Abstract
The purpose of this study was to examine the association between hypothalamic-pituitary-adrenal axis (HPA-axis) reactivity and proactive and reactive aggression in pre-pubertal children. After a 30-min controlled base line period, 73 7-year-old children (40 males and 33 females) were randomly assigned to one of two experimental tasks designed to elicit fear (N = 33) or frustration (N = 32), or a validity check condition (N = 8). This was followed by a 60-min controlled regulation phase. A total of 17 saliva samples for cortisol analysis were collected including 12 post-stress samples at 5-min intervals. Reactive and proactive aggression levels were assessed via the teacher-completed Aggression Behavior Teacher Checklist (Dodge and Coie, J Pers Soc Psychol, 53(6), 1146–1158, 1987). Reactive aggression significantly predicted total and peak post-stress cortisol regardless of stress modality. Proactive aggression was not a predictor of any cortisol index. Examination of pure reactive, proactive, combined, or non-aggressive children indicated that reactive aggressive children had higher cortisol reactivity than proactive and non-aggressive children. Our data suggest that while an overactive HPA-axis response to stress is associated with reactive aggression, stress induced HPA-axis variability does not seem to be related to proactive aggression.
Similar content being viewed by others
References
Achenbach, T. M. (1992). Manual for the child behavior checklist/2–3 and 1992 profile. Burlington: University of Vermont.
Allison, P. D. (1990). Change scores as dependent variables in regression analysis. Sociological Methodology, 20, 93–114.
Anderson, C. A., & Bushman, B. J. (2002). Human aggression. Annual Review of Psychology, 53, 27–51.
Atkins, M. S., & Stoff, D. M. (1993). Instrumental and hostile aggression in childhood disruptive behavior disorders. Journal of Abnormal Child Psychology, 21(2), 165–178. doi:10.1007/BF00911314.
Atkins, M. S., Stoff, D. M., Osborne, M. L., & Brown, K. (1993). Distinguishing instrumental and hostile aggression: does it make a difference. Journal of Abnormal Child Psychology, 21(4), 355–365. doi:10.1007/BF01261598.
Calkins, S. (1997). Cardiac vagal tone indices of temperamental reactivity and behavioral regulation in young children. Developmental Psychobiology, 31(2), 125–135. doi:10.1002/(SICI)1098-2302(199709)31:2<125::AID-DEV5>3.0.CO;2-M.
Cicchetti, D., & Rogosch, F. A. (2001). The impact of child maltreatment and psychopathology on neuroendocrine functioning. Development and Psychopathology, 13(4), 783–804.
Clow, A., Thorn, L., Evans, P., & Hucklebridge, F. (2004). The awakening cortisol response: methodological issues and significance. Stress (Amsterdam, Netherlands), 7(1), 29–37. doi:10.1080/10253890410001667205.
Coccaro, E. F., McCloskey, M. S., Fitzgerald, D. A., & Phan, K. L. (2006). Amygdala and orbitofrontal reactivity to social threat in individuals with impulsive aggression. Biological Psychiatry, 62(2), 168–178. doi:10.1016/j.biopsych.2006.08.024.
de Kloet, E. R. (1991). Brain corticosteroid receptor balance and homeostatic control. Frontiers in Neuroendocrinology, 12(2), 95–164.
de Rooij, S. R., Painter, R. C., Phillips, D. I. W., Osmond, C., Tanck, M. W. T., Bossuyt, P. M. M., et al. (2006). Cortisol responses to psychological stress in adults after prenatal exposure to the Dutch famine. Psychoneuroendocrinology, 31(10), 1257–1265. doi:10.1016/j.psyneuen.2006.09.007.
Dodge, K. A. (1991). The structure and function of proactive and reactive aggression. In D. J. Pepler, & K. H. Rubin (Eds.), The development and treatment of childhood aggression (pp. 201–218). Hillsdale, NJ: Erlbaum.
Dodge, K. A., & Coie, J. D. (1987). Social-information-processing factors in reactive and proactive aggression in children’s peer groups. Journal of Personality and Social Psychology, 53(6), 1146–1158.
Dodge, K. A., Lochman, J. E., Harnish, J. D., & Bates, J. E. (1997). Reactive and proactive aggression in school children and psychiatrically impaired chronically assaultive youth. Journal of Abnormal Psychology, 106(1), 37–51. doi:10.1037/0021-843X.106.1.37.
