Hostname: page-component-586b7cd67f-tf8b9 Total loading time: 0 Render date: 2024-11-29T11:38:07.495Z Has data issue: false hasContentIssue false
  • English
  • Français

Allostasis and the development of internalizing and externalizing problems: Changing relations with physiological systems across adolescence

Published online by Cambridge University Press:  21 October 2011

Paul D. Hastings ,
Elizabeth A. Shirtcliff ,
Bonnie Klimes-Dougan ,
Amber L. Allison ,
Laura Derose ,
Kimberley T. Kendziora ,
Barbara A. Usher  and
Carolyn Zahn-Waxler
Paul D. Hastings*
Affiliation:
University of California, Davis
Elizabeth A. Shirtcliff
Affiliation:
University of New Orleans
Bonnie Klimes-Dougan
Affiliation:
University of Minnesota
Amber L. Allison
Affiliation:
University of New Orleans
Laura Derose
Affiliation:
Adelphi University
Kimberley T. Kendziora
Affiliation:
American Institutes for Research
Barbara A. Usher
Affiliation:
National Institute on Drug Abuse
Carolyn Zahn-Waxler
Affiliation:
University of Wisconsin
*
Address correspondence and reprint requests to: Paul D. Hastings, University of California Davis, Center for Mind & Brain, 267 Cousteau Place, Davis, CA 95618; E-mail: [email protected].
Get access Rights & Permissions [Opens in a new window]

Abstract

Allostasis, or the maintenance of stability through physiological change, refers to the process by which individuals adjust to the continually changing demands that are put upon somatic activity by salient events. Bauer and colleagues proposed that allostasis could be detected through patterns of the joint reactivity of the autonomic nervous system (ANS) and hypothalamic–pituitary–adrenal (HPA) axis system under stressful conditions. We examined the associations between ANS and HPA reactivity and the development of externalizing and internalizing problems over 2 years in a sample of 215 adolescents. The interactions of ANS and HPA reactivity were contemporaneously associated with, and longitudinally predictive of, adolescents' emotional and behavioral problems. Adolescents with symmetrical high reactivity across systems had more internalizing and fewer externalizing problems initially. Over time, both symmetrical and asymmetrical reactivity predicted increasing internalizing problems in girls, depending on the measure of ANS activity that was examined, heart rate, or blood pressure reactivity. Implications for the understanding of allostasis and the dynamic nature of the relations between multiple physiological regulatory systems and adolescents' developing psychopathology are discussed.

Type
Articles
Information
Development and Psychopathology , Volume 23 , Issue 4: Allostatic Load: Part 2 , November 2011 , pp. 1149 - 1165
Copyright
Copyright © Cambridge University Press 2011

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

Achenbach, T. M. (1991a). Manual for the Child Behavior Checklist/4–18 and 1991 profile. Burlington, VT: University of Vermont, Department of Psychiatry.Google Scholar
Achenbach, T. M. (1991b). Manual for the Youth Self-Report and 1991 profile. Burlington, VT: University of Vermont, Department of Psychiatry.Google Scholar
Adam, E. K., Doane, L. D., Zinbarg, R. E., Mineka, S., Craske, M. G., & Griffith, J. W. (2010). Prospective prediction of major depressive disorder from cortisol awakening responses in adolescence. Psychoneuroendocrinology, 35, 921–931.CrossRefGoogle ScholarPubMed
Alink, L. R. A., 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, 427–450.CrossRefGoogle ScholarPubMed
Angold, A., Costello, E. J., & Erkanli, A. (1999). Comorbidity. Journal of Child Psychology and Psychiatry, 40, 57–87.CrossRefGoogle ScholarPubMed
Basset, J. R., Marshall, P. M., & Spillane, R. (1987). The physiological measurement of acute stress (public speaking) in bank employees. International Journal of Psychophysiology, 5, 265–273.CrossRefGoogle Scholar
Bauer, A. M., Boyce, W. T., & Quas, J. A. (2002). Associations between physiological reactivity and children's behavior: Advantages of a multisystem approach. Developmental and Behavioral Pediatrics, 23, 102–113.CrossRefGoogle ScholarPubMed
Beauchaine, T. P. (in press). Physiological markers of emotional and behavioral dysregulation in externalizing psychopathology. Monographs of the Society for Research in Child Development.Google Scholar
Beauchaine, T. P., Hong, J., & Marsh, P. (2008). Sex differences in autonomic correlates of conduct problems and aggression. Journal of the American Academy of Child & Adolescent Psychiatry, 47, 788–796.CrossRefGoogle ScholarPubMed
Bernston, G. G., Bechara, A., Damasio, H., Tranel, D., & Cacioppo, J. T. (2007). Amygdala contribution to selective dimensions of emotion. Social Cognitive and Affective Neuroscience, 2, 123–129.Google Scholar
Berntson, G. G., & Cacioppo, J. T. (2007). Integrative physiology: Homeostasis, allostasis, and the orchestration of systemic physiology. In Cacioppo, J. T., Tassinary, L. G., & Berntson, G. G. (Eds.), Handbook of psychophysiology (pp. 433–452). New York: Cambridge University Press.CrossRefGoogle Scholar
Berntson, G. G., Cacioppo, J. T., & Quigley, K. S. (1991). Autonomic determinism: The modes of autonomic control, the doctrine of autonomic space, and the laws of autonomic constraint. Psychological Review, 98, 459–487.CrossRefGoogle ScholarPubMed
Berntson, G. G., Quigley, K. S., & Lozano, D. (2007). Cardiovascular psychophysiology. In Cacioppo, J. T., Tassinary, L. G., & Berntson, G. G. (Eds.), Handbook of psychophysiology (pp. 182–210). New York: Cambridge University Press.CrossRefGoogle 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
Brownley, K. A., Hurwitz, B. E., & Schneiderman, N. (2000). Cardiovascular psychophysiology. In Cacioppo, J. T., Tassinary, L. G., & Bernston, G. G. (Eds.), Handbook of psychophysiology (pp. 224–264). New York: Cambridge University Press.Google Scholar
Buss, K. A., Davidson, R. J., Kalin, N. H., & Goldsmith, H.H. (2004). Context-specific freezing and associated physiological reactivity as a dysregulated fear response. Developmental Psychology, 40, 583–594.CrossRefGoogle ScholarPubMed
Charkoudian, N., & Rabbitts, J. A. (2009). Sympathetic neural mechanisms in human cardiovascular health and disease. Mayo Clinic Proceedings, 84, 822–830.CrossRefGoogle ScholarPubMed
Chrousos, G. P., & Gold, P. W. (1992). The concepts of stress and stress system disorders. Overview of physical and behavioral homeostasis. Journal of the American Medical Association, 267, 1244–1252.CrossRefGoogle ScholarPubMed
Cicchetti, D. (2008). A multiple-levels-of-analysis perspective on research in development and psychopathology. In Beauchaine, T. P. & Hinshaw, S. P. (Eds.), Child and adolescent psychopathology (pp. 27–57). Hoboken, NJ: Wiley.Google Scholar
Cicchetti, D., & Curtis, W.J. (2007). Multilevel perspectives on pathways to resilient functioning. Development and Psychopathology, 19, 627–629.CrossRefGoogle ScholarPubMed
Cicchetti, C., & Gunnar, M. R. (2008). Integrating biological measures into the design and evaluation of preventive interventions. Development and Psychopathology, 20, 737–743.CrossRefGoogle ScholarPubMed
Cicchetti, D., & Rogosch, F. A. (in press). Neuroendocrine regulation and emotional adaptation in the context of child maltreatment. Monographs of the Society for Research on Child Development.Google Scholar
Cicchetti, D., & Toth, S. L. (2009). The past achievements and future promises of developmental psychopathology: The coming of age of a discipline. Journal of Child Psychology and Psychiatry, 50, 16–25.CrossRefGoogle ScholarPubMed
Del Guidice, M., Ellis, B. J., & Shirtcliff, E. A. (2011). The adaptive calibration of stress responsivity: An integrative model. Neuroscience and Behavioral Reviews, 35, 1562–1592.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Dietrich, A., Riese, H., Sondeijker, F. E. P. L., Greaves-Lord, K., van Roon, A. M., Ormel, J., et al. (2007). Externalizing and internalizing problems in relations to autonomic function: A population-based study in preadolescents. Journal of the American Academy of Child & Adolescent Psychiatry, 46, 378–386.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Dunn, A. J., & Berridge, C. W. (1990). Physiological and behavioral responses to corticotrophin-releasing factor administration: Is CRF a mediator of anxiety or stress responses? Brain Research Reviews, 15, 71–100.CrossRefGoogle ScholarPubMed
El-Sheikh, M., Erath, S., 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.CrossRefGoogle ScholarPubMed
Essex, M. J., Klein, M. H., Cho, E., & Kraemer, H. C. (2003). Exposure to maternal depression and marital conflict: Gender differences in children's later mental health symptoms. Journal of the American Academy of Child & Adolescent Psychiatry, 42, 728–737.CrossRefGoogle ScholarPubMed
Evans, G. W., Kim, P., Ting, A. H., Tesher, H. B., & Shannis, D. (2007). Cumulative risk, maternal responsiveness, and allostatic load among young adolescents. Developmental Psychology, 43, 341–351.CrossRefGoogle ScholarPubMed
Fairchild, G., van Goozen, S. H. M., Stollery, S. J., Brown, J., Gardiner, J., Herbert, J., et al. (2008). Cortisol diurnal rhythm and stress reactivity in male adolescents with early-onset or adolescence-onset conduct disorder. Biological Psychiatry, 64, 599–606.CrossRefGoogle ScholarPubMed
Fortunato, C. K., Dribin, A. E., Granger, D. A., & Buss, K. A. (2008). Salivary alpha-amylase and cortisol in toddlers: Differential relations to affective behavior. Developmental Psychobiology, 50, 807–818.CrossRefGoogle ScholarPubMed
Gentzler, A. L., Santucci, A. K, Kovacs, M., & Fox, N. A. (2009). Respiratory sinus arrhythmia reactivity predicts emotion regulation and depressive symptoms in at-risk and control children. Biological Psychology, 82, 156–163.CrossRefGoogle ScholarPubMed
Girdler, S. S., Pedersen, C. A., Straneva, P. A., Lesermen, J., Stanwyck, C. L., Benjamin, S., et al. (1998). Dysregulation of cardiovascular and neuroendocrine responses to stress in premenstrual dysphoric disorder. Psychiatry Research, 81, 163–178.CrossRefGoogle ScholarPubMed
Gordis, E. B., Granger, D. A., Susman, E. J., & Trickett, P. K. (2006). Asymmetry between salivary cortisol and α-amylase reactivity to stress: Relation to aggressive behavior in adolescents. Psychoneuroendocrinology, 31, 976–987.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Gottlieb, G. (1996). Developmental psychobiological theory. In Cairns, R. B., Elder, G. H., & Costello, A. (Eds.), Developmental science (pp. 63–96). Cambridge: Cambridge University Press.CrossRefGoogle Scholar
