Hostname: page-component-78c5997874-mlc7c Total loading time: 0 Render date: 2024-11-10T11:12:21.810Z Has data issue: false hasContentIssue false

Maternal sensitivity and adrenocortical functioning across infancy and toddlerhood: Physiological adaptation to context?

Published online by Cambridge University Press:  11 April 2016

Daniel Berry*
Affiliation:
University of Illinois, Urbana–Champaign
Clancy Blair
Affiliation:
New York University
Michael Willoughby
Affiliation:
RTI International
Douglas A. Granger
Affiliation:
Johns Hopkins University Arizona State University
W. Roger Mills-Koonce
Affiliation:
University of North Carolina at Greensboro
the Family Life Project Key Investigators
Affiliation:
University of North Carolina at Greensboro Pennsylvania State University
*
Address correspondence and reprint requests to: Daniel Berry, Department of Educational Psychology, College of Education #230B, University of Illinois, Urbana–Champaign, 1310 South Sixth Street, Champaign, IL 61820; E-mail: djberry@illinois.edu.

Abstract

Theory suggests that early experiences may calibrate the “threshold activity” of the hypothalamus–pituitary–adrenal axis in childhood. Particularly challenging or particularly supportive environments are posited to manifest in heightened physiological sensitivity to context. Using longitudinal data from the Family Life Project (N = 1,292), we tested whether links between maternal sensitivity and hypothalamus–pituitary–adrenal axis activity aligned with these predictions. Specifically, we tested whether the magnitude of the within-person relation between maternal sensitivity and children's cortisol levels, a proxy for physiological sensitivity to context, was especially pronounced for children who typically experienced particularly low or high levels of maternal sensitivity over time. Our results were consistent with these hypotheses. Between children, lower levels of mean maternal sensitivity (7–24 months) were associated with higher mean cortisol levels across this period (measured as a basal sample collected at each visit). However, the magnitude and direction of the within-person relation was contingent on children's average levels of maternal sensitivity over time. Increases in maternal sensitivity were associated with contemporaneous cortisol decreases for children with typically low-sensitive mothers, whereas sensitivity increases were associated with cortisol increases for children with typically high-sensitive mothers. No within-child effects were evident at moderate levels of maternal sensitivity.

