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Longitudinal synergies between cortisol reactivity and diurnal testosterone and antisocial behavior in young adolescents

Published online by Cambridge University Press:  03 January 2017

Elizabeth J. Susman*
Affiliation:
Pennsylvania State University
Melissa K. Peckins
Affiliation:
Pennsylvania State University
Jacey L. Bowes
Affiliation:
Pennsylvania State University
Lorah D. Dorn
Affiliation:
Pennsylvania State University
*
Address correspondence and reprint requests to: Elisabeth Susman, College of Health and Human Development, 101 Biobehavioral Health Building, Pennsylvania State University, University Park, PA 16802; E-mail: [email protected].

Abstract

The aims were to identify the correspondence between simultaneous, longitudinal changes in cortisol reactivity and diurnal testosterone and to test the hypothesis that cortisol reactivity and diurnal testosterone interact so as to influence antisocial behavior. Participants were 135 children and young adolescents assessed at 6-month intervals over 1 year. Upon enrollment girls were age 8, 10, or 12 years (N = 69, M = 10.06 years) and boys were age 9, 11, or 13 years (N = 66, M = 10.94 years). Assessments included Tanner staging by a nurse, cortisol reactivity (Trier Social Stress Test for Children), diurnal testosterone, and interviews and questionnaires. Growth models showed that cortisol reactivity and diurnal testosterone basal levels (intercept) and rate of change (slopes) were not related, suggesting different mechanisms of growth. Longitudinal regression analyses assessed cortisol reactivity and diurnal testosterone longitudinally. The interactions of cortisol reactivity and diurnal testosterone showed that when diurnal testosterone was low, boys with low cortisol reactivity were reported to have more behavior problems (i.e., oppositional defiant disorder symptoms and attention problems) than when testosterone was high. In addition, when diurnal testosterone was high, boys with high or moderate cortisol reactivity were significantly higher on total antisocial behavior, attention behavior problems, and oppositional defiant disorder symptoms than when testosterone was low or moderate. The results were similar but less frequent for girls. These findings advance the science of young adolescence by showing the interaction between preexisting sensitivity to stressors and the normative testosterone changes of puberty and antisocial behavior.

Type
Regular Articles
Copyright
Copyright © Cambridge University Press 2016 

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References

Achenbach, T. M. (2001). ASEBA, Child Behavior Checklist for Ages 4–18 (CBCL/4–18). Burlington, VT: University of Vermont.Google Scholar
Achenbach, T. M., & Rescorla, L. A. (2001). Manual for the ASEBA school-age forms and profiles. Burlington, VT: University of Vermont, Research Center for Children, Youth, and Families.Google Scholar
Alink, L. R. A., van IJzendoorn, M., Bakermans-Kranenburg, M., Mesman, J., Juffer, F., & Koot, H. (2008). Cortisol and externalizing behavior in children and adolescents: Mixed meta-analytic evidence for the inverse relation of basal cortisol and cortisol reactivity with externalizing behavior. Developmental Psychobiology, 50, 427450. doi:10.1002/dev.20300 Google Scholar
Almeida, S., Petenusci, S., Franci, J. A., Silva, A., & Carvalho, T. (2000). Chronic immobilization-induced stress increases plasma testosterone and delays testicular maturation in pubertal rats. Andrologia, 32, 711. doi:10.1111/j.1439-0272.2000.tb02858.x CrossRefGoogle ScholarPubMed
Archer, J. (2006). Testosterone and human aggression: An evaluation of the challenge hypothesis. Neuroscience & Biobehavioral Reviews, 30, 319345. doi:10.1016/j.neubiorev.2004.12.007 Google Scholar
