, R. L., Gibbon, M., Williams, J. B. W. (2002). Structured Clinical Interview for DSM-IV-TR Axis I disorders, research version, patient edition. New York: New York Psychiatric Institute, Biometric Research.Google Scholar
Fowler, J. H., & Christakis, N. A. (2008). Dynamic spread of happiness in a large social network: Longitudinal analysis over 20 years in the Framingham Heart Study. British Medical Journal, 337, a2338.Google Scholar
Golberstein, E., Whitlock, J. L., & Downs, M. F. (2013). Social contagion of mental health: Evidence from college roommates. Health Economics, 22, 965986. doi:10.1002/hec.2873Google Scholar
Goldberg, S., Levitan, R., Leung, E., Masellis, M., Basile, V. S., Nemeroff, C. B., & Atkinson, L. (2003). Cortisol concentrations in 12- to 18-month-old infants: Stability over time, location, and stressor. Biological Psychiatry, 54, 719726. doi:10.1016/S0006-3223(03)00010-6Google Scholar
Goodman, S. H., & Gotlib, I. (1999). Risk for psychopathology in the children of depressed mothers: A developmental model for understanding mechanisms of transmission. Psychological Review, 106, 458490. doi:10.1037/10449-000Google Scholar
Goodman, S. H., Rouse, M. H., Connell, A. M., Broth, M. R., Hall, C. M., & Heyward, D. (2011). Maternal depression and child psychopathology: A meta-analytic review. Clinical Child and Family Psychology Review, 14, 127. doi:10.1007/s10567-010-0080-1Google Scholar
Gunnar, M. R., & Donzella, B. (2002). Social regulation of the cortisol levels in early human development. Psychoneuroendocrinology, 27, 199220.Google Scholar
Hane, A. A., & Fox, N. A. (2006). Ordinary variations in maternal caregiving influence human infants’ stress reactivity. Psychological Science, 17, 550556.Google Scholar
Hibel, L. C., Granger, D. A., Blair, C., & Finegood, E. D. (2015). Maternal-child adrenocortical attunement in early childhood: Continuity and change. Developmental Psychobiology, 57, 8395. doi:10.1002/dev.21266Google Scholar
Hibel, L. C., Trumbell, J. M., & Mercado, E. (2014). Work/non-workday differences in mother, child, and mother–child morning cortisol in a sample of working mothers and their children. Early Human Development, 90, 17. doi:10.1016/j.earlhumdev.2013.11.007Google Scholar
Hunter, A. L., Minnis, H., & Wilson, P. (2011). Altered stress responses in children exposed to early adversity: A systematic review of salivary cortisol studies. Stress, 14, 614626.Google Scholar
Jessop, D. S., & Turner-Cobb, J. M. (2008). Measurement and meaning of salivary cortisol: A focus on health and disease in children: Review. Stress, 11, 114.Google Scholar
Ji, S., Long, Q., Newport, D. J., Na, H., Knight, B., Zach, E. B., … Stowe, Z. N. (2011). Validity of depression rating scales during pregnancy and the postpartum period: Impact of trimester and parity. Journal of Psychiatric Research, 45, 213219. doi:10.1016/j.jpsychires.2010.05.017Google Scholar
Johnson, K. C., Brennan, P. A., Stowe, Z. N., Leibenluft, E., & Newport, D. J. (2014). Physiological regulation in infants of women with a mood disorder: Examining associations with maternal symptoms and stress. Journal of Child Psychology and Psychiatry, and Allied Disciplines, 55, 191198. doi:10.1111/jcpp.12130Google Scholar
Kirschbaum, C., & Hellhammer, D. H. (1989). Salivary cortisol in psychobiological research: An overview. Neuropsychobiology, 22, 150169.Google Scholar
Landry, S. H., Smith, K. E., Swank, P. R., & Guttentag, C. (2008). A responsive parenting intervention: The optimal timing across early childhood for impacting maternal behaviors and child outcomes. Developmental Psychology, 44, 13351353. doi:10.1037/a0013030Google Scholar
Laurent, H. K., Ablow, J. C., & Measelle, J. (2011). Risky shifts: How the timing and course of mothers’ depressive symptoms across the perinatal period shape their own and infant's stress response profiles. Development and Psychopathology, 23, 521538. doi:10.1017/S0954579411000083Google Scholar
Laurent, H. K., Ablow, J. C., & Measelle, J. (2012). Taking stress response out of the box: Stability, discontinuity, and temperament effects on HPA and SNS across social stressors in mother–infant dyads. Developmental Psychology, 48, 35.Google Scholar
LeMoult, J., Chen, M. C., Foland-Ross, L. C., Burley, H. W., & Gotlib, I. H. (2015). Concordance of mother-daughter diurnal cortisol production: Understanding the intergenerational transmission of risk for depression. Biological Psychology, 108, 98104. doi:10.1016/j.biopsycho.2015.03.019Google Scholar
Lopez-Duran, N. L., Mayer, S. E., & Abelson, J. L. (2014). Modeling neuroendocrine stress reactivity in salivary cortisol: Adjusting for peak latency variability. Stress, 17, 285295. doi:10.3109/10253890.2014.915517Google Scholar
Lovejoy, M. C., Graczyk, P. A., O'Hare, E., & Neuman, G. (2000). Maternal depression and parenting behavior: A meta-analytic review. Clinical Psychology Review, 20, 561592.10.1016/S0272-7358(98)00100-7Google Scholar