Edwards, S., Clow, A., Evans, P., & Hucklebridge, F. (2001). Exploration of the awakening cortisol response in relation to diurnal cortisol secretory activity. Life Sciences, 68(18), 2093–2103. doi:10.1016/S0024-3205(01)00996-1.
Geiss, A., Varadi, E., Steinbach, K., Bauer, H. W., & Anton, F. (1997). Psychoneuroimmunological correlates of persisting sciatic pain in patients who underwent discectomy. Neuroscience Letters, 237(2–3), 65–68. doi:10.1016/S0304-3940(97)00810-0.
Gerra, G., Zaimovic, A., Avanzini, P., & Chittolini, B. (1997). Neurotransmitter–neuroendocrine responses to experimentally induced aggression in humans: influence of personality variable. Psychiatry Research, 66(1), 33–43. doi:10.1016/S0165-1781(96)02965-4.
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(8), 976–987. doi:10.1016/j.psyneuen.2006.05.010.
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(1), 96–103. doi:10.1016/j.yhbeh.2007.09.002.
Johnson, E. O., Kamilaris, T. C., Chrousos, G. P., & Gold, P. W. (1992). Mechanisms of stress: a dynamic overview of hormonal and behavioral homeostasis. Neuroscience and Biobehavioral Reviews, 16(2), 115–130. doi:10.1016/S0149-7634(05)80175-7.
Kabbaj, M., Devine, D. P., Savage, V. R., & Akil, H. (2000). Neurobiological correlates of individual differences in novelty-seeking behavior in the rat: differential expression of stress-related molecules. The Journal of Neuroscience, 20(18), 6983–6988.
Kalin, N. H. (1999a). Primate models and aggression. Journal of Clinical Psychiatry Monograph Series, 17(2), 22–24.
Kalin, N. H. (1999b). Primate models to understand human aggression. Journal of Clinical Psychiatry, 60(15), 29–32.
Kalin, N. H., Larson, C., Shelton, S. E., & Davidson, R. J. (1998). Asymmetric frontal brain activity, cortisol, and behavior associated with fearful temperament in rhesus monkeys. Behavioral Neuroscience, 112(2), 286–292. doi:10.1037/0735-7044.112.2.286.
Kempes, M., de Vries, H., Matthys, W., van Engeland, H., & van Hoof, J. (2008). Differences in cortisol response affect the distinction of observed reactive and proactive aggression in children with aggressive behaviour disorders. Journal of Neural Transmission, 115(1), 139–147. doi:10.1007/s00702-007-0810-9.
Knutson, J. F., Fordyce, D. J., & Anderson, D. J. (1980). Escalation of irritable aggression: control by consequences and antecedents. Aggressive Behavior, 6(4), 347–359. doi:10.1002/1098-2337(1980)6:4<347::AID-AB2480060403>3.0.CO;2-J.
Kruesi, M. J., Schmidt, M. E., Donnelly, M., & Hibbs, E. D. (1989). Urinary free cortisol output and disruptive behavior in children. Journal of the American Academy of Child and Adolescent Psychiatry, 28(3), 441–443. doi:10.1097/00004583-198905000-00024.
Little, T. D., Jones, S. M., Henrich, C. C., & Hawley, P. H. (2003). Disentangling the “whys” from the “whats” of aggressive behaviour. International Journal of Behavioral Development, 27(2), 122–133. doi:10.1080/01650250244000128.
Mathews, J. N., Altman, D. G., Campbell, M. J., & Royston, P. (1990). Analysis of serial measurements in medical research. British Medical Journal, 300(6719), 230–235.
McBurnett, K., Lahey, B. B., Frick, P. J., & Risch, C. (1991). Anxiety, inhibition, and conduct disorder in children: II. Relation to salivary cortisol. Journal of the American Academy of Child and Adolescent Psychiatry, 30(2), 192–196. doi:10.1097/00004583-199103000-00005.
McBurnett, K., Lahey, B. B., Rathouz, P. J., & Loeber, R. (2000). Low salivary cortisol and persistent aggression in boys referred for disruptive behavior. Archives of General Psychiatry, 57(1), 38–43. doi:10.1001/archpsyc.57.1.38.
McBurnett, K., Raine, A., Stouthamer-Loeber, M., Loeber, R., