Hostname: page-component-cd9895bd7-dk4vv Total loading time: 0 Render date: 2024-12-26T08:14:52.285Z Has data issue: false hasContentIssue false
  • English
  • Français

Biological sensitivity to context: A test of the hypothesized U-shaped relation between early adversity and stress responsivity

Published online by Cambridge University Press:  26 July 2019

Nila Shakiba ,
Bruce J. Ellis ,
Nicole R. Bush  and
W. Thomas Boyce
Nila Shakiba*
Affiliation:
Department of Psychology, University of Utah, Salt Lake City, UT, USA
Bruce J. Ellis
Affiliation:
Department of Psychology, University of Utah, Salt Lake City, UT, USA Department of Anthropology, University of Utah, Salt Lake City, UT, USA
Nicole R. Bush
Affiliation:
Departments of Psychiatry and Pediatrics, University of California, San Francisco, Division of Developmental Medicine, San Francisco, CA, USA
W. Thomas Boyce
Affiliation:
Departments of Psychiatry and Pediatrics, University of California, San Francisco, Division of Developmental Medicine, San Francisco, CA, USA
*
Author for Correspondence: Nila Shakiba, Department of Psychology, 380 South 1530 East, BEH S Room 502, University of Utah, Salt Lake City, UT84112; E-mail: [email protected].
Get access Rights & Permissions [Opens in a new window]

Abstract

We conducted signal detection analyses to test for curvilinear, U-shaped relations between early experiences of adversity and heightened physiological responses to challenge, as proposed by biological sensitivity to context theory. Based on analysis of an ethnically diverse sample of 338 kindergarten children (4–6 years old) and their families, we identified levels and types of adversity that, singly and interactively, predicted high (top 25%) and low (bottom 25%) rates of stress reactivity. The results offered support for the hypothesized U-shaped curve and conceptually replicated and extended the work of Ellis, Essex, and Boyce (2005). Across both sympathetic and adrenocortical systems, a disproportionate number of children growing up under conditions characterized by either low or high adversity (as indexed by restrictive parenting, family stress, and family economic condition) displayed heightened stress reactivity, compared with peers growing up under conditions of moderate adversity. Finally, as hypothesized by the adaptive calibration model, a disproportionate number of children who experienced exceptionally stressful family conditions displayed blunted cortisol reactivity to stress.

Keywords

autonomic nervous systembiological sensitivity to contextearly adversityhypothalamic–pituitary–adrenal axisstress reactivity
Type
Regular Articles
Information
Development and Psychopathology , Volume 32 , Issue 2 , May 2020 , pp. 641 - 660
Copyright
Copyright © Cambridge University Press 2019

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

Alkon, A., Boyce, W. T., Tran, L., Harley, K. G., Neuhaus, J., & Eskenazi, B. (2014). Prenatal adversities and Latino children's autonomic nervous system reactivity trajectories from 6 months to 5 years of age. PLOS ONE, 9, e86283. doi:10.1371/journal.pone.0086283CrossRefGoogle ScholarPubMed
Alkon, A., Goldstein, L., Smider, N., Essex, M., Boyce, W., & Kupfer, D. (2003). Developmental and contextual influences on autonomic reactivity in young children. Developmental Psychobiology, 42, 64–78. doi:10.1002/dev.10082CrossRefGoogle ScholarPubMed
Azar, R., Paquette, D., Zoccolillo, M., Baltzer, F., & Tremblay, R. E. (2007). The association of major depression, conduct disorder, and maternal overcontrol with a failure to show a cortisol buffered response in 4-month-old infants of teenage mothers. Biological Psychiatry, 62, 573–579. doi:10.1016/j.biopsych.2006.11.009CrossRefGoogle ScholarPubMed
Bar-Haim, Y., Marshall, P., & Fox, N. (2000). Developmental changes in heart period and high-frequency heart period variability from 4 months to 4 years of age. Developmental Psychobiology, 37, 44–56. doi:10.1002/1098-2302(200007)37:1<44::AID-DEV6>3.0.CO;2-73.0.CO;2-7>CrossRefGoogle ScholarPubMed
Bateup, H. S., Booth, A., Shirtcliff, E. A., & Granger, D. A. (2002). Testosterone, cortisol, and women's competition. Evolution and Human Behavior, 23, 181–192. doi:10.1016/s1090-5138(01)00100-3CrossRefGoogle Scholar
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. doi:10.1017/s0954579401002012CrossRefGoogle ScholarPubMed
Beauchaine, T. P., Gatzke-Kopp, L., & Mead, H. K. (2007). Polyvagal theory and developmental psychopathology: Emotion dysregulation and conduct problems from preschool to adolescence. Biological Psychology, 74, 174–184. doi:10.1016/j.biopsycho.2005.08.008CrossRefGoogle Scholar