Belsky, J., & Pluess, M. (2009). Beyond diathesis-stress: Differential susceptibility to environmental influences. Psychological Bulletin, 135, 885908. doi:10.1037/a0017376 CrossRefGoogle ScholarPubMed
Boyce, W. T., & Ellis, B. J. (2005). Biological sensitivity to context: An evolutionary–developmental theory of the origins and functions of stress reactivity. Development and Psychopathology, 17, 271301. doi:10.1017/s0954579405050145 Google Scholar
Brain, P., & Susman, E. J. (1997). Hormonal aspects of antisocial behavior and violence. In Stoff, D. M., Breiling, J., & Maser, J. (Eds.), Handbook of antisocial behavior (pp. 314323). New York: Wiley.Google Scholar
Brooks-Gunn, J., & Warren, M. (1989). Biological and social contributions to negative affect in young adolescent girls. Child Development, 60, 4055. doi:10.2307/1131069 CrossRefGoogle ScholarPubMed
Buske-Kirschbaum, A., Jobst, S., Wustmans, A., Kirschbaum, C., Rauh, W., & Hellhammer, D. (1997). Attenuated free cortisol response to psychosocial stress in children with atopic dermatitis. Journal of Biobehavioral Medicine, 59, 419426.Google ScholarPubMed
Carré, J. M., & Mehta, P. H. (2011). Importance of considering testosterone-cortisol interactions in predicting human aggression and dominance. Aggressive Behavior, 37, 489491. doi:10.1002/ab.20407 CrossRefGoogle ScholarPubMed
Centers for Disease Control and Prevention. (2014). Trends in the prevalence of behaviors that contribute to violence. National Youth Risk Behavior Surveillance: 1991–2013. Retrieved from http://www.cdc.gov/healthyyouth/data/yrbs/pdf/trends/us_violence_trend_yrbs.pdf Google Scholar
Charmandari, E., Kino, T., Souvatzoglou, E., & Chrousos, G. (2003). Pediatric stress: Hormonal mediators and human development. Hormone Research, 59, 161179. doi:10.1159/000069325 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, 12441252. doi:10.1001/jama.1992.03480090092034 CrossRefGoogle ScholarPubMed
Dabbs, J. M., Jurkovic, G. J., & Frady, R. L. (1991). Salivary testosterone and cortisol among late adolescent male offenders. Journal of Abnormal Child Psychology, 19, 469478.CrossRefGoogle ScholarPubMed
Del Giudice, M., Ellis, B. J., & Shirtcliff, E. A. (2011). The adaptive calibration model of stress responsivity. Neuroscience and Biobehavioral Reviews, 35, 15621592. doi:10.1016/j.neubiorev.2010.11.007 Google Scholar
Dorn, L. D., Campo, J. C., Thato, S., Dahl, R. E., Lewin, D., Chandra, R., & Di Lorenzo, C. (2003). Psychological comorbidity and stress reactivity in children and adolescents with recurrent abdominal pain and anxiety disorders. Journal of the American Academy of Child & Adolescent Psychiatry, 42, 6675. doi:10.1097/00004583-200301000-00012 CrossRefGoogle ScholarPubMed
Dorn, L. D., Susman, E. J., Nottelmann, E. D., Inoff-Germain, G., & Chrousos, G. P. (1990). Perceptions of puberty: Adolescent, parent, and health care personnel ratings of pubertal stage. Developmental Psychology, 28, 322329. doi:10.1037/0012-1649.26.2.322 CrossRefGoogle Scholar
Duke, S. A., Balzer, B. W., & Steinbeck, K. S. (2014). Testosterone and its effects on human male adolescent mood and behavior: A systematic review. Journal of Adolescent Health, 55, 315322. doi:10.1016/j.jadohealth.2014.05.007 CrossRefGoogle ScholarPubMed
Eisenberg, N., Sulik, M. J., Spinrad, T. L., Edwards, A., Eggum, N. D., Liew, J., … Hart, D. (2012). Differential susceptibility and the early development of aggression: Interactive effects of respiratory sinus arrhythmia and environmental quality. Developmental Psychology, 48, 755768. doi:10.1037/a0026518 Google Scholar
Ellis, B. J., Boyce, W. T., Belsky, J., Bakermans-Kranenburg, M. J., & van IJzendoorn, M. H. (2011). Differential susceptibility to the environment: An evolutionary–neurodevelopmental theory. Development and Psychopathology, 23, 728. doi: 0.1017/S0954579410000611 CrossRefGoogle Scholar