Type
Regular Articles
Copyright
Copyright © Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Alink, L. R., van IJzendoorn, M. H., Bakermans-Kranenburg, M. J., Mesman, J., Juffer, F., & Koot, H. M. (2008). Cortisol and externalizing behavior in children and adolescents: Mixed meta-analytic evidence for the inverse relation of basal cortisol and cortisol reactivity with externalizing behavior. Developmental Psychobiology, 50, 427450. doi:10.1002/dev.20300 CrossRefGoogle ScholarPubMed
Allison, P. D. (2009). Fixed effects regression methods in SAS (Paper 184-31). Paper presented at the 31st Annual SAS Conference, Cary, NC. Retrieved from http://www2.sas.com/proceedings/sugi31/184-31.pdf Google Scholar
Asparouhov, T. (2008). Scaling of sampling weights for two level models in Mplus 4.2. Los Angeles: Muthén & Muthén.Google Scholar
Belsky, J., & Pluess, M. (2009). Beyond diathesis stress: Differential susceptibility to environmental influences. Psychological Bulletin, 135, 885908. doi:10.1037/a0017376 Google Scholar
Blair, C., Granger, D. A., & Peters Razza, R. (2005). Cortisol reactivity is positively related to executive function in preschool children attending Head Start. Child Development, 76, 554567. doi:10.1111/j.1467-8624.2005.00863.x Google Scholar
Blair, C., Granger, D. A., Willoughby, M., Mills-Koonce, R., Cox, M., Greenberg, M. T., et al. (2011). Salivary cortisol mediates effects of poverty and parenting on executive functions in early childhood. Child Development, 82, 19701984. doi:10.1111/j.1467-8624.2011.01643.x Google Scholar
Blair, C., & Raver, C. C. (2012). Child development in the context of adversity: Experiential canalization of brain and behavior. American Psychologist, 67, 309. doi:10.1037/a0027493 Google Scholar
Blair, C., Raver, C. C., & Berry, D. J. (2014). Two approaches to estimating the effect of parenting on the development of executive function in early childhood. Developmental Psychology, 50, 554. doi:10.1037/a0033647 Google Scholar
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, 271301. doi:10.1017/S0954579405050145 Google Scholar
Bruce, J., Davis, E. P., & Gunnar, M. R. (2002). Individual differences in children's cortisol response to the beginning of a new school year. Psychoneuroendocrinology, 27, 635650. doi:10.1016/S0306-4530(01)00031-2 Google Scholar
Bugental, D. B., Schwartz, A., & Lynch, C. (2010). Effects of an early family intervention on children's memory: The mediating effects of cortisol levels. Mind, Brain, and Education, 4, 159170. doi:10.1111/j.1751-228X.2010.01095.x Google Scholar
Caldji, C., Diorio, J., & Meaney, M. J. (2000). Variations in maternal care in infancy regulate the development of stress reactivity. Biological Psychiatry, 48, 11641174. doi:10.1016/S0006-3223(00)01084-2 CrossRefGoogle ScholarPubMed
Caldji, C., Tannenbaum, B., Sharma, S., Francis, D., Plotsky, P. M., & Meaney, M. J. (1998). Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat. Proceedings of the National Academy of Sciences, 95, 53355340.Google Scholar
Coplan, J. D., Andrews, M. W., Rosenblum, L. A., Owens, M. J., Friedman, S., Gorman, J. M., et al. (1996). Persistent elevations of cerebrospinal fluid concentrations of corticotropin-releasing factor in adult nonhuman primates exposed to early-life stressors: Implications for the pathophysiology of mood and anxiety disorders. Proceedings of the National Academy of Sciences, 93, 16191623.Google Scholar
Coplan, J. D., Trost, R. C., Owens, M. J., Cooper, T. B., Gorman, J. M., Nemeroff, C. B., et al. (1998). Cerebrospinal fluid concentrations of somatostatin and biogenic amines in grown primates reared by mothers exposed to manipulated foraging conditions. Archives of General Psychiatry, 55, 473477. doi:10.1001/archpsyc.55.5.473 CrossRefGoogle ScholarPubMed
Cox, M., Paley, B., Burchinal, M., & Payne, C. (1999). Marital perceptions and interactions across the transition to parenthood. Journal of Marriage and the Family, 61, 611625. http://www.jstor.org/stable/353564 Google Scholar
Davis, E. P., Donzella, B., Krueger, W. K., & Gunnar, M. R. (1999). The start of a new school year: Individual differences in salivary cortisol response in relation to child temperament. Developmental Psychobiology, 35, 188196. doi:10.1002/(SICI)1098-2302(199911)35:3<188::AID-DEV3>3.0.CO;2-KGoogle Scholar