Belsky, J., & Pluess, M. (2009). Beyond diathesis stress: Differential susceptibility to environmental influences. Psychological Bulletin, 135, 885–908. doi:10.1037/a0017376CrossRefGoogle ScholarPubMed
Berntson, G., Bigger, J., Eckberg, D., Grossman, P., Kaufman, P., Malik, M., … van der Molen, M. W. (1997). Heart rate variability: Origins, methods, and interpretive caveats. Psychophysiology, 34, 623–648. doi:10.1111/j.1469-8986.1997.tb02140.xCrossRefGoogle ScholarPubMed
Berntson, G., Cacioppo, J., & Quigley, K. (1993). Respiratory sinus arrhythmia: Autonomic origins, physiological mechanisms, and psychophysiological implications. Psychophysiology, 30, 183–196.CrossRefGoogle ScholarPubMed
Berntson, G. G., Quigley, K. S., Jang, J., & Boysen, S. T. (1990). An approach to artifact identification: Application to heart period data. Psychophysiology, 27, 586–598. doi:10.1111/j.1469-8986.1990.tb01982.xCrossRefGoogle ScholarPubMed
Berry, D., Blair, C., Willoughby, M., Granger, D. A., Mills-Koonce, W. R., & Family Life Project Key Investigators. (2017). Maternal sensitivity and adrenocortical functioning across infancy and toddlerhood: Physiological adaptation to context? Development and Psychopathology, 29, 303–317. doi:10.1017/s0954579416000158CrossRefGoogle ScholarPubMed
Blair, C., Granger, D. A., Kivlighan, K. T., Mills-Koonce, R., Willoughby, M., Greenberg, M. T., … Fortunato, C. K. (2008). Maternal and child contributions to cortisol response to emotional arousal in young children from low-income, rural communities. Developmental Psychology, 44, 1095–1109. doi:10.1037/0012-1649.44.4.1095CrossRefGoogle ScholarPubMed
Block, J. H. (1965). The child-rearing practices report. Unpublished manuscript, University of California, Berkeley.Google Scholar
Bornstein, M. H., & Suess, P. E. (2000). Child and mother cardiac vagal tone: Continuity, stability, and concordance across the first 5 years. Developmental Psychology, 36, 54–65. doi:10.1037//0012-1649.36.1.54CrossRefGoogle ScholarPubMed
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, 271–301. doi:10.1017/s0954579405050145Google Scholar
Boyce, W. T., Quas, J., Alkon, A., Smider, N. A., Essex, M. J., & Kupfer, D. J. (2001). Autonomic reactivity and psychopathology in middle childhood. British Journal of Psychiatry, 179, 144–150. doi:10.1192/bjp.179.2.144CrossRefGoogle ScholarPubMed
Bronfenbrenner, U. (1979). The ecology of human development: Experiments by nature and design. Cambridge, MA: Harvard University Press.Google Scholar
Bronfenbrenner, U. (1989). Ecological systems theory. Annals of Child Development, 6, 187–249.Google Scholar
Bugental, D. B., Martorell, G. A., & Barraza, V. (2003). The hormonal costs of subtle forms of infant maltreatment. Hormones and Behavior, 43, 237–244. doi:10.1016/s0018-506x(02)00008-9CrossRefGoogle ScholarPubMed
Bunea, I. M., Szentágotai-Tătar, A., & Miu, A. C. (2017). Early-life adversity and cortisol response to social stress: A meta-analysis. Translational Psychiatry, 7, 1274. doi:10.1038/s41398-017-0032-3CrossRefGoogle ScholarPubMed
Bush, N. R., Alkon, A., Obradović, J., Stamperdahl, J., & Boyce, W. T. (2011). Differentiating challenge reactivity from psychomotor activity in studies of children's psychophysiology: Considerations for theory and measurement. Journal of Experimental Child Psychology, 110, 62–79. doi:10.1016/j.jecp.2011.03.004CrossRefGoogle Scholar
Bush, N. R., & Boyce, W. T. (2014). The contributions of early experience to biological development and sensitivity to context. In Handbook of developmental psychopathology (pp. 287–309). Boston: Springer.CrossRefGoogle Scholar
Bush, N. R., & Boyce, W. T. (2016). Differential sensitivity to context: Implications for developmental psychopathology. In Cicchetti, D. (Ed.), Developmental psychopathology (pp. 107–137). Hoboken, NJ: Wiley.Google Scholar
Bush, N. R., Caron, Z. K., Blackburn, K. S., & Alkon, A. (2016). Measuring cardiac autonomic nervous system (ANS) activity in toddlers—Testing and developmental challenges. Journal of Visualized Experiments, 108, e53652. doi:10.3791/53652Google Scholar
Bush, N. R., Jones-Mason, K., Coccia, M., Caron, Z., Alkon, A., Thomas, M., … Epel, E. S. (2017). Effects of pre- and postnatal maternal stress on infant temperament and autonomic nervous system reactivity and regulation in a diverse, low-income population. Development and Psychopathology, 29, 1553–1571. doi:10.1017/S0954579417001237CrossRefGoogle Scholar
Bush, N. R., Obradović, J., Adler, N., & Boyce, W. T. (2011). Kindergarten stressors and cumulative adrenocortical activation: The “first straws” of allostatic load? Development and Psychopathology, 23, 1089–1106. doi:10.1017/s0954579411000514CrossRefGoogle ScholarPubMed
Cacioppo, J. T., Uchino, B. N., & Berntson, G. G. (1994). Individual differences in the autonomic origins of heart rate reactivity: The psychometrics of respiratory sinus arrhythmia and preejection period. Psychophysiology, 31, 412–419.CrossRefGoogle ScholarPubMed
Calkins, S. D., & Keane, S. P. (2004). Cardiac vagal regulation across the preschool period: Stability, continuity, and implications for childhood adjustment. Developmental Psychobiology, 45, 101–112. doi:10.1002/dev.20020CrossRefGoogle ScholarPubMed
Carlson, R. (1985). Gesell School Readiness Test. In Keyser, D. & Sweetland, R. (Eds.), Test critiques. Kansas City, KS: Test Corporation of America.Google Scholar
Chatterton, R. T. Jr., Vogelsong, K. M., Lu, Y. C., & Hudgens, G. A. (1997). Hormonal responses to psychological stress in men preparing for skydiving. Journal of Clinical Endocrinology and Metabolism, 82, 2503–2509. doi:10.1210/jc.82.8.2503Google ScholarPubMed
Chen, E., Langer, D. A., Raphaelson, Y. E., & Matthews, K. A. (2004). Socioeconomic status and health in adolescents: The role of stress interpretations. Child Development, 75, 1039–1052. doi:10.1111/j.1467-8624.2004.00724.xCrossRefGoogle ScholarPubMed
Conradt, E., Abar, B., Sheinkopf, S., Lester, B., Lagasse, L., Seifer, R., … Hinckley, M. (2014). The role of prenatal substance exposure and early adversity on parasympathetic functioning from 3 to 6 years of age. Developmental Psychobiology, 56, 821–835. doi:10.1002/dev.21155CrossRefGoogle ScholarPubMed
Conradt, E., Beauchaine, T., Abar, B., Lester, B. M., Lagasse, L. L., Shankaran, S., … Hammond, J. A. (2016). RSA reactivity at one month moderates the relation between early caregiving stress exposure and biobehavioral outcomes at age three. Psychophysiology, 53, 83–96. doi:10.1111/psyp.12569CrossRefGoogle Scholar
Davies, P. T., Sturge-Apple, M. L., Cicchetti, D., & Cummings, E. M. (2008). Adrenocortical underpinnings of children's psychological reactivity to interparental conflict. Child Development, 79, 1693–1706. doi:10.1111/j.1467-8624.2008.01219.xCrossRefGoogle ScholarPubMed
Deković, M., Janssens, J. M. A. M., & Gerris, J. R. M. (1991). Factor structure and construct validity of the Block Child Rearing Practice Report (CRPR): Psychological Assessment. Journal of Consulting & Clinical Psychology, 3, 182–187. doi:10.1037/1040-3590.3.2.182CrossRefGoogle Scholar
Del Giudice, M., & Ellis, B. J. (2016). Evolutionary foundations of developmental psychopathology. In Cicchetti, D. (Ed.), Developmental psychopathology: Vol. 2. Developmental neuroscience (3rd ed., pp. 1–58). New York: Wiley.Google Scholar
Del Giudice, M., Ellis, B. J., & Shirtcliff, E. A. (2011). The adaptive calibration model of stress responsivity. Neuroscience & Biobehavioral Reviews, 35, 1562–1592. doi:10.1016/j.neubiorev.2010.11.007CrossRefGoogle ScholarPubMed
Del Giudice, M., Hinnant, J. B., Ellis, B. J., & El-Sheikh, M. (2012). Adaptive patterns of stress responsivity: A preliminary investigation. Developmental Psychology, 48, 775–790. doi:10.1037/a0026519CrossRefGoogle ScholarPubMed
DePasquale, C. E., Raby, K. L., Hoye, J., & Dozier, M. (2018). Parenting predicts strange situation cortisol reactivity among children adopted internationally. Psychoneuroendocrinology, 89, 86–91. doi:10.1016/j.psyneuen.2018.01.003CrossRefGoogle ScholarPubMed
Durand, C. P. (2013). Does raising type 1 error rate improve power to detect interactions in linear regression models? A simulation study. PLOS ONE, 8, e71079. doi:10.1371/journal.pone.0071079CrossRefGoogle ScholarPubMed
Eisenberg, N., Fabes, R., Bustamante, D., Mathy, R., Miller, P., & Lindholm, E. (1988). Differentiation of vicariously induced emotional reactions in children. Developmental Psychology, 24, 237–246. doi:10.1037/0012-1649.24.2.237CrossRefGoogle Scholar
Ellis, B. J., Bates, J. E., Dodge, K. A., Fergusson, D. M., John Horwood, L., Pettit, G. S., & Woodward, L. (2003). Does father absence place daughters at special risk for early sexual activity and teenage pregnancy? Child Development, 74, 801–821. doi:10.1111/1467-8624.00569CrossRefGoogle ScholarPubMed
Ellis, B. J., & Del Giudice, M. (2014). Beyond allostatic load: Rethinking the role of stress in regulating human development. Development and Psychopathology, 26, 1–20. doi:10.1017/s0954579413000849CrossRefGoogle ScholarPubMed