Fairchild, G., van Goozen, S. H., Stollery, S. J., Brown, J., Gardiner, J., Herbert, J., & Goodyer, I. M. (2008). Cortisol diurnal rhythm and stress reactivity in male adolescents with early-onset or adolescence-onset conduct disorder. Biological Psychiatry, 64, 599606. doi:10.1016/j.biopsych.2008.05.022 CrossRefGoogle ScholarPubMed
Farrington, D. P. (1995). The Twelfth Jack Tizard Memorial Lecture: The development of offending and antisocial behaviour from childhood: Key findings from the Cambridge Study in Delinquent Development. Journal of Child Psychology and Psychiatry, 36, 929964. doi:10.1111/j.1469-7610.1995.tb01342.x Google Scholar
Finkelstein, J. W., Susman, E. J., Chinchilli, V. M., Kunselman, S. J., D'Arcangelo, M. R., Schwab, J., … Kulin, H. E. (1997). Estrogen or testosterone increases self-reported aggressive behaviors in hypogonadal adolescents. Journal of Clinical Endocrinology and Metabolism, 82, 24332438. doi:10.1210/jc.82.8.2433 Google ScholarPubMed
Gordis, E., Granger, D. A., Susman, E. J., & Trickett, P. K. (2009). Asymmetry between salivary cortisol and α-amylase reactivity to stress: Relation to aggressive behavior in adolescents. Psychoneuroendocrinology, 31, 976987.CrossRefGoogle Scholar
Granger, D. A., Shirtcliff, E. A., Zahn-Waxler, C., Usher, B., Klimes-Dougan, B., & Hastings, P. (2003). Salivary testosterone diurnal variation and psychopathology in adolescent boys and females: Individual differences and developmental effects. Development and Psychopathology, 15, 431449. doi:10.1017/S0954579403000233 Google Scholar
Grumbach, M. M., & Styne, D. M. (1998). Puberty: Ontogeny, neuroendocrinology, physiology, and disorders. In Larsen, P. R., Kronenberg, H. M., Melmed, K. S., & Polonsky, K. (Eds.), Williams textbook of endocrinology (pp. 11151286). Philadelphia, PA: W. B. Saunders.Google Scholar
Gunnar, M. R., & Vazquez, D. M. (2001). Low cortisol and a flattening of expected daytime rhythm: Potential indices of risk in human development. Development and Psychopathology, 3, 515538. PMID:11523846Google Scholar
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, 6985. doi:10.1017/S0954579409000054 Google Scholar
Haltigan, J., Roisman, G. I., Susman, E. J., Barnett-Walker, K., & Monahan, K. C. (2011). Elevated trajectories of externalizing problems are associated with lower awakening cortisol levels in midadolescence. Developmental Psychology, 47, 472478. doi:10.1037/a0021911 Google Scholar
Han, G., Miller, J. G., Cole, P. M., Zahn-Waxler, C., & Hastings, P. D. (2015), Adolescents’ internalizing and externalizing problems predict their affect-specific HPA and HPG axes reactivity. Developmental Psychobiology, 57, 769785. doi:10.1002/dev.21268 Google Scholar
Handa, R. J., Burgess, L. H., Kerr, J. E., & O'Keefe, J. A. (1994). Gonadal steroid hormone receptors and sex differences in the hypothalamo-pituitary-adrenal axis. Hormones and Behavior, 28, 464476. doi:10.1006/hbeh.1994.1044 CrossRefGoogle ScholarPubMed
Heim, C., & Nemeroff, C. (2001). The role of childhood trauma in the neurobiology of mood and anxiety disorders: Preclinical and clinical studies. Biological Psychiatry, 49, 10231039. doi:10.1016/S0006-3223(01)01157-X CrossRefGoogle ScholarPubMed
Herting, M. M., Gautam, P., Spielberg, E., Dahl, R. E., & Sowell, E. R. (2014). The role of testosterone and estradiol in brain volume changes across adolescence: A longitudinal structural MRI study. Human Brain Mapping, 35, 56335645. doi:10.1002/hbm.22575 Google Scholar
Hollingshead, A. B. (1975). Four-Factor Index of Social Status. Unpublished manuscript, Yale University.Google Scholar
Holz, N., Boecker, R., Buchmann, A. F., Blomeyer, D., Baumeister, S., Hohmann, S., … Laucht, M. (2014). Evidence for a sex-dependent MAOA × Childhood Stress interaction in the neural circuitry of aggression. Cerebral Cortex, 25, 111. doi:10.1093/cercor/bhu249 Google Scholar
Huang, B., Hillman, J., Ding, L., Biro, F. M., Dorn, L. D., & Susman, E. J. (2012). Correspondence between gonadal steroid hormone concentrations and secondary sexual characteristics assessed by clinicians, adolescents, and parents. Journal of Research on Adolescence, 22, 381391. doi:10.1111/j.1532-7795.2011.00773.x CrossRefGoogle ScholarPubMed
Jaccard, J., & Turrisi, R. (2003). Interaction effects in multiple regression (2nd ed.). Newbury Park, CA: Sage.Google Scholar
Josephs, R. A., Sellers, J. G., Newman, M. L., & Mehta, P. H. (2006). The mismatch effect: When testosterone and status are at odds. Journal of Personality and Social Psychology, 90, 999. doi:10.1037/0022-3514.90.6.999 CrossRefGoogle ScholarPubMed
Kirschbaum, C., Wüst, S., & Hellhammer, D. H. (1992). Consistent sex differences in cortisol responses to psychological stress. Psychosomatic Medicine, 54, 648657. doi:10.1097/00006842-199211000-00004 Google 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, 695719. doi:10.1017/s0954579401003157 Google Scholar
Kokko, K., Pulkkinen, L., Huesman, L., Dubow, E., & Boxer, P. (2009). Intensity of aggression in childhood as a predictor of different forms of adult aggression: A two-country (Finland and the Unites States) analysis. Journal of Research on Adolescence, 19, 934. doi:10.1111/j.1532-7795.2009.00579.x CrossRefGoogle ScholarPubMed
Koss, K. J., George, M. R. W., Cicchetti, D., Davis, P. T., Cummings, E. M., & Sturge-Apple, M. L. (2013). Patterns of children's adrenocortical reactivity to interparental conflict and associations with child adjustment: A growth mixture modeling approach. Developmental Psychobiology, 49, 37–26. doi:10.1037/a0028246 Google ScholarPubMed
Kudielka, B. M., Hellhammer, D. H., & Kirchbaum, C. (2007). Ten years of research with the Trier Social Stress Test—Revisited. In Harmon-Jones, E. & Winkielman, P. (Eds.), Social neuroscience, integrating biological and psychological explanations of social behavior (pp. 5683). New York: Guilford Press.Google Scholar
Laurent, H. K., Ablow, J. C., & Measelle, J. (2012). Taking stress response out of the box: Stability, discontinuity and temperament effects on HPA and SNS across social stressors in mother-infant dyads. Developmental Psychology, 48, 3545. doi:10.1037/a0025518 Google Scholar
Legro, R. S., Lin, H. M., Demers, L. M., & Lloyd, T. (2003). Urinary free cortisol increases in adolescent Caucasian females during perimenarche. Journal of Clinical Endocrinology and Metabolism, 88, 215219. doi:10.1210/jc.2002-020256 Google Scholar
Loeber, R., & Stouthamer-Loeber, M. (1998). Development of juvenile aggression and violence: Some common misconceptions and controversies. American Psychologist, 53, 2259.CrossRefGoogle ScholarPubMed
Lopez-Duran, N. L., Olson, S. L., Hajal, N. J., Felt, B. T., & Vazquez, D. M. (2009). Hypothalamic-pituitary-adrenal axis functioning in reactive and proactive aggression in children. Journal of Abnormal Child Psychology, 37, 169182. doi:10.1007/s10802-008-9263-3 Google Scholar
Marshall, W. A., & Tanner, J. M. (1969). Variations in patterns of pubertal change in girls. Archives of Disease in Childhood, 44, 291303. doi:10.1136/adc.44.235.291 Google Scholar
Marshall, W. A., & Tanner, J. M. (1970). Variations in the pattern of pubertal changes in boys. Archives of Disease in Childhood, 45, 1323. doi:10.1136/adc.45.239.13 Google Scholar
Mehta, P. H., & Joseph, R. A. (2010). Testosterone and cortisol jointly regulate dominance: Evidence for a dual-hormone hypothesis. Hormones and Behavior, 58, 898906. doi:10.1016/j.yhbeh.2010.08.020 Google Scholar
Mitamura, R., Yano, K., Suzuki, N., Ito, Y., Makita, Y., & Okuno, A. (1999). Diurnal rhythms of luteinizing hormone, follicle-stimulating hormone, and testosterone secretion before the onset of male puberty. Journal of Clinical Endocrinology and Metabolism, 84, 2937. doi:10.1210/jc.84.1.29 Google Scholar
Monroe, S. M., & Simmons, A. D. (1991). Diathesis-stress theories in the context of life stress research: Implications for the depressive disorders. Psychological Bulletin, 110, 406425. doi:10.1037/0033-2909.110.3.406 Google Scholar
Montoya, E. R., Terburg, D., Bos, P. A., & van Honk, J. (2012). Testosterone, cortisol, and serotonin as key regulators of social aggression: A review and theoretical perspective. Motivation and Emotion, 36, 6573. doi:10.1007/s11031-011-9264-3 Google Scholar
Nottelmann, E. D., Susman, E. J., Dorn, L. D., Inoff-Germain, G., Loriaux, D. L., Cutler, G. B. Jr., & Chrousos, G. P. (1987). Developmental processes in early adolescence: Relations among chronologic age, pubertal stage, height, weight, and serum levels of gonadotropins, sex steroids, and adrenal androgens. Journal of Adolescent Health Care, 8, 246260. PMID:3583875Google Scholar
Paus, T., Nawaz-Khan, I., Leonard, G., Perron, M., Pike, B., Pitiot, A., … Pausova, Z. (2010). Sexual dimorphism in the adolescent brain: Role of testosterone and androgen receptor in global and local volumes of grey and white matter. Hormones and Behavior, 57, 6375. doi:10.1016/j.hbeh2009.08.004 CrossRefGoogle 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, 366372. doi:10.1016/j.jadohealth.2012.01.005 Google Scholar
Piacentini, J., Roper, M., Jensen, P., Lucas, C., Fisher, P., Bird, H., … Dulcan, M. (1999). Informant-based determinants of symptom attenuation in structured child psychiatric interviews. Journal of Abnormal Child Psychology, 27, 417428. doi:10.1023/A:1021923808118 Google Scholar
Platje, E., Popma, A., Vermeiren, R. R., Doreleijers, T. A., Meeus, W. H., van Lier, P. A., … Jansen, L. (2015). Testosterone and cortisol in relation to aggression in a non-clinical sample of boys and girls. Aggressive Behavior, 41, 478487. doi:10.1002/ab.215 Google Scholar
Pluess, M., & Belsky, J. (2011). Prenatal programming of postnatal plasticity? Development and Psychopathology, 23, 2938. doi:10.1017/S0954579410000623 Google Scholar
Popma, A., Vermeiren, R., Geluk, C. A, Rinne, T., van den Brink, W., Knol, D. L., … Doreleijers, T. A. (2007). Cortisol moderates the relationship between testosterone and aggression in delinquent male adolescents. Biological Psychiatry, 61, 405411. doi:10.1016/j.biopsych.2006.06.006 Google Scholar
Pruessner, J. C., Kirschbaum, C., Meinlschmid, G., & Hellhammer, D. H. (2003). Two formulas for computation of the area under the curve represent measures of total hormone concentration versus time-dependent change. Psychoneuroendocrinology, 28, 916931. doi:10.1016/S0306-4530(02)00108-7 CrossRefGoogle ScholarPubMed
Randazzo, W., Dockray, S., & Susman, E. J. (2008). The stress response in adolescents with inattentive type ADHD symptoms. Child Psychiatry and Human Development, 39, 2738. doi:10.1007/s10578-007-0068-3 CrossRefGoogle ScholarPubMed
Richters, J. E., & Weintraub, S. (1990). Beyond diathesis: Toward an understanding of high-risk environments. In Rolf, J. E., Masten, A. S., Cicchetti, D. K., Nuechterlein, S., & Weintraub, S. (Eds.), Risk and protective factors in the development of psychopathology (pp. 6796). New York: Cambridge University Press.Google 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, 326333. doi:10.1016/j.yhbeh.2007.05.008 Google Scholar
Ruiz-Cortiz, Z. T. (2012). Gonadal sex steroids: Production, action and interactions in mammals, steroids. In Ostojic, S. M. (Ed.), From physiology to clinical medicine. InTech. Retrieved from http://www.intechopen.com/books/steroids-from-physiology-to-clinical-medicine/gonadal-sex-steroids-production-action-and-interactions-in-mammals Google Scholar
