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The symphonic structure of childhood stress reactivity: Patterns of sympathetic, parasympathetic, and adrenocortical responses to psychological challenge

Published online by Cambridge University Press:  09 June 2014

Jodi A. Quas ,
Ilona S. Yim ,
Tim F. Oberlander ,
David Nordstokke ,
Marilyn J. Essex ,
Jeffrey M. Armstrong ,
Nicole Bush ,
Jelena Obradović  and
W. Thomas Boyce
Jodi A. Quas*
Affiliation:
University of California–Irvine
Ilona S. Yim
Affiliation:
University of California–Irvine
Tim F. Oberlander
Affiliation:
University of British Columbia
David Nordstokke
Affiliation:
University of British Columbia
Marilyn J. Essex
Affiliation:
University of Wisconsin–Madison
Jeffrey M. Armstrong
Affiliation:
University of Wisconsin–Madison
Nicole Bush
Affiliation:
University of California–San Francisco
Jelena Obradović
Affiliation:
Stanford University
W. Thomas Boyce
Affiliation:
University of California–San Francisco
*
Address correspondence and reprint requests to: Jodi Quas, Department of Psychology and Social Behavior, University of California, Irvine, CA 92697-7085; E-mail: [email protected].
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Abstract

Despite widespread recognition that the physiological systems underlying stress reactivity are well coordinated at a neurobiological level, surprisingly little empirical attention has been given to delineating precisely how the systems actually interact with one another when confronted with stress. We examined cross-system response proclivities in anticipation of and following standardized laboratory challenges in 664 4- to 14-year-olds from four independent studies. In each study, measures of stress reactivity within both the locus coeruleus-norepinephrine system (i.e., the sympathetic and parasympathetic branches of the autonomic nervous system) and the corticotrophin releasing hormone system (i.e., the hypothalamic–pituitary–adrenal axis) were collected. Latent profile analyses revealed six distinctive patterns that recurred across the samples: moderate reactivity (average cross-system activation; 52%–80% of children across samples), parasympathetic-specific reactivity (2%–36%), anticipatory arousal (4%–9%), multisystem reactivity (7%–14%), hypothalamic–pituitary–adrenal axis specific reactivity (6%–7%), and underarousal (0%–2%). Groups meaningfully differed in socioeconomic status, family adversity, and age. Results highlight the sample-level reliability of children's neuroendocrine responses to stress and suggest important cross-system regularities that are linked to development and prior experiences and may have implications for subsequent physical and mental morbidity.

Type
Regular Articles
Information
Development and Psychopathology , Volume 26 , Issue 4pt1 , November 2014 , pp. 963 - 982
Copyright
Copyright © Cambridge University Press 2014 

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References

Alkon, A., Boyce, W. T., Davis, N. V., & Eskenazi, B. (2011). Developmental changes in autonomic nervous system resting and reactivity measures in Latino children from 6 to 60 months of age. Journal of Developmental & Behavioral Pediatrics, 32, 668.CrossRefGoogle ScholarPubMed
Alkon, A., Goldstein, L. H., Smider, N., Essex, M. J., Kupfer, D. J., & Boyce, W. T. (2003). Developmental and contextual influences on autonomic reactivity in young children. Developmental Psychobiology, 42, 64–78.Google Scholar
Altshuler, J. L., & Ruble, D. N. (1989). Developmental changes in children's awareness of strategies for coping with uncontrollable stress. Child Development, 60, 1337–1349.Google Scholar
Bauer, A. M., Quas, J. A., & Boyce, W. T. (2002). Associations between physiological reactivity and children's behavior: Advantages of a multisystem approach. Journal of Developmental & Behavioral Pediatrics, 23, 102.CrossRefGoogle ScholarPubMed