Davis, E. P., Townsend, E. L., Gunnar, M. R., Georgieff, M. K., Guiang, S. F., Ciffuentes, R. F., et al. (2004). Effects of prenatal betamethasone exposure on regulation of stress physiology in healthy premature infants. Psychoneuroendocrinology, 29, 10281036. doi:10.1016/j.psyneuen.2003.10.005 Google Scholar
de Kloet, E. R., Oitzl, M. S., & Joëls, M. (1999). Stress and cognition: Are corticosteroids good or bad guys? Trends in Neurosciences, 22, 422426. doi:10.1016/S0166-2236(99)01438-1 Google Scholar
Del Giudice, M., Ellis, B. J., & Shirtcliff, E. A. (2011). The adaptive calibration model of stress responsivity. Neuroscience & Biobehavioral Reviews, 35, 15621592. doi:10.1016/j.neubiorev.2010.11.007 Google Scholar
Del Giudice, M., Hinnant, J. B., Ellis, B. J., & El-Sheikh, M. (2012). Adaptive patterns of stress responsivity: A preliminary investigation. Developmental Psychology, 48, 775790.CrossRefGoogle ScholarPubMed
Dill, B. T. (1999). Poverty in the rural US: Implications for children, families, and communities. New York: Annie E. Casey Foundation.Google Scholar
Dozier, M., Peloso, E., Lewis, E., Laurenceau, J. P., & Levine, S. (2008). Effects of an attachment-based intervention on the cortisol production of infants and toddlers in foster care. Development and Psychopathology, 20, 845859 doi:10.1111/j.1751-228X.2010.01095.x Google Scholar
Enders, C. K. (2010). Applied missing data analysis. New York: Guilford Press.Google Scholar
Feeney, J., Gaffney, P., & O'Mara, S. M. (2012). Age and cortisol levels modulate judgment of positive and negative facial expressions. Psychoneuroendocrinology, 37, 827835. doi:10.1016/j.psyneuen.2011.09.015 CrossRefGoogle ScholarPubMed
Feldman, R. (2007). Parent-infant synchrony biological foundations and developmental outcomes. Current Directions in Psychological Science, 16, 340345. doi:10.1111/j.1467-8721.2007.00532.x Google Scholar
Flinn, M. V. (2006). Evolution and ontogeny of stress response to social challenges in the human child. Developmental Review, 26, 138174. doi:10.1016/j.dr.2006.02.003 Google Scholar
Flinn, M. V., & England, B. G. (1995). Childhood stress and family environment. Current Anthropology, 36, 854866. http://www.jstor.org/stable/2744033 Google Scholar
Fox, N. A., & Calkins, S. D. (2003). The development of self-control of emotion: Intrinsic and extrinsic influences. Motivation and Emotion, 27, 726. doi:10.1023/A:1023622324898 Google Scholar
Granger, D. A., Kivlighan, K. T., Fortunato, C., Harmon, A. G., Hibel, L. C., Schwartz, E. B., et al. (2007). Integration of salivary biomarkers into developmental and behaviorally-oriented research: Problems and solutions for collecting specimens. Physiology &. Behavior, 924, 583590. doi:10.1016/j.physbeh.2007.05.004 Google Scholar
Gunnar, M. R. (1992). Reactivity of the hypothalamic–pituitary–adrenocortical system to stressors in normal infants and children. Pediatrics, 90, 491497.Google Scholar
Gunnar, M. R., Brodersen, L., Nachmias, M., Buss, K., & Rigatuso, J. (1996). Stress reactivity and attachment security. Developmental Psychobiology, 29, 191204. doi:10.1111/j.1467-8624.1996.tb01748.x Google Scholar
Gunnar, M. R., & Donzella, B. (2002). Social regulation of the cortisol levels in early human development. Psychoneuroendocrinology, 27, 199220. doi:10.1016/s0306-4530(01)00045-2 Google Scholar
Gunnar, M. R., & Herrera, A. M. (2013). The development of stress reactivity: A neurobiological perspective. In Zelazo, P. D. (Ed.), The Oxford handbook of developmental psychology (Vol. 2, pp. 4580). Oxford: Oxford University Press.Google Scholar
Gunnar, M. R., & Quevedo, K. (2007). The neurobiology of stress and development. Annual Review of Psychology, 58, 145173.CrossRefGoogle ScholarPubMed
Gunnar, M. R., Talge, N. M., & Herrera, A. (2009). Stressor paradigms in developmental studies: What does and does not work to produce mean increases in salivary cortisol. Psychoneuroendocrinology, 34, 953967. doi:10.1016/j.psyneuen.2009.02.010 CrossRefGoogle Scholar