Granger, D. A., Shirtcliff, E. A., Zahn-Waxler, C., Usher, B., Klimes-Dougan, B., & Hastings, P.D. (2003). Salivary testosterone diurnal variation and psychopathology in adolescent males and females: Individual differences and developmental effects. Development and Psychopathology, 15, 431–449.CrossRefGoogle ScholarPubMed
Granger, D. A., Weisz, J. R., & Kauneckis, D. (1994). Neuroendocrine reactivity, internalizing behavior problems, and control-related cognitions in clinic-referred children and adolescents. Journal of Abnormal Psychology, 103, 267–276.CrossRefGoogle ScholarPubMed
Granger, D. A., Weisz, J. R., McCracken, J. T., & Ikeda, S. C. (1996). Reciprocal influences among adrenocortical activation, psychosocial processes, and the behavioral adjustment of clinic-referred children. Child Development, 67, 3250–3262.CrossRefGoogle ScholarPubMed
Guerry, J. D., & Hastings, P. D. (2011). In search of HPA axis dysregulation in child and adolescent depression. Clinical Child and Family Psychology Review, 14, 135–160.CrossRefGoogle ScholarPubMed
Gump, B. B., Reihman, J., Stewart, P., Lonky, E., Darvill, T., Granger, D. A., et al. (2009). Trajectories of maternal depressive symptoms over her child's life span: Relation to adrenocortical, cardiovascular, and emotional functioning in children. Development and Psychopathology, 21, 207–225.CrossRefGoogle ScholarPubMed
Gunnar, M. R., & Talge, N. M. (2008). Neuroendocrine measures in developmental research. In Schmidt, L. A. & Segalowitz, S. J. (Eds.), Developmental psychophysiology: Theory, systems, and methods (pp. 343–364). New York: Cambridge University Press.Google Scholar
Hankin, B., Mermelstein, R., & Roesch, L. (2007). Sex differences in adolescent depression: Stress exposure and reactivity models. Child Development, 78, 279–295.CrossRefGoogle ScholarPubMed
Hastings, P. D., Nuselovici, J. N., Klimes-Dougan, B., Kendziora, K. T., Usher, B. A., Ho, M. R., et al. (2009). Dysregulated coherence of subjective and cardiac emotional activation in adolescents with internalizing and externalizing problems. Journal of Child Psychology and Psychiatry, 50, 1348–1356.CrossRefGoogle ScholarPubMed
Hastings, P. D., Ruttle, P., Serbin, L. A., Mills, R. S. L., Stack, D.M., & Schwartzman, A.E. (in press). Adrenocortical stress reactivity and regulation in preschoolers: Relations with parenting, temperament, and psychopathology. Developmental Psychobiology.Google Scholar
Hastings, P. D., Zahn-Waxler, C., & Usher, B. A. (2007). Cardiovascular and affective responses to social stress in adolescents with internalizing and externalizing problems. International Journal of Behavioral Development, 31, 77–87.CrossRefGoogle Scholar
Henry, J. P., Haviland, M. G., Cummings, M. A., Anderson, D. L., Nelson, J. C., MacMurray, J. P., et al. (1992). Shared neuroendocrine patterns of post-traumatic stress disorder and alexithymia. Psychosomatic Medicine, 54, 407–415.CrossRefGoogle ScholarPubMed
Hofer, S. M., Horn, J. L., & Eber, H. W. (1997). A robust five-factor structure of the 16PF: Strong evidence from independent rotation and confirmatory factorial invariance procedures. Personality and Individual Differences, 23, 247–269.CrossRefGoogle Scholar
Hollingshead, A. B. (1975). Four Factor Index of Social Status. Unpublished manuscript.Google Scholar
Juster, R. P., McEwen, B. S., & Lupien, S. J. (2010). Allostatic load biomarkers of chronic stress and impact on health and cognition. Neuroscience and Biobehavioral Reviews, 35, 2–16.CrossRefGoogle ScholarPubMed
Kagan, J., Snidman, N., Arcus, D., & Reznick, J. S. (1994). Galen's prophecy: Temperament in human nature. New York: Basic Books.Google Scholar
Kaltas, G. A., & Chrousos, G. P. (2007). The neuroendocrinology of stress. In Cacioppo, J. T., Tassinary, L. G., & Bernston, G. C. (Eds.), Handbook of psychophysiology (pp. 303–318). New York: Cambridge University Press.Google Scholar
Kelly, M. M., Tyrka, A. R., Anderson, G. M., Price, L. H., & Carpenter, L. L. (2008). Sex differences in emotional and physiological responses to the Tier Social Stress Test. Journal of Behavior Therapy and Experimental Psychiatry, 39, 87–98.CrossRefGoogle Scholar
Kirschbaum, C., Pirke, K., & Hellhammer, D. H. (1993). The “Trier Social Stress Test”: A tool for investigating psychobiological stress responses in a laboratory setting. Neuropsychobiology, 28, 76–81.CrossRefGoogle Scholar
Klimes-Dougan, B., Brand, A. E., Zahn-Waxler, C., Usher, B., Hastings, P. D., Kendziora, K., et al. (2007). Parental emotion socialization in adolescence: Differences in sex, age and problem status. Social Development, 16, 326–342.CrossRefGoogle Scholar
Klimes-Dougan, B., Hastings, P. D., Granger, D. A., Usher, B. A., & Zahn-Waxler, C. (2001). Adrenocortical activity in at-risk and normally developing adolescents: Individual differences in salivary cortisol basal levels, diurnal variation, and responses to social challenges. Development and Psychopathology, 13, 695–719.CrossRefGoogle ScholarPubMed
Kraemer, H. C., Measelle, J. R., Ablow, J. C., Essex, M. J., Boyce, W. T., & Kupfer, D. J. (2003). A new approach to integrating data from multiple informants in psychiatric assessment and research: Mixing and matching contexts and perspectives. American Journal of Psychiatry, 160, 1566–1577.CrossRefGoogle Scholar
Kraemer, H. C., Yesavage, J. A., Taylor, J. L., & Kupfer, D. (2000). How can we learn about developmental processes from cross-sectional studies, or can we? American Journal of Psychiatry, 157, 163–171.CrossRefGoogle ScholarPubMed
Kudielka, B. M., Buske-Kirschbaum, A., Hellhammer, D. H., & 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.CrossRefGoogle ScholarPubMed
Lewis, M., Ramsay, D. S., & Sullivan, M. W. (2006). The relation of ANS and HPA activation to infant anger and sadness response to goal blockage. Developmental Psychobiology, 48, 397–405.CrossRefGoogle ScholarPubMed
Lopez-Duran, N. L., Kovacs, M., & George, C. J. (2009). Hypothalamic–pituitary–adrenal axis dysregulation in depressed children and adolescents: A meta-analysis. Psychoneuroendocrinology, 34, 1272–1283.CrossRefGoogle ScholarPubMed
Lorber, M. F. (2004). Psychophysiology of aggression, psychopathy, and conduct problems: A meta analysis. Psychological Bulletin, 130, 531–552.CrossRefGoogle ScholarPubMed
Lovallo, W. R., & Thomas, T. L. (2000). Stress hormones in psychophysiological research: Emotional, behavioral, and cognitive implications. In Cacioppo, J. T., Tassinary, L. G., & Bernston, G. C. (Eds.), Handbook of psychophysiology (pp. 342–367). New York: Cambridge University Press.Google Scholar
Lupien, S. J., Ouellet-Morin, I., Hupbach, A., Tu, M. T., Buss, C., Walker, D., et al. (2006). Beyond the stress concept: Allostatic load—A developmental biological and cognitive perspective. In Cicchetti, D. & Cohen, D. (Eds.), Developmental psychopathology: Vol. 2. Developmental neuroscience (pp. 578–628). New York: Wiley.Google Scholar
Maheu, F. S., Dozier, M., Guyer, A. E., Mandell, D., Peloso, E., Poeth, K., et al. (2010). A preliminary study of medial temporal love function in youths with a history of caregiver deprivation and emotional neglect. Cognitive, Affective, & Behavioral Neuroscience, 10, 34–39.CrossRefGoogle Scholar
Mason, J. W., Giller, E. L., Kosten, T. R., & Harkness, L. (1988). Elevation of urinary norepinephrine/cortisol ratio in posttraumatic stress disorder. Journal of Nervous and Mental Disease, 176, 498–502.CrossRefGoogle ScholarPubMed
Mathew, S. J., Coplan, J. D., Goetz, R. R., Feder, A., Greenwald, S., Dahl, R. E., et al. (2003). Differentiating depressed adolescent 24h cortisol secretion in light of their adult clinical outcome. Neuropsychopharmacology, 28, 1336–1343.CrossRefGoogle ScholarPubMed
McEwen, B. S. (1998). Stress, adaptation, and disease: Allostasis and allostatic load. Annals of the New York Academy of Sciences, 840, 33–44.CrossRefGoogle ScholarPubMed
McEwen, B. S., & Stellar, E. (1993). Stress and the individual: Mechanisms leading to disease. Archives of Internal Medicine, 153, 2093–3101.CrossRefGoogle ScholarPubMed
Merikangas, K. R., Avenevoli, S., Dierker, L., & Grillon, C. (1999). Vulnerability factors among children at risk for anxiety disorders. Biological Psychiatry, 46, 1523–1535.CrossRefGoogle ScholarPubMed
Miller, G. E., Chen, E., & Zhou, E. S. (2007). If it goes up, must it come down? Chronic stress and the hypothalamic–pituitary–adrenocortical axis in humans. Psychological Bulletin, 133, 25–45.CrossRefGoogle ScholarPubMed
Miskovic, V., & Schmidt, L. A. (in press). New directions in the study of individual differences in temperament: A brain–body approach to understanding fearful and fearless children. Monographs of the Society for Research in Child Development.Google Scholar
Munck, A., Guyre, P. M., & Holbrook, N. J. (1984). Physiological functions of glucocorticoids in stress and their relation to pharmacological actions. Endocrinology Reviews, 5, 25–44.CrossRefGoogle ScholarPubMed
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 and Adolescent Psychology, 38, 513–524.CrossRefGoogle ScholarPubMed
Nock, M. K., & Mendes, W. B. (2008). Physiological arousal, distress tolerance, and social problem-solving deficits among adolescent self-injurers. Journal of Consulting and Clinical Psychology, 76, 28–38.CrossRefGoogle ScholarPubMed
Nottelmann, E. D., & Jensen, P. S. (1995). Comorbidity of disorders in children and adolescents: Developmental perspectives. Advances in Clinical Child Psychology, 17, 109–155.CrossRefGoogle Scholar
Obradovic, J., Bush, N. R., Stamperdahl, J., Alder, 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.CrossRefGoogle ScholarPubMed
Ortiz, J., & Raine, A. (2004). Heart rate level and antisocial behavior in children and adolescents: A meta-analysis. Journal of the American Academy of Child & Adolescent Psychiatry, 43, 154–162.CrossRefGoogle ScholarPubMed
Olsson, K. A., Kenardy, J. A., De Young, A. C., & Spence, S. H. (2008). Predicting children's post-traumatic stress symptoms following hospitalization for accidental injury: Combining the Child Trauma Screening Questionnaire and heart rate. Journal of Anxiety Disorders, 22, 1447–1453.CrossRefGoogle ScholarPubMed
Pine, D. S., Coplan, J. D., Papp, L. A., Klein, R. G., Martinez, J. M., & Kovalenko, P. (1998). Ventilatory physiology of children and adolescents with anxiety disorders. Archives of General Psychiatry, 55, 123–129.CrossRefGoogle ScholarPubMed
Popma, A., Jansen, L. M. C., Vermeiren, R., Steiner, H., Raine, A., Van Goozen, S. H. M., et al. (2006). Hypothalamus pituitary adrenal axis and autonomic activity during stress in delinquent male adolescents and controls. Psychoneuroendocrinology, 31, 948–957.CrossRefGoogle ScholarPubMed
Porges, S. W. (2001). The polyvagal theory: Phylogenetic substrates of a social nervous system. International Journal of Psychophysiology, 42, 123–146.CrossRefGoogle ScholarPubMed
Porges, S. W. (2007). The polyvagal perspective. Biological Psychology, 74, 116–143.CrossRefGoogle ScholarPubMed
Quas, J. A., Bauer, A. M., & Boyce, W. T. (2004). Physiological reactivity, social support, and memory in early childhood. Child Development, 75, 797–814.CrossRefGoogle ScholarPubMed
Raine, A. (2008). From genes to brain to antisocial behavior. Current Directions in Psychological Science, 17, 323–328.CrossRefGoogle Scholar
Rao, U., Hammen, C., Ortiz, L. R., Chen, L., & Poland, R. E. (2008). Effects of early and recent adverse experiences on adrenal response to psychosocial stress in depressed adolescents. Biological Psychiatry, 64, 521–526.CrossRefGoogle ScholarPubMed
Robins, R. W., Trzesniewski, K. H., Tracy, J. L., Gosling, S. D., & Potter, J. (2002). Global self-esteem across the lifespan. Psychology and Aging, 17, 423–434.CrossRefGoogle Scholar
Rogeness, G. A, Cepeda, C., Macedo, C. A., Fischer, C., & Harris, W. R. (1990). Differences in heart rate and blood pressure in children with conduct disorder, major depression and separation anxiety. Psychiatry Research, 33, 199–206.CrossRefGoogle ScholarPubMed
Rudolph, K. D., Troop-Gordon, W., & Granger, D. (2010). Peer victimization and aggression: Moderation by individual differences in salivary control and alpha amylase. Journal of Abnormal Child Psychology, 38, 843–856.CrossRefGoogle Scholar
Ruttle, P. L., Shirtcliff, E. A., Serbin, L. A., Fisher, D. B., & Schwartzman, A. E. (2011). Disentangling psychobiological mechanisms underlying internalizing and externalizing behaviors in youth: Longitudinal and concurrent associations with cortisol. Hormones and Behavior, 59, 123–132.CrossRefGoogle ScholarPubMed
Sapolsky, R. M., Romero, L. M., & Munck, A. U. (2000). How do glucocorticoids influence stress response? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocrinology Reviews, 21, 55–89.Google ScholarPubMed
Schafer, J. L., & Graham, J. W. (2002). Missing data: Our view of the state of the art. Psychological Methods, 7, 147–177.CrossRefGoogle ScholarPubMed
Shannon, K. E., Beauchaine, T. P., Brenner, S. L., Neuhaus, E., & Gatzke-Kopp, L. (2007). Familial and temperamental predictors of resilience in children at risk for conduct disorder and depression. Development and Psychopathology, 19, 701–727.CrossRefGoogle ScholarPubMed
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, 691–703.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Shirtcliff, E., Zahn-Waxler, C., Klimes-Dougan, B., & Slattery, M. (2007). Salivary dehydroepiandrosterone responsiveness to social challenge in adolescents with internalizing problems. Journal of Child Psychology and Psychiatry, 48, 580–591.CrossRefGoogle ScholarPubMed
Snoek, H., Van Goozen, S. H. M., Matthys, W., Buitelaar, J. K., & Van Engeland, H. (2004). Stress responsivity in children with externalizing behavior disorders. Development and Psychopathology, 16, 389–406.CrossRefGoogle ScholarPubMed
Sterling, P., & Eyer, J. (1988). Allostasis: A new paradigm to explain arousal pathology. In Fisher, S. & Reason, J. (Eds.), Handbook of life stress, cognition and health (pp. 629–649). Oxford: Wiley.Google Scholar
Strang, N. M., Hanson, J. L., & Pollak, S. D. (in press). The importance of biological methods in linking social experience with social and emotional development. Monographs of the Society for Research in Child Development.Google Scholar
Stroud, L. R., Salovey, P., & Epel, E. S. (2002). Sex differences in stress responses: Social rejection versus achievement stress. Biological Psychiatry, 52, 318–327.CrossRefGoogle ScholarPubMed
Sylvers, P., Brennan, P. A., Lilienfeld, S. O., & Alden, S. A. (2010). Gender differences in autonomic indicators of antisocial personality disorder features. Personality Disorders: Theory, Research, and Treatment, 1, 87–96.CrossRefGoogle ScholarPubMed
Taylor, S. E., Klein, L. C., Lewis, B. P., Gruenewald, T. L., Gurung, R. A. R., & Updegraff, J. A. (2000). Biobehavioral responses to stress in females: Tend-and-befriend, not fight-or-flight. Psychological Review, 107, 411–429.CrossRefGoogle Scholar
Tomarken, A. J., & Waller, N. G. (2005). Structural equation modeling: Strengths, limitations, and misconceptions. Annual Review of Psychology, 1, 31–65.CrossRefGoogle ScholarPubMed
Tonhajzerova, I., Ondrejka, I., Javorka, K., Turianikova, Z, Farsky, I., & Javorka, M. (2010). Cardiac autonomic regulation is impaired in girls with major depression. Progress in Neuro-Psychopharmacology & Biological Psychiatry, 34, 613–618.CrossRefGoogle ScholarPubMed
van Goozen, S. H., Fairchild, G., & Harold, G. T. (2008). The role of neurobiological deficits in childhood antisocial behavior. Current Directions in Psychological Science, 17, 224–228.CrossRefGoogle Scholar
van Goozen, S. H., Matthys, W., Cohen-Kettenis, P. T., Buitelaar, J. K., & van Engeland, H. (2000). Hypothalamic–pituitary–adrenal axis and autonomic nervous system activity in disruptive children and matched controls. Journal of the American Academy of Child & Adolescent Psychiatry, 39, 1438–1445.CrossRefGoogle ScholarPubMed
van Goozen, S. H., Matthys, W., Cohen-Kettenis, P. T., Gispen-de Wied, C., Wiegant, V. M., & van Engeland, H. (1998). Salivary cortisol and cardiovascular activity during stress in oppositional–defiant disorder boys and normal controls. Biological Psychiatry, 43, 531–539.CrossRefGoogle ScholarPubMed
Weems, C. F., & Carrion, V. G. (2007). The association between PTSD symptoms and salivary cortisol in youth: The role of time since the trauma. Journal of Traumatic Stress, 20, 903–907.CrossRefGoogle ScholarPubMed
Weems, C. F., Zakem, A. H., Costa, N. M., Cannon, M. F., & Watts, S. E. (2005). Physiological response and childhood anxiety: Association with symptoms of anxiety disorders and cognitive bias. Journal of Clinical Child & Adolescent Psychology, 34, 712–723.CrossRefGoogle ScholarPubMed
Worthman, C. M., & Panter-Brick, C. (2008). Homeless street children in Nepal: Use of allostatic load to assess the burden of childhood adversity. Development and Psychopathology, 20, 233–255.CrossRefGoogle ScholarPubMed
Zahn-Waxler, C., Klimes-Dougan, B., Hastings, P. D., Duggal, S., Gruber, R., Usher, B. A., et al. (2001). The role of emotion in the development of psychopathology: Protocol #97-M-0116. Bethesda, MD: National Institute of Mental Health.Google Scholar
Zahn-Waxler, C., Shirtcliff, E. A., & Marceau, K. (2008). Disorders of childhood and adolescence: Gender and psychopathology. Annual Review of Clinical Psychology, 4, 275–303.CrossRefGoogle ScholarPubMed