Beauchaine, T. P. (2009). Some difficulties in interpreting psychophysiological research with children. Monographs of the Society for Research in Child Development, 74, 80–88.Google Scholar
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.CrossRefGoogle ScholarPubMed
Beauchaine, T. P., Neuhaus, E., Brenner, S. L., & Gatzke-Kopp, L. (2010). Ten good reasons to consider biological processes in prevention and intervention research. Development and Psychopathology, 20, 745.CrossRefGoogle Scholar
Berntson, G. G., Cacioppo, J. T., & Quigley, K. S. (1993). Cardiac psychophysiology and autonomic space in humans: Empirical perspectives and conceptual implications. Psychological Bulletin, 114, 296.CrossRefGoogle ScholarPubMed
Berntson, G. G., Cacioppo, J. T., Quigley, K. S., & Fabro, V. T. (1994). Autonomic space and psychophysiological response. Psychophysiology, 31, 44–61.Google Scholar
Berntson, G. G., Uchino, B. N., & Cacioppo, J. T. (1994). Origins of baseline variance and the law of initial values. Psychophysiology, 31, 204–210.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, 271–301.CrossRefGoogle ScholarPubMed
Boyce, W. T., Essex, M. J., Alkon, A., Goldsmith, H. H., Kraemer, H. C., & Kupfer, D. J. (2006). Early father involvement moderates biobehavioral susceptibility to mental health problems in middle childhood. Journal of the American Academy of Child & Adolescent Psychiatry, 45, 1510–1520.Google 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.Google Scholar
Bruce, J., Fisher, P. A., Pears, K. C., & Levine, S. (2009). Morning cortisol levels in preschool-aged foster children: Differential effects of maltreatment type. Developmental Psychobiology, 51, 14–23.Google Scholar
Burt, K. B., & Obradović, J. (2012). The construct of psychophysiological reactivity: Statistical and psychometric issues. Developmental Review, 33, 29–57.CrossRefGoogle Scholar
Buske-Kirschbaum, A., Jobst, S., Psych, D., Wustmans, A., Kirschbaum, C., Rauh, W., et al. (1997). Attenuated free cortisol response to psychosocial stress in children with atopic dermatitis. Psychosomatic Medicine, 59, 419–426.Google Scholar
Cacioppo, J. T., Berntson, G. G., Malarkey, W. B., Kiecolt-Glaser, J. K., Sheridan, J. F., Poehlmann, K. M., et al. (1998). Autonomic, neuroendocrine, and immune responses to psychological stress: The reactivity hypothesis. Annals of the New York Academy of Sciences, 840, 664–673.CrossRefGoogle 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.Google Scholar
Calkins, S. D. (1997). Cardiac vagal tone indices of temperamental reactivity and behavioral regulation in young children. Developmental Psychobiology, 31, 125–135.Google Scholar
Cannon, W. B. (1932). The wisdom of the body. New York: Norton.CrossRefGoogle Scholar
Cicchetti, D. (2010). Resilience under conditions of extreme stress: A multilevel perspective. World Psychiatry, 9, 145–154.CrossRefGoogle Scholar
Cicchetti, D., & Rogosch, F. A. (2001). The impact of child maltreatment and psychopathology on neuroendocrine functioning. Development and Psychopathology, 13, 783–804.Google Scholar
Cicchetti, D., & Rogosch, F. A. (2012). Neuroendocrine regulation and emotional adaptation in the context of child maltreatment. Monographs of the Society for Research in Child Development, 77, 87–95.Google Scholar
Compas, B. E., Connor-Smith, J. K., Saltzman, H., Thomsen, A. H., & Wadsworth, M. E. (2001). Coping with stress during childhood and adolescence: Problems, progress, and potential in theory and research. Psychological Bulletin, 127, 87–127.Google Scholar
Crabbe, J. C., Wahlsten, D., & Dudek, B. C. (1999). Genetics of mouse behavior: Interactions with laboratory environment. Science, 284, 1670–1672.CrossRefGoogle ScholarPubMed
Dahl, R. E., & Gunnar, M. R. (2009). Heightened stress responsiveness and emotional reactivity during pubertal maturation: Implications for psychopathology. Development and Psychopathology, 21, 1–6.CrossRefGoogle ScholarPubMed
Davies, P. T., Sturge-Apple, M. L., Cicchetti, D., Manning, L. G., & Zale, E. (2009). Children's patterns of emotional reactivity to conflict as explanatory mechanisms in links between interpartner aggression and child physiological functioning. Journal of Child Psychology and Psychiatry, 50, 1384–1391.Google Scholar
De Kloet, E., Fitzsimons, C., Datson, N., Meijer, O., & Vreugdenhil, E. (2009). Glucocorticoid signaling and stress-related limbic susceptibility pathway: About receptors, transcription machinery and microRNA. Brain Research, 1293, 129–141.Google Scholar
Del Giudice, M., Benjamin Hinnant, J., Ellis, B. J., & El-Sheikh, M. (2012). Developmental programming of children's physiological responsivity—Adaptive patterns of stress responsivity: A preliminary investigation. Developmental Psychology, 48, 775.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.Google Scholar
Dickerson, S. S., & Kemeny, M. E. (2004). Acute stressors and cortisol responses: A theoretical integration and synthesis of laboratory research. Psychological Bulletin, 130, 355–391. doi:10.1037/0033-2909.130.3.355 Google Scholar
Doussard-Roosevelt, J. A., Montgomery, L. A., & Porges, S. W. (2003). Short-term stability of physiological measures in kindergarten children: Respiratory sinus arrhythmia, heart period, and cortisol. Developmental Psychobiology, 43, 230–242.Google Scholar
El-Sheikh, M., Erath, S. A., Buckhalt, J. A., Granger, D. A., & Mize, J. (2008). Cortisol and children's adjustment: The moderating role of sympathetic nervous system activity. Journal of Abnormal Child Psychology, 36, 601–611.Google Scholar
El-Sheikh, M., Keller, P. S., & Erath, S. A. (2007). Marital conflict and risk for child maladjustment over time: Skin conductance level reactivity as a vulnerability factor. Journal of Abnormal Child Psychology, 35, 715–727.Google Scholar
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.Google Scholar
Essex, M. J., Boyce, W. T., Goldstein, L. H., Armstrong, J. M., Kraemer, H. C., & Kupfer, D. J. (2002). The confluence of mental, physical, social, and academic difficulties in middle childhood: II. Developing the MacArthur Health & Behavior Questionnaire. Journal of the American Academy of Child & Adolescent Psychiatry, 41, 588–603.Google 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.Google Scholar
Essex, M. J., Kraemer, H. C., Armstrong, J. M., Boyce, W. T. B., Goldsmith, H. H., Klein, M. H., et al. (2006). Exploring risk factors for the emergence of children's mental health problems. Archives of General Psychiatry, 63, 1246.CrossRefGoogle ScholarPubMed
Evans, G. W., & Kim, P. (2007). Childhood poverty and health cumulative risk exposure and stress dysregulation. Psychological Science, 18, 953–957.CrossRefGoogle ScholarPubMed
Faes, T. J. C., De Neeling, N. N. D., Kingma, R., TenVoorde, B. J., & Karemaker, J. M. (1995). On the quantification of heart rate changes in autonomic function tests: Relations between measures in beats per minute, seconds and dimensionless ratios. Clinical Science, 89, 557–564.Google Scholar
Forbes, E. E., & Dahl, R. E. (2010). Pubertal development and behavior: Hormonal activation of social and motivational tendencies. Brain and Cognition, 72, 66–72.Google Scholar
Gellman, M., Spitzer, S., Ironson, G., Llabre, M., Saab, P., Pasin, R. D. C., et al. (1990). Posture, place, and mood effects on ambulatory blood pressure. Psychophysiology, 27, 544–551.Google Scholar
Glassman, R. B. (1973). Persistence and loose coupling in living systems. Behavioral Science, 18, 83–98.Google Scholar
Gordis, E. B., Feres, N., Olezeski, C. L., Rabkin, A. N., & Trickett, P. K. (2010). Skin conductance reactivity and respiratory sinus arrhythmia among maltreated and comparison youth: Relations with aggressive behavior. Journal of Pediatric Psychology, 35, 547–558.Google Scholar