Ellis, B. J., & Del Giudice, M. (2019). Developmental adaptation to stress: An evolutionary perspective. Annual Review of Psychology, 70, 111–139. doi:10.1146/annurev-psych-122216-011732CrossRefGoogle Scholar
Ellis, B. J., Essex, M. J., & Boyce, W. T. (2005). Biological sensitivity to context: II. Empirical explorations of an evolutionary–developmental theory. Development and Psychopathology, 17, 303–328. doi:10.1017/s0954579405050157CrossRefGoogle ScholarPubMed
Ellis, B. J., Oldehinkel, A. J., & Nederhof, E. (2017). The adaptive calibration model of stress responsivity: An empirical test in the Tracking Adolescents' Individual Lives Survey study. Development and Psychopathology, 29, 1001–1021. doi:10.1017/s0954579416000985CrossRefGoogle ScholarPubMed
El-Sheikh, M. (2005). The role of emotional responses and physiological reactivity in the marital conflict–child functioning link. Journal of Child Psychology and Psychiatry, 46, 1191–1199. doi:10.1111/j.1469-7610.2005.00418.xCrossRefGoogle ScholarPubMed
El-Sheikh, M., & Erath, S. A. (2011). Family conflict, autonomic nervous system functioning, and child adaptation: State of the science and future directions. Development and Psychopathology, 23, 703–721. doi:10.1017/S0954579411000034CrossRefGoogle ScholarPubMed
El-Sheikh, M., & Hinnant, J. B. (2011). Marital conflict, respiratory sinus arrhythmia, and allostatic load: Interrelations and associations with the development of children's externalizing behavior. Development and Psychopathology, 23, 815–829. doi:10.1017/s0954579411000320CrossRefGoogle ScholarPubMed
El-Sheikh, M., Kouros, C. D., Erath, S., Cummings, E. M., Keller, P., & Staton, L. (2009). Marital conflict and children's externalizing behavior: Pathways involving interactions between parasympathetic and sympathetic nervous system activity. Monographs of the Society for Research in Child Development, 74, vii–79. doi:10.1111/j.1540-5834.2009.00501.xGoogle Scholar
Engert, V., Efanov, S. I., Dedovic, K., Duchesne, A., Dagher, A., & Pruessner, J. C. (2010). Perceived early-life maternal care and the cortisol response to repeated psychosocial stress. Journal of Psychiatry & Neuroscience, 35, 370–377. doi:10.1503/jpn.100022CrossRefGoogle ScholarPubMed
Enlow, M. B., King, L., Schreier, H. M., Howard, J. M., Rosenfield, D., Ritz, T., & Wright, R. J. (2014). Maternal sensitivity and infant autonomic and endocrine stress responses. Early Human Development, 90, 377–385. doi:10.1016/j.earlhumdev.2014.04.007CrossRefGoogle Scholar
Essex, M. J., Klein, M. H., Cho, E., & Kalin, N. H. (2002). Maternal stress beginning in infancy may sensitize children to later stress exposure: Effects on cortisol and behavior. Biological Psychiatry, 52, 776–784. doi:10.1016/s0006-3223(02)01553-6CrossRefGoogle ScholarPubMed
Evans, B. E., Greaves-Lord, K., Euser, A. S., Tulen, J. H., Franken, I. H., & Huizink, A. C. (2013). Determinants of physiological and perceived physiological stress reactivity in children and adolescents. PLOS ONE, 8, e61724. doi:10.1371/journal.pone.0061724CrossRefGoogle ScholarPubMed
Eysenck, H. J. (1983). Stress, disease, and personality: The inoculation effect. In Cooper, C. L. (Ed.), Stress research (pp. 121–146). New York: Wiley.Google Scholar
Fearon, R. P., Tomlinson, M., Kumsta, R., Skeen, S., Murray, L., Cooper, P. J., & Morgan, B. (2017). Poverty, early care, and stress reactivity in adolescence: Findings from a prospective, longitudinal study in South Africa. Development and Psychopathology, 29, 449–464. doi:10.1017/s0954579417000104CrossRefGoogle ScholarPubMed
Feldman, R., Granat, A., Pariente, C., Kanety, H., Kuint, J., & Gilboa-Schechtman, E. (2009). Maternal depression and anxiety across the postpartum year and infant social engagement, fear regulation, and stress reactivity. Journal of the American Academy of Child & Adolescent Psychiatry, 48, 919–927. doi:10.1097/chi.0b013e3181b21651CrossRefGoogle ScholarPubMed
Fernald, L. C., Burke, H. M., & Gunnar, M. R. (2008). Salivary cortisol levels in children of low-income women with high depressive symptomatology. Development and Psychopathology, 20, 423–436. doi:10.1017/s0954579408000205CrossRefGoogle ScholarPubMed
Fisher, P. A., Kim, H. K., Bruce, J., & Pears, K. C. (2012). Cumulative effects of prenatal substance exposure and early adversity on foster children's HPA-axis reactivity during a psychosocial stressor. International Journal of Behavioral Development, 36, 29–35. doi:10.1177/0165025411406863CrossRefGoogle ScholarPubMed
Flinn, M. V., Nepomnaschy, P. A., Muehlenbein, M. P., & Ponzi, D. (2011). Evolutionary functions of early social modulation of hypothalamic-pituitary-adrenal axis development in humans. Neuroscience & Biobehavioral Reviews, 35, 1611–1629. doi:10.1016/j.neubiorev.2011.01.005CrossRefGoogle ScholarPubMed
Fox, A. R., Hammond, L. E., & Mezulis, A. H. (2018). Respiratory sinus arrhythmia and adaptive emotion regulation as predictors of nonsuicidal self-injury in young adults. International Journal of Psychophysiology, 133, 1–11. doi:10.1016/j.ijpsycho.2018.09.006CrossRefGoogle ScholarPubMed
Gangel, M. J., Shanahan, L., Kolacz, J., Janssen, J. A., Brown, A., Calkins, S. D., … Wideman, L. (2017). Vagal regulation of cardiac function in early childhood and cardiovascular risk in adolescence. Psychosomatic Medicine, 79, 614–621. doi:10.1097/PSY.0000000000000458CrossRefGoogle ScholarPubMed
Gifford, R. M., & Reynolds, R. M. (2017). Sex differences in early-life programming of the hypothalamic–pituitary–adrenal axis in humans. Early Human Development, 114, 7–10. doi:10.1016/j.earlhumdev.2017.09.011CrossRefGoogle ScholarPubMed
Gump, B. B., Matthews, K. A., & Räikkönen, K. (1999). Modeling relationships among socioeconomic status, hostility, cardiovascular reactivity, and left ventricular mass in African American and White children. Health Psychology, 18, 140–150. doi:10.1037//0278-6133.18.2.140CrossRefGoogle ScholarPubMed
Gunnar, M. R., Frenn, K., Wewerka, S. S., & Van Ryzin, M. J. (2009). Moderate versus severe early life stress: Associations with stress reactivity and regulation in 10–12-year-old children. Psychoneuroendocrinology, 34, 62–75. doi:10.1016/j.psyneuen.2008.08.013CrossRefGoogle ScholarPubMed
Hackman, D. A., Betancourt, L. M., Brodsky, N. L., Kobrin, L., Hurt, H., & Farah, M. J. (2013). Selective impact of early parental responsivity on adolescent stress reactivity. PLOS ONE, 8, e58250. doi:10.1371/journal.pone.0058250CrossRefGoogle ScholarPubMed
Hagan, M. J., Roubinov, D. S., Purdom Marreiro, C. L., & Luecken, L. J. (2014). Childhood interparental conflict and HPA axis activity in young adulthood: Examining nonlinear relations. Developmental Psychobiology, 56, 871–880. doi:10.1002/dev.21157CrossRefGoogle ScholarPubMed
Halberstadt, A. G. (1986). Family socialization of emotional expression and nonverbal communication styles and skills. Journal of Personality and Social Psychology, 51, 827–836. doi:10.1037//0022-3514.51.4.827CrossRefGoogle Scholar
Henckens, M. J., van Wingen, G. A., Joëls, M., & Fernández, G. (2012). Time-dependent effects of cortisol on selective attention and emotional interference: A functional MRI study. Frontiers in Integrative Neuroscience, 6, 66. doi:10.3389/fnint.2012.00066CrossRefGoogle ScholarPubMed
Hinnant, J. B., Erath, S. A., & El-Sheikh, M. (2015). Harsh parenting, parasympathetic activity, and development of delinquency and substance use. Journal of Abnormal Psychology, 124, 137–151. doi:10.1037/abn0000026CrossRefGoogle ScholarPubMed
Holochwost, S. J., Gariépy, J. L., Mills-Koonce, W. R., Propper, C. B., Kolacz, J., & Granger, D. A. (2017). Individual differences in the activity of the hypothalamic pituitary adrenal axis: Relations to age and cumulative risk in early childhood. Psychoneuroendocrinology, 81, 36–45. doi:10.1016/j.psyneuen.2017.03.023CrossRefGoogle ScholarPubMed
Johnson, P. L., & O'Leary, K. D. (1987). Parental behavior patterns and conduct problems in girls. Journal of Abnormal Child Psychology, 15, 573–581. doi:10.1007/bf00917242CrossRefGoogle Scholar
Juster, R. P., McEwen, B. S., & Lupien, S. J. (2010). Allostatic load biomarkers of chronic stress and impact on health and cognition. Neuroscience & Biobehavioral Reviews, 35, 2–16. doi:10.1016/j.neubiorev.2009.10.002CrossRefGoogle ScholarPubMed
Juster, R. P., Sindi, S., Marin, M. F., Perna, A., Hashemi, A., Pruessner, J. C., & Lupien, S. J. (2011). A clinical allostatic load index is associated with burnout symptoms and hypocortisolemic profiles in healthy workers. Psychoneuroendocrinology, 36, 797–805. doi:10.1016/j.psyneuen.2010.11.001CrossRefGoogle ScholarPubMed
Kagan, J., & Snidman, N. (1991). Temperamental factors in human development. American Psychologist, 46, 856–862. doi:10.1037//0003-066x.46.8.856CrossRefGoogle ScholarPubMed
Kaufman, A., & Kaufman, N. (1983). Kaufman Assessment Battery for Children. Circle Pines, MN: American Guidance Service.Google Scholar
Kelsey, R. M., & Guethlein, W. (1990). An evaluation of the ensemble averaged impedance cardiogram. Psychophysiology, 27, 24–33. doi:10.1111/j.1469-8986.1990.tb02173.xCrossRefGoogle ScholarPubMed
Kiernan, M., Kraemer, H. C., Winkleby, M. A., King, A. C., & Taylor, C. B. (2001). Do logistic regression and signal detection identify different subgroups at risk? Implications for the design of tailored interventions. Psychological Methods, 6, 35–48. doi:10.1037/1082-989x.6.1.35CrossRefGoogle ScholarPubMed
Kirschbaum, C., Kudielka, B. M., Gaab, J., Schommer, N. C., & Hellhammer, D. H. (1999). Impact of gender, menstrual cycle phase, and oral contraceptives on the activity of the hypothalamus-pituitary-adrenal axis. Psychosomatic Medicine, 61, 154–162. doi:10.1097/00006842-199903000-00006CrossRefGoogle ScholarPubMed
Koole, S. L., & Lakens, D. (2012). Rewarding replications: A sure and simple way to improve psychological science. Perspectives on Psychological Science, 7, 608–614. doi:10.1177/1745691612462586CrossRefGoogle ScholarPubMed
Koss, K. J., Mliner, S. B., Donzella, B., & Gunnar, M. R. (2016). Early adversity, hypocortisolism, and behavior problems at school entry: A study of internationally adopted children. Psychoneuroendocrinology, 66, 31–38. doi:10.1016/j.psyneuen.2015.12.018CrossRefGoogle ScholarPubMed
Kraemer, H. C. (1992). Evaluating medical tests: Objective and quantitative guidelines. Newbury Park, CA: Sage.Google Scholar
Kuhn, M. A., Ahles, J. J., Aldrich, J. T., Wielgus, M. D., & Mezulis, A. H. (2018). Physiological self-regulation buffers the relationship between impulsivity and externalizing behaviors among nonclinical adolescents. Journal of Youth and Adolescence, 47, 829–841. doi:10.1007/s10964-017-0689-1CrossRefGoogle ScholarPubMed
Kukolja, J., Schläpfer, T. E., Keysers, C., Klingmüller, D., Maier, W., Fink, G. R., & Hurlemann, R. (2008). Modeling a negative response bias in the human amygdala by noradrenergic–glucocorticoid interactions. Journal of Neuroscience, 28, 12868–12876. doi:10.1523/jneurosci.3592-08.2008CrossRefGoogle ScholarPubMed
Levine, S., & Mody, T. (2003). The long-term psychobiological consequences of intermittent postnatal separation in the squirrel monkey. Neuroscience & Biobehavioral Reviews, 27, 83–89. doi:10.1016/s0149-7634(03)00011-3CrossRefGoogle ScholarPubMed
López, H. H., Hay, A. C., & Conklin, P. H. (2009). Attractive men induce testosterone and cortisol release in women. Hormones and Behavior, 56, 84–92. doi:10.1016/j.yhbeh.2009.03.004CrossRefGoogle ScholarPubMed
Lovallo, W. R. (2013). Early life adversity reduces stress reactivity and enhances impulsive behavior: Implications for health behaviors. International Journal of Psychophysiology, 90, 8–16. doi:10.1016/j.ijpsycho.2012.10.006CrossRefGoogle ScholarPubMed
Luecken, L. J., Kraft, A., & Hagan, M. J. (2009). Negative relationships in the family-of-origin predict attenuated cortisol in emerging adults. Hormones and Behavior, 55, 412–417. doi:10.1016/j.yhbeh.2008.12.007CrossRefGoogle ScholarPubMed
Lyons, D. M., & Parker, K. J. (2007). Stress inoculation-induced indications of resilience in monkeys. Journal of Traumatic Stress, 20, 423–433. doi:10.1002/jts.20265CrossRefGoogle ScholarPubMed
Macrì, S., Zoratto, F., & Laviola, G. (2011) Early-stress regulates resilience, vulnerability and experimental validity in laboratory rodents through mother-offspring hormonal transfer. Neuroscience & Biobehavioral Reviews, 35, 1534–1543. doi:10.1016/j.neubiorev.2010.12.014CrossRefGoogle ScholarPubMed
Martin, A., Rief, W., Klaiberg, A., & Braehler, E. (2006). Validity of the brief Patient Health Questionnaire mood scale (PHQ-9) in the general population. General Hospital Psychiatry, 28, 71–77. doi:10.1016/j.genhosppsych.2005.07.003CrossRefGoogle Scholar
Masharani, U., Shiboski, S., Eisner, M. D., Katz, P. P., Janson, S. L., Granger, D. A., & Blanc, P. D. (2005). Impact of exogenous glucocorticoid use on salivary cortisol measurements among adults with asthma and rhinitis. Psychoneuroendocrinology, 30, 744–752. doi:10.1016/j.psyneuen.2005.03.003CrossRefGoogle ScholarPubMed
Mazur, A., Susman, E. J., & Edelbrock, S. (1997). Sex difference in testosterone response to a video game contest. Evolution and Human Behavior, 18, 317–326. doi:10.1016/s1090-5138(97)00013-5CrossRefGoogle Scholar
McClelland, G. H., & Judd, C. M. (1993). Statistical difficulties of detecting interactions and moderator effects. Psychological Bulletin, 114, 376–390. doi:10.1037//0033-2909.114.2.376CrossRefGoogle ScholarPubMed
Morin-Major, J. K., Marin, M. F., Durand, N., Wan, N., Juster, R. P., & Lupien, S. J. (2016). Facebook behaviors associated with diurnal cortisol in adolescents: Is befriending stressful? Psychoneuroendocrinology, 63, 238–246. doi:10.1016/j.psyneuen.2015.10.005CrossRefGoogle ScholarPubMed
Munafò, M. R., Nosek, B. A., Bishop, D. V., Button, K. S., Chambers, C. D., du Sert, N. P., … Ioannidis, J. P. (2017). A manifesto for reproducible science. Nature Human Behaviour, 1, 0021. doi:10.1038/s41562-016-0021CrossRefGoogle Scholar
Obradović, J., Bush, N. R., & Boyce, W. T. (2011). The interactive effect of marital conflict and stress reactivity on externalizing and internalizing symptoms: The role of laboratory stressors. Development and Psychopathology, 23, 101–114. doi:10.1017/S0954579410000672CrossRefGoogle ScholarPubMed
Obradović, J., Bush, N. R., Stamperdahl, J., Adler, N. E., & Boyce, W. T. (2010). Biological sensitivity to context: The interactive effects of stress reactivity and family adversity on socioemotional behavior and school readiness. Child Development, 81, 270–289. doi:10.1111/j.1467-8624.2009.01394.xCrossRefGoogle ScholarPubMed
O'Hara, R., Mumenthaler, M. S., Davies, H., Cassidy, E. L., Buffum, M., Namburi, S., … Kraemer, H. C. (2002). Cognitive status and behavioral problems in older hospitalized patients. Annals of General Hospital Psychiatry, 1, 1. doi:10.1186/1475-2832-1-1CrossRefGoogle ScholarPubMed
Oosterman, M., De Schipper, J. C., Fisher, P., Dozier, M., & Schuengel, C. (2010). Autonomic reactivity in relation to attachment and early adversity among foster children. Development and Psychopathology, 22, 109–118. doi:10.1017/s0954579409990290CrossRefGoogle ScholarPubMed
Ouellet-Morin, I., Robitaille, M. P., Langevin, S., Cantave, C., Brendgen, M., & Lupien, S. J. (2018). Enduring effect of childhood maltreatment on cortisol and heart rate responses to stress: The moderating role of severity of experiences. Development and Psychopathology. Advance online publication. doi:10.1017/s0954579418000123Google ScholarPubMed
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, 933–941. doi:10.1001/archpsyc.61.9.933CrossRefGoogle ScholarPubMed
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, 1466–1483. doi:10.1016/j.neubiorev.2010.09.003CrossRefGoogle ScholarPubMed
Peckins, M. K., Dockray, S., Eckenrode, J. L., Heaton, J., & Susman, E. J. (2012). The longitudinal impact of exposure to violence on cortisol reactivity in adolescents. Journal of Adolescent Health, 51, 366–372. doi:10.1016/j.jadohealth.2012.01.005CrossRefGoogle ScholarPubMed
Peckins, M. K., Susman, E. J., Negriff, S., Noll, J., & Trickett, P. K. (2015). Cortisol profiles: A test for adaptive calibration of the stress response system in maltreated and nonmaltreated youth. Development and Psychopathology, 27, 1461–1470. doi:10.1017/s0954579415000875CrossRefGoogle ScholarPubMed
Porges, S. W. (2007). The polyvagal perspective. Biological Psychology, 74, 116–143. doi:10.1016/j.biopsycho.2006.06.009CrossRefGoogle ScholarPubMed
Porter, B., & O'Leary, K. D. (1980). Marital discord and childhood behavior problems. Journal of Abnormal Child Psychology, 8, 287–295. doi:10.1007/bf00916376CrossRefGoogle ScholarPubMed
Quas, J. A., Yim, I. S., Oberlander, T. F., Nordstokke, D., Essex, M. J., Armstrong, J. M., … Boyce, W. T. (2014). The symphonic structure of childhood stress reactivity: Patterns of sympathetic, parasympathetic, and adrenocortical responses to psychological challenge. Development and Psychopathology, 26, 963–982. doi:10.1017/s0954579414000480CrossRefGoogle ScholarPubMed
Radloff, L. S. (1977). The CES–D scale: A self-report depression scale for research in the general population. Applied Psychological Measurement, 1, 385–401. doi:10.1177/014662167700100306CrossRefGoogle Scholar
Rickel, A. U., & Biasatti, L. L. (1982). Modification of the Block Child Rearing Practice Report. Journal of Clinical Psychology, 38, 129–133. doi:10.1002/1097-4679(198201)38:1<129::aid-jclp2270380120>3.0.co;2-33.0.CO;2-3>CrossRefGoogle Scholar
Roney, J. R., Lukaszewski, A. W., & Simmons, Z. L. (2007). Rapid endocrine responses of young men to social interactions with young women. Hormones and Behavior, 52, 326–333. doi:10.1016/j.yhbeh.2007.05.008CrossRefGoogle ScholarPubMed
Rudolph, C. D., Rudolph, A. M., Hostetter, M. K., Lister, G. L., & Siegel, N. J. (2003). Rudolph's pediatrics (21st ed.). New York: McGraw-Hill Medical.Google Scholar
Rutter, M. (1987). Psychosocial resilience and protective mechanisms. American Journal of Orthopsychiatry, 57, 316–331. doi:10.1111/j.1939-0025.1987.tb03541.xCrossRefGoogle ScholarPubMed
Seery, M. D., Holman, E. A., & Silver, R. C. (2010). Whatever does not kill us: Cumulative lifetime adversity, vulnerability, and resilience. Journal of Personality and Social Psychology, 99, 1025–1041. doi:10.1037/a0021344CrossRefGoogle Scholar