Shaffer, D., Fisher, P., Lucas, C. P., Dulcan, M. K., & Schwab-Stone, M. E. (2000). NIMH Diagnostic Interview Schedule for Children version IV (NIMH DISC-IV): Description, differences from previous versions, and reliability of some common diagnoses. Journal of the American Academy of Child & Adolescent Psychiatry, 39, 2838.Google Scholar
Shenk, C. E., Dorn, L. D., Kolko, D. J., Susman, E. J., Noll, J. G., & Bukstein, O. G. (2012). Predicting treatment response for oppositional defiant and conduct disorder using pre-treatment adrenal and gonadal hormones. Journal of Child and Family Studies, 21, 973981. doi:10.1007/s10826-011-9557-x Google Scholar
Shirtcliff, E. A., Dismukes, A. R., Marceau, K., Ruttle, P. A., Simmons, J. G., & Han, G. (2015). A dual axis approach to understanding neuroendocrine development, Developmental Psychobiology, 57, 643653. doi:10.1002/dev21337 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, 690703. doi:10.1002/dev.20336 Google Scholar
Soma, K. K. (2006). Testosterone and aggression: Berthold, birds and beyond. Journal of Neuroendocrinology, 18, 543551. doi:10.1111/j.1365-2826.2006.01440.x Google Scholar
Stroud, L. R., Foster, E., Papandonatos, G. D., Handwerger, K., Granger, D. A., Kivlighan, K. T., & Niaura, R. (2009). Stress response and the adolescent transition: Performance versus peer rejection stressors. Development and Psychopathology, 21, 4768. doi:10.1017/S0954579409000042 Google Scholar
Susman, E. J. (2006). Psychobiology of persistent antisocial behavior: Stress, early vulnerabilities and the attenuation hypothesis. Neuroscience & Biobehavioral Reviews, 30, 376389. doi:10.1016/j.neubiorev.2005.08.002 Google Scholar
Susman, E. J., Dockray, S., Granger, D. A., Blades, K. T., Randazzo, W., Heaton, J. A., & Dorn, L. D. (2010). Cortisol and alpha amylase reactivity and timing of puberty: Vulnerabilities for antisocial behavior in young adolescents. Psychoneuroendocrinology, 35, 557569. doi:10.1016/j.psyneuen.2009.09.00 Google Scholar
Susman, E. J., Dorn, L. D., Inoff-Germain, G., Nottelmann, E. D., & Chrousos, G. P. (1997). Cortisol reactivity, distress behavior, and behavioral problems in young adolescents: A longitudinal perspective. Journal of Research on Adolescence, 7, 81105. doi:10.1207/s15327795jra0701_5 Google Scholar
Susman, E. J., Houts, R. M., Steinberg, L., Belsky, J., Cuffman, E., DeHart, G., … NICHD Early Child Care Research Network. (2010). Longitudinal development of secondary sexual characteristics in girls and boys between ages 9½ and 15½ years. Archives of Pediatrics and Adolescent Medicine, 164, 166173. doi:10.1001/archpediatrics.2009.261 Google Scholar
Susman, E. J., Inoff-Germain, G., Nottelmann, E. D., Loriaux, D. L., Cutler, G. B. Jr., & Chrousos, G. P. (1987). Hormones, emotional dispositions, and aggressive attributes in young adolescents. Child Development, 58, 11141134. doi:10.2307/1130551 Google Scholar
van Bokhoven, I., van Goozen, S. H., van Engeland, H., Schaal, B., Arseneault, L., Séguin, J. R., … Tremblay, R. E. (2006). Salivary testosterone and aggression, delinquency, and social dominance in a population-based longitudinal study of adolescent males. Hormones and Behavior, 50, 118125. doi:10.1016/j.yhbeh.2006.02.002 Google Scholar
van Goozen, S. H. M., Fairchild, G., Snoek, H., & Harold, G. T. (2007). The evidence for a neurobiological model of childhood antisocial behavior. Psychological Bulletin, 133, 149182. doi:10.1037/0033-2909.133.1.149 Google Scholar
Viau, V. (2002). Functional cross-talk between the hypothalamic-pituitary-gonadal and -adrenal axes. Journal of Neuroendocrinology, 14, 506513. doi:10.1046/j.1365-2826.2002.00798.x Google Scholar
Zuckerman, M. (1999). Vulnerability to psychopathology: A biosocial model. Washington, DC: American Psychological Association.Google Scholar