Gordis, E. B., Granger, D. A., Susman, E. J., & Trickett, P. K. (2006). Asymmetry between salivary cortisol and alpha-amylase reactivity to stress: Relation to aggressive behavior in adolescents. Psychoneuroendocrinology, 31, 976–987. doi:10.1016/j.psyneuen.2006.05.010 Google Scholar
Gordis, E. B., Granger, D. A., Susman, E. J., & Trickett, P. K. (2008). Salivary alpha amylase–cortisol asymmetry in maltreated youth. Hormones and behavior, 53, 96–103.Google Scholar
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.Google Scholar
Gunnar, M. R., & Herrera, A. M. (2013). The development of stress reactivity: 3. A neurobiological perspective. In The Oxford handbook of developmental psychology: Vol. 2. Self and other (p. 45). Oxford: Oxford University Press.Google Scholar
Gunnar, M. R., & Quevedo, K. (2007). The neurobiology of stress and development. Annual Review of Psychology, 58, 145–173.Google Scholar
Gunnar, M. R., Tout, K., de Haan, M., Pierce, S., & Stanbury, K. (1997). Temperament, social competence, and adrenocortical activity in preschoolers. Developmental Psychobiology, 31, 65–85.3.0.CO;2-S>CrossRefGoogle ScholarPubMed
Gunnar, M. R., Wewerka, S., Frenn, K., Long, J. D., & Griggs, C. (2009). Developmental changes in hypothalamus–pituitary–adrenal activity over the transition to adolescence: Normative changes and associations with puberty. Development and Psychopathology, 21, 69–85.Google Scholar
Harkness, K. L., Stewart, J. G., & Wynne-Edwards, K. E. (2011). Cortisol reactivity to social stress in adolescents: Role of depression severity and child maltreatment. Psychoneuroendocrinology, 36, 173–181.Google Scholar
Hastings, P. D., Shirtcliff, E. A., Klimes-Dougan, B., Allison, A. L., Derose, L., Kendziora, K. T., et al. (2011). Allostasis and the development of internalizing and externalizing problems: Changing relations with physiological systems across adolescence. Development and Psychopathology, 23, 1149.Google Scholar
Heim, C., & Nemeroff, C. B. (1999). The impact of early adverse experiences on brain systems involved in the pathophysiology of anxiety and affective disorders. Biological Psychiatry, 46, 1509–1522.Google Scholar
Hertzman, C., & Boyce, T. (2010). How experience gets under the skin to create gradients in developmental health. Annual Review of Public Health, 31, 329–347.Google Scholar
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.Google Scholar
Johnson, P. L., & O'Leary, K. D. (1987). Parental behavior pattern and conduct problems in girls. Journal of Abnormal Child Psychology, 15, 573–581.Google Scholar
Kagan, J. (2011). Three lessons learned. Perspectives on Psychological Science, 6, 107–113.CrossRefGoogle ScholarPubMed
Kirschbaum, C., & Hellhammer, D. H. (1994). Salivary cortisol in psychoneuroendocrine research: Recent developments and applications. Psychoneuroendocrinology, 19, 313–333.Google Scholar
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, 76–81. doi:10.1159/000119004 Google Scholar
Klein, M. H., Hyde, J. S., Essex, M. J., & Clark, R. (1998). Maternity leave, role quality, work involvement, and mental health one year after delivery. Psychology of Women Quarterly, 22, 239–266.CrossRefGoogle Scholar
Koss, K. J., George, M. R. W., Cummings, E. M., Davies, P. T., El-Sheikh, M., & Cicchetti, D. (2013). Asymmetry in children's salivary cortisol and alpha-amylase in the context of marital conflict: Links to children's emotional security and adjustment. Developmental Psychobiology. Advance online publication.Google Scholar
Kroenke, C. H., Epel, E., Adler, N., Bush, N. R., Obradović, J., Lin, J., et al. (2011). Autonomic and adrenocortical reactivity and buccal cell telomere length in kindergarten children. Psychosomatic Medicine, 73, 533–540.Google Scholar
Kudel, I., Farber, S. L., Mrus, J. M., Leonard, A. C., Sherman, S. N., & Tsevat, J. (2006). Patterns of responses on health-related quality of life questionnaires among patients with HIV/AIDS. Journal of General Internal Medicine, 21, S48–S55.Google Scholar
Kudielka, B., Buske-Kirschbaum, A., Hellhammer, D., & Kirschbaum, C. (2004). HPA axis responses to laboratory psychosocial stress in healthy elderly adults, younger adults, and children: Impact of age and gender. Psychoneuroendocrinology, 29, 83–98.Google Scholar
Lewejohann, L., Reinhard, C., Schrewe, A., Brandewiede, J., Haemisch, A., Görtz, N., et al. (2006). Environmental bias? Effects of housing conditions, laboratory environment and experimenter on behavioral tests. Genes, Brain and Behavior, 5, 64–72.Google Scholar
Lisonbee, J. A., Pendry, P., Mize, J., & Gwynn, E. P. (2010). Hypothalamic–pituitary–adrenal and sympathetic nervous system activity and children's behavioral regulation. Mind, Brain, and Education, 4, 171–181.Google Scholar
Loman, M. M., & Gunnar, M. R. (2010). Early experience and the development of stress reactivity and regulation in children. Neuroscience & Biobehavioral Reviews, 34, 867–876.Google Scholar
Lovallo, W. (1975). The cold pressor test and autonomic function: A review and integration. Psychophysiology, 12, 268–282.Google Scholar
Lupien, S. J., King, S., Meaney, M. J., & McEwen, B. S. (2001). Can poverty get under your skin? Basal cortisol levels and cognitive function in children from low and high socioeconomic status. Development and Psychopathology, 13, 653–676.Google Scholar
Lupien, S. J., McEwen, B. S., Gunnar, M. R., & Heim, C. (2009). Effects of stress throughout the life span on the brain, behaviour and cognition. Nature Reviews Neuroscience, 10, 434–445.Google Scholar
McEwen, B. S. (1998). Seminars in medicine of the Beth Israel Deaconess Medical Center: Protective and damaging effects of stress mediators. New England Journal of Medicine, 338, 171–179.Google Scholar
McEwen, B. S. (2006). Protective and damaging effects of stress mediators: Central role of the brain. Dialogues in Clinical Neuroscience, 8, 367.Google Scholar
McEwen, B. S., & Gianaros, P. J. (2010). Central role of the brain in stress and adaptation: Links to socioeconomic status, health, and disease. Annals of the New York Academy of Sciences, 1186, 190–222.Google Scholar
McEwen, B. S., & Stellar, E. (1993). Stress and the individual: Mechanisms leading to disease. Archives of Internal Medicine, 153, 2093.Google Scholar
Miller, G. E., Chen, E., Fok, A. K., Walker, H., Lim, A., Nicholls, E. F., et al. (2009). Low early-life social class leaves a biological residue manifested by decreased glucocorticoid and increased proinflammatory signaling. Proceedings of the National Academy of Sciences, 106, 14716–14721.Google Scholar
Muthén, B. (2008). Latent variable hybrids: Overview of old and new models. Advances in Latent Variable Mixture Models, 1, 1–24.Google Scholar
Nagin, D. S., & Odgers, C. L. (2010). Group-based trajectory modeling in clinical research. Annual Review of Clinical Psychology, 6, 109–138. doi:10.1146/annurev.clinpsy.121208.131413 Google Scholar
Natsuaki, M. N., Klimes-Dougan, B., Ge, X., Shirtcliff, E. A., Hastings, P. D., & Zahn-Waxler, C. (2009). Early pubertal maturation and internalizing problems in adolescence: Sex differences in the role of cortisol reactivity to interpersonal stress. Journal of Clinical Child & Adolescent Psychology, 38, 513–524.CrossRefGoogle ScholarPubMed
Nylund, K. L., Asparouhov, T., & Muthén, B. O. (2007). Deciding on the number of classes in latent class analysis and growth mixture modeling: A Monte Carlo simulation study. Structural Equation Modeling, 14, 535–569.Google Scholar
Obradović, J. (2012). How can the study of physiological reactivity contribute to our understanding of adversity and resilience processes in development? Development and Psychopathology, 24, 371–387.Google 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.Google Scholar
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.Google Scholar
Porges, S. W. (2007). The polyvagal perspective. Biological Psychology, 74, 116–143.Google Scholar
Porter, B., & O'Leary, K. D. (1980). Marital discord and childhood behavior problems. Journal of Abnormal Psychology, 8, 287–295.Google Scholar