Merwin, S. M., Smith, V. C., Kushner, M., Lemay, E. P., & Dougherty, L. R. (2017). Parent-child adrenocortical concordance in early childhood: The moderating role of parental depression and child temperament. Biological Psychology. Advance online publication. doi:10.1016/j.biopsycho.2017.01.013Google Scholar
Newport, D. J., Stowe, Z. N., & Nemeroff, C. B. (2002). Parental depression: Animal models of an adverse life event. American Journal of Psychiatry, 159, 12651283.Google Scholar
Papp, L. M., Pendry, P., & Adam, E. K. (2009). Mother-adolescent physiological synchrony in naturalistic settings: Within-family cortisol associations and moderators. Journal of Family Psychology, 23, 882894.Google Scholar
Paulson, J. F., & Bazemore, S. D. (2010). Prenatal and postpartum depression in fathers and its association with maternal depression: A meta-analysis. Journal of the American Medical Association, 303, 19611969.Google Scholar
Powers, S. I., Pietromonaco, P. R., Gunlicks, M., & Sayer, A. (2006). Dating couples’ attachment styles and patterns of cortisol reactivity and recovery in response to a relationship conflict. Journal of Personality and Social Psychology, 90, 513528.Google Scholar
Pratt, M., Apter-Levi, Y., Vakart, A., Kanat-Maymon, Y., Zagoory-Sharon, O., & Feldman, R. (2017). Mother-child adrenocortical synchrony: Moderation by dyadic relational behavior. Hormones and Behavior, 89, 167175. doi:10.1016/j.yhbeh.2017.01.003Google Scholar
Ramsay, D., & Lewis, M. (2003). Reactivity and regulation in cortisol and behavioral responses to stress. Child Development, 74, 456464. doi:10.1111/1467-8624.7402009Google Scholar
Righetti-Veltema, M., Conne-Perréard, E., Bousquet, A., & Manzano, J. (2002). Postpartum depression and mother–infant relationship at 3 months old. Journal of Affective Disorders, 70, 291306. doi:10.1016/S0165-0327(01)00367-6Google Scholar
Rosenquist, J. N., Fowler, J. H., & Christakis, N. A. (2011). Social network determinants of depression. Molecular Psychiatry, 16, 273281.Google Scholar
Ruttle, P. L., Serbin, L. A., Stack, D. M., Schwartzman, A. E., & Shirtcliff, E. A. (2011). Adrenocortical attunement in mother-child dyads: Importance of situational and behavioral characteristics. Biological Psychology, 88, 104111. doi:10.1016/j.biopsycho.2011.06.014Google Scholar
Sanchez, M. M. (2006). The impact of early adverse care on HPA axis development: Nonhuman primate models. Hormones and Behavior, 50, 623631. doi:10.1016/j.yhbeh.2006.06.012Google Scholar
Sanchez, M. M., McCormack, K., Grand, A. P., Fulks, R., Graff, A., & Maestripieri, D. (2010). Effects of sex and early maternal abuse on adrenocorticotropin hormone and cortisol responses to the corticotropin-releasing hormone challenge during the first 3 years of life in group-living rhesus monkeys. Development and Psychopathology, 22, 4553. doi:10.1017/S0954579409990253Google Scholar
Saxbe, D. E., Margolin, G., Spies Shapiro, L., Ramos, M., Rodriguez, A., & Iturralde, E. (2014). Relative influences: Patterns of HPA axis concordance during triadic family interaction. Health Psychology, 33, 273281.Google Scholar
Schechter, J. C., Brennan, P. A., Smith, A. K., Stowe, Z. N., Newport, D. J., & Johnson, K. C. (2017). Maternal prenatal psychological distress and preschool cognitive functioning: The protective role of positive parental engagement. Journal of Abnormal Child Psychology, 45, 249260. doi:10.1007/s10802-016-0161-9Google Scholar
Sethre-Hofstad, L., Stansbury, K., & Rice, M. A. (2002). Attunement of maternal and child adrenocortical response to child challenge. Psychoneuroendocrinology, 27, 731747.Google Scholar
Smith, A. K., Newport, D. J., Ashe, M. P., Brennan, P. A., Laprairie, J. L., Calamaras, M., … Stowe, Z. N. (2011). Predictors of neonatal hypothalamic-pituitary-adrenal axis activity at delivery. Clinical Endocrinology, 75, 9095. doi:10.1111/j.1365-2265.2011.03998.xGoogle Scholar
Steer, R. A., Ball, R., Raneeri, W. F., & Beck, A. T. (1997). Further evidence for the construct validity of the Beck Depression Inventory-II with psychiatric outpatients. Psychological Reports, 80, 443446.Google Scholar
Thompson, L. A., & Trevathan, W. R. (2008). Cortisol reactivity, maternal sensitivity, and learning in 3-month-old infants. Infant Behavior and Development, 31, 92106.Google Scholar
van Bakel, H. J. A., & Riksen-Walraven, J. M. (2008). Adrenocortical and behavioral attunement in parents with 1-year-old infants. Developmental Psychobiology, 50, 196201.Google Scholar
Woody, M. L., Feurer, C., Sosoo, E. E., Hastings, P. D., & Gibb, B. E. (2016). Synchrony of physiological activity during mother–child interaction: Moderation by maternal history of major depressive disorder. Journal of Child Psychology and Psychiatry, 57, 843850. doi:10.1111/jcpp.12562Google Scholar