Harmon, A. G., Hibel, L. C., Rumyantseva, O., & Granger, D. A. (2007). Measuring salivary cortisol in studies of child development: Watch out—What goes in may not come out of saliva collection devices. Developmental Psychobiology, 495, 495500. doi:10.1002/dev.20231 Google Scholar
Hellhammer, J., Fries, E., Schweisthal, O. W., Schlotz, W., Stone, A. A., & Hagemann, D. (2007). Several daily measurements are necessary to reliably assess the cortisol rise after awakening: State-and-trait components. Psychoneuroendocrinology, 32, 8086. doi:10.1016/j.psyneuen.2006.10.005 Google Scholar
Het, S., Ramlow, G., & Wolf, O. T. (2005). A meta-analytic review of the effects of acute cortisol administration on human memory. Psychoneuroendocrinology, 30, 771784. doi:10.1016/j.psyneuen.2005.03.005 Google Scholar
Hirano, K., & Imbens, G. (2004). The propensity score with continuous treatments. In Gelman, A. & Meng, X. L. (Eds.), Applied Bayesian modeling and causal inference from incomplete-data perspectives. New York: Wiley.Google Scholar
Hostinar, C. E., Sullivan, R. M., & Gunnar, M. R. (2014). Psychobiological mechanisms underlying the social buffering of the hypothalamic–pituitary–adrenocortical axis: A review of animal models and human studies across development. Psychological Bulletin, 140, 256282. doi:10.1037/a0032671 CrossRefGoogle Scholar
Imai, K., & van Dyk, D. A. (2004). Causal inference with general treatment regimes. Journal of the American Statistical Association, 99, 854866. doi:10.1198/016214504000001187 Google Scholar
Kirschbaum, C., & Hellhammer, D. H. (1989). Salivary cortisol in psychobiological research: An overview. Neuropsychobiology, 223, 150169. doi:10.1159/000118611 Google Scholar
Larson, M., White, B. P., Cochran, A., Donzella, B., & Gunnar, M. R. (1998). Dampening of the cortisol response to handling at 3 months in human infants and its relation to sleep, circadian cortisol activity, and behavioral distress. Developmental Psychobiology, 33, 327337. doi:10.1002/(SICI)1098-2302(199812)33:4<327::AID-DEV4>3.0.CO;2-SGoogle Scholar
Lupien, S. J., Maheu, F., Tu, M., Fiocco, A., & Schramek, T. E. (2007). The effects of stress and stress hormones on human cognition: Implications for the field of brain and cognition. Brain and Cognition, 653, 209237. doi:10.1016/j.bandc.2007.02.007 Google Scholar
Lyons, D. M., Lopez, J. M., Yang, C., & Schatzberg, A. F. (2000). Stress-level cortisol treatment impairs inhibitory control of behavior in monkeys. Journal of Neuroscience, 20, 78167821.Google Scholar
Lyons, D. M., & Parker, K. J. (2007). Stress inoculation-induced indications of resilience in monkeys. Journal of Traumatic Stress, 20, 423433. doi:10.1002/jts.20265 Google Scholar
McCartney, K., & Rosenthal, R. (2000). Effect size, practical importance, and social policy for children. Child Development, 71, 173180. http://www.jstor.org/stable/1132230 Google Scholar
McEwen, B. S. (2000). The neurobiology of stress: From serendipity to clinical relevance. Brain Research, 886, 172189. doi:10.1016/s0006-8993(00)02950-4 Google Scholar
McEwen, B. S., & Wingfield, J. C. (2003). The concept of allostasis in biology and biomedicine. Hormones and Behavior, 43, 215. doi:10.1016/S0018-506X(02)00024-7 Google Scholar
Meaney, M. J., & Szyf, M. (2005). Environmental programming of stress responses through DNA methylation: Life at the interface between a dynamic environment and a fixed genome. Dialogues in Clinical Neuroscience, 7, 103123.Google Scholar
Montoya, E. R., Terburg, D., Bos, P. A., & van Honk, J. (2012). Testosterone, cortisol, and serotonin as key regulators of social aggression: A review and theoretical perspective. Motivation and Emotion, 36, 6573. doi:10.1007/s11031-011-9264-3 Google Scholar
Muthén, L. K., & Muthén, B. O. (2009). Mplus: Statistical analysis with latent variables: User's guide. Los Angeles: Author.Google Scholar
NICHD Early Child Care Research Network. (1997). The effects of infant child care on infant–mother attachment security: Results of the NICHD Study of Early Child Care. Child Development, 68, 860879. doi:http://www.jstor.org/stable/1132038 Google Scholar
Parker, K. J., Buckmaster, C. L., Schatzberg, A. F., & Lyons, D. M. (2004). Prospective investigation of stress inoculation in young monkeys. Archives of General Psychiatry, 61, 933941.Google Scholar