Quas, J. A., Carrick, N., Alkon, A., Goldstein, L., & Boyce, W. T. (2006). Children's memory for a mild stressor: The role of sympathetic activation and parasympathetic withdrawal. Developmental Psychobiology, 48, 686–702. doi:10.1002/dev.20184 Google Scholar
Quas, J. A., Murowchick, E., Bensadoun, J. r., & Boyce, W. T. (2002). Predictors of children's cortisol activation during the transition to kindergarten. Journal of Developmental & Behavioral Pediatrics, 23, 304–313.Google Scholar
Quas, J. A., Yim, I. S., Edelstein, R. S., Cahill, L., & Rush, E. B. (2011). The role of cortisol reactivity in children's and adults’ memory of a prior stressful experience. Developmental Psychobiology, 53, 166–174. doi:10.1002/dev.20505 Google Scholar
Quevedo, K., Johnson, A. E., Loman, M. L., LaFavor, T. L., & Gunnar, M. (2012). The confluence of adverse early experience and puberty on the cortisol awakening response. International Journal of Behavioral Development, 36, 19–28.Google Scholar
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.CrossRefGoogle Scholar
Raine, A. (2002). Biosocial studies of antisocial and violent behavior in children and adults: A review. Journal of Abnormal Child Psychology, 30, 311–326.Google Scholar
Rogosch, F. A., Dackis, M. N., & Cicchetti, D. (2011). Child maltreatment and allostatic load: Consequences for physical and mental health in children from low-income families. Development and Psychopathology, 23, 1107.Google Scholar
Roozendaal, B., Hahn, E. L., Nathan, S. V., Dominique, J. F., & McGaugh, J. L. (2004). Glucocorticoid effects on memory retrieval require concurrent noradrenergic activity in the hippocampus and basolateral amygdala. Journal of Neuroscience, 24, 8161–8169.Google Scholar
Ruble, D. N., Boggiano, A. K., Feldman, N. S., & Loebl, J. H. (1980). Developmental analysis of the role of social comparison in self-evaluation. Developmental Psychology, 16, 105.Google Scholar
Salomon, K., Matthews, K. A., & Allen, M. T. (2000). Patterns of sympathetic and parasympathetic reactivity in a sample of children and adolescents. Psychophysiology, 37, 842–849.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, 21, 55–89.Google Scholar
Shirtcliff, E. A., & Essex, M. J. (2008). Concurrent and longitudinal associations of basal and diurnal cortisol with mental health symptoms in early adolescence. Developmental Psychobiology, 50, 690–703.Google Scholar
Shirtcliff, E. A., Granger, D. A., Booth, A., & Johnson, D. (2005). Low salivary cortisol levels and externalizing behavior problems in youth. Development and Psychopathology, 17, 167–184.Google Scholar
Tarullo, A. R., & Gunnar, M. R. (2006). Child maltreatment and the developing HPA axis. Hormones and Behavior, 50, 632–639.Google Scholar
Taylor, S. E., Lerner, J. S., Sage, R. M., Lehman, B. J., & Seeman, T. E. (2004). Early environment, emotions, responses to stress, and health. Journal of Personality, 72, 1365–1394.Google Scholar
Torpy, D. J., & Chrousos, G. P. (1996). The three-way interactions between the hypothalamic–pituitary–adrenal and gonadal axes and the immune system. Bailliere's Clinical Rheumatology, 10, 181.Google Scholar
Weiner, H. (1992). Perturbing the organism: The biology of stressful experience. Chicago: University of Chicago Press.Google Scholar
Wilder, J. (1958). Modern psychophysiology and the law of initial value. American Journal of Psychotherapy, 12, 199–221.Google Scholar
Yim, I. S., Quas, J. A., Cahill, L., & Hayakawa, C. M. (2010). Children's and adults’ salivary cortisol responses to an identical psychosocial laboratory stressor. Psychoneuroendocrinology, 35, 241–248. doi:10.1016/j.psyneuen.2009.06.014 Google Scholar
Zimmer-Gembeck, M. J., & Skinner, E. A. (2011). Review: The development of coping across childhood and adolescence: An integrative review and critique of research. International Journal of Behavioral Development, 35, 1–17.Google Scholar