Shader, T. M., Gatzke-Kopp, L. M., Crowell, S. E., Reid, M. J., Thayer, J. F., Vasey, M. W., … Beauchaine, T. P. (2018). Quantifying respiratory sinus arrhythmia: Effects of misspecifying breathing frequencies across development. Development and Psychopathology, 30, 351–366. doi:10.1017/s0954579417000669CrossRefGoogle ScholarPubMed
Shirtcliff, E. A., Skinner, M. L., Obasi, E. M., & Haggerty, K. P. (2017). Positive parenting predicts cortisol functioning six years later in young adults. Developmental Science, 20, e12461. doi:10.1111/desc.12461CrossRefGoogle ScholarPubMed
Spielberger, C. D. (1988). Manual for the State-Trait Anger Expression Inventory (STAXI). Odessa, FL: Psychological Assessment Resources.Google Scholar
Strine, T. W., Mokdad, A. H., Balluz, L. S., Gonzalez, O., Crider, R., Berry, J. T., & Kroenke, K. (2008). Depression and anxiety in the United States: Findings from the 2006 behavioral risk factor surveillance system. Psychiatric Services, 59, 1383–1390. doi:10.1176/appi.ps.59.12.1383CrossRefGoogle ScholarPubMed
Suurland, J., van der Heijden, K. B., Huijbregts, S. C. J., Van Goozen, S. H. M., & Swaab, H. (2018). Infant parasympathetic and sympathetic activity during baseline, stress and recovery: Interactions with prenatal adversity predict physical aggression in toddlerhood. Journal of Abnormal Child Psychology, 46, 755–768. doi:10.1007/s10802-017-0337-yCrossRefGoogle ScholarPubMed
Swets, J. A. (1972). Signal detection in medical diagnosis. In Computer diagnosis and diagnostic methods (pp. 8–28). Springfield, IL: Thomas.Google Scholar
Taylor, Z. E., Spinrad, T. L., VanSchyndel, S. K., Eisenberg, N., Huynh, J., Sulik, M. J., & Granger, D. A. (2013). Sociodemographic risk, parenting, and effortful control: Relations to salivary alpha-amylase and cortisol in early childhood. Developmental Psychobiology, 55, 869–880. doi:10.1002/dev.21079CrossRefGoogle ScholarPubMed
Ursache, A., & Blair, C. (2015). Children's cortisol and salivary alpha-amylase interact to predict attention bias to threatening stimuli. Physiology & Behavior, 138, 266–272. doi:10.1016/j.physbeh.2014.10.002CrossRefGoogle ScholarPubMed
van de Wiel, N. M. H., Van Goozen, S. H. M., 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, 1011–1018. doi:10.1097/01.chi.0000126976.56955.43CrossRefGoogle ScholarPubMed
van Honk, J., Tuiten, A., van den Hout, M., Koppeschaar, H., Thijssen, J., de Haan, E., & Verbaten, R. (2000). Conscious and preconscious selective attention to social threat: Different neuroendocrine response patterns. Psychoneuroendocrinology, 25, 577–591. doi:10.1016/s0306-4530(00)00011-1CrossRefGoogle ScholarPubMed
Vilagut, G., Forero, C. G., Barbaglia, G., & Alonso, J. (2016). Screening for depression in the general population with the center for epidemiologic studies depression (CES-D): A systematic review with meta-analysis. PLOS ONE, 11, e0155431. doi:10.1371/journal.pone.0155431CrossRefGoogle ScholarPubMed
Wilsmer Fries, A. B., Shirtcliff, E. A., & Pollak, S. D. (2008). Neuroendocrine dysregulation following early social deprivation in children. Developmental Psychobiology, 50, 588–599. doi:10.1002/dev.20319CrossRefGoogle ScholarPubMed
Yesavage, J. A., Hoblyn, J., Sheikh, J., Tinklenberg, J. R., Noda, A., O'Hara, R., … Kraemer, H. C. (2003). Age and disease severity predict choice of atypical neuroleptic: A signal detection approach to physicians’ prescribing decisions. Journal of Psychiatric Research, 37, 535–538. doi:10.1016/s0022-3956(03)00053-0CrossRefGoogle ScholarPubMed
Yesavage, J. A., Jo, B., Adamson, M. M., Kennedy, Q., Noda, A., Hernandez, B., … Murphy, G. M. Jr. (2011). Initial cognitive performance predicts longitudinal aviator performance. Journals of Gerontology Series B: Psychological Sciences and Social Sciences, 66, 444–453. doi:10.1093/geronb/gbr031CrossRefGoogle ScholarPubMed
Zhang, W., Fagan, S. E., & Gao, Y. (2017). Respiratory sinus arrhythmia activity predicts internalizing and externalizing behaviors in non-referred boys. Frontiers in Psychology, 8, 1496. doi:10.3389/fpsyg.2017.01496CrossRefGoogle ScholarPubMed
Zwaan, R. A., Etz, A., Lucas, R. E., & Donnellan, M. B. (2017). Making replication mainstream. Behavioral and Brain Sciences, 41, 1–50. doi:10.1017/s0140525×17001972Google Scholar
Zweig, M. H., & Campbell, G. (1993). Receiver-operating characteristic (ROC) plots: A fundamental evaluation tool in clinical medicine. Clinical Chemistry, 39, 561–577.CrossRefGoogle ScholarPubMed
Supplementary material: File

Shakiba et al. supplementary material

Shakiba et al. supplementary material 1

Download Shakiba et al. supplementary material(File)
File 144.2 KB