Parker, K. J., & Maestripieri, D. (2011). Identifying key features of early stressful experiences that produce stress vulnerability and resilience in primates. Neuroscience & Biobehavioral Reviews, 35, 14661483. doi:10.1016/j.neubiorev.2010.09.003 Google Scholar
Rutter, M. (2012). Resilience as a dynamic concept. Development and Psychopathology, 24, 335344. doi:10.1017/S0954579412000028 Google Scholar
Salvador, A., & Costa, R. (2009). Coping with competition: Neuroendocrine responses and cognitive variables. Neuroscience & Biobehavioral Reviews, 33, 160170. doi:10.1016/j.neubiorev.2008.09.005 Google Scholar
Sánchez, M. M., Noble, P. M., Lyon, C. K., Plotsky, P. M., Davis, M., Nemeroff, C. B., et al. (2005). Alterations in diurnal cortisol rhythm and acoustic startle response in nonhuman primates with adverse rearing. Biological Psychiatry, 57, 373381. doi:10.1016/j.biopsych.2004.11.032 Google Scholar
Sapolsky, R. M., Romero, L. M., & Munck, A. U. (2000). How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocrine Reviews, 211, 5589. doi:10.1210/er.21.1.55 Google Scholar
Satorra, A., & Bentler, P. M. (2001). A scaled difference chi-square test statistic for moment structure analysis. Psychometrika, 66, 507514. doi:10.1007/BF02296192 Google Scholar
Singer, J. D., & Willett, J. B. (2003). Applied longitudinal data analysis: Modeling change and event occurrence. Oxford: Oxford University Press.Google Scholar
Slopen, N., McLaughlin, K. A., & Shonkoff, J. P. (2014). Interventions to improve cortisol regulation in children: A systematic review. Pediatrics, 133, 312326. doi:10.1542/peds.2013-163 Google Scholar
Tarullo, A. R., Mliner, S., & Gunnar, M. R. (2011). Inhibition and exuberance in preschool classrooms: Associations with peer social experiences and changes in cortisol across the preschool year. Developmental Psychology, 47, 1374. doi:10.1037/a0024093 Google Scholar
Toki, S. Morinobu, S., Imanaka, A., Yamamoto, S., Yamawaki, S., & Honma, K. (2007). Importance of early lighting conditions in maternal care by dam as well as anxiety and memory later in life of offspring. European Journal of Neuroscience, 25, 815829. doi:10.1111/j.1460-9568.2007.05288.x Google Scholar
van Honk, J., Tuiten, A., van den Hout, M., Koppeschaar, H., Thijssen, J., de Haan, E., et al. (1998). Baseline salivary cortisol levels and preconscious selective attention for threat: A pilot study. Psychoneuroendocrinology, 23, 741747.Google Scholar
Vernon-Feagans, L., Cox, M., & the Key FLP Investigators (2013). The Family Life Project: An epidemiological and developmental study of young children living in poor rural communities. Monographs of the Society for Research in Child Development, 78(5, Serial No. 310), 1174.Google Scholar
Vijayraghavan, S., Wang, M., Birnbaum, S. G., Williams, G. V., & Arnsten, A. F. (2007). Inverted-U dopamine D1 receptor actions on prefrontal neurons engaged in working memory. Nature Neuroscience, 10, 376384. doi:10.1038/nn1846 CrossRefGoogle ScholarPubMed
Watamura, S., Donzella, B., Kertes, D. A., & Gunnar, M. R. (2004). Developmental changes in baseline cortisol activity in early childhood: Relations with napping and effortful control. Developmental Psychobiology, 45, 125133. doi:10.1002/dev.20026 Google Scholar
Weaver, I. C., Cervoni, N., Champagne, F. A., D'Alessio, A. C., Sharma, S., Seckl, J. R., et al. (2004). Epigenetic programming by maternal behavior. Nature Neuroscience, 7, 847854. doi:10.1038/nn1276 Google Scholar
Weaver, I. C., Meaney, M. J., & Szyf, M. (2006). Maternal care effects on the hippocampal transcriptome and anxiety-mediated behaviors in the offspring that are reversible in adulthood. Proceedings of the National Academy of Sciences, 103, 34803485. doi:10.1073/pnas.0507526103 Google Scholar
Wiener, S. G., Bayart, F., Faull, K. F., & Levine, S. (1990). Behavioral and physiological responses to maternal separation in squirrel monkeys. Behavioral Neuroscience, 104, 108115. doi:10.1037/0735-7044.104.1.108 Google Scholar
Supplementary material: File

Berry supplementary material

Berry supplementary material

Download Berry supplementary material(File)
File 29.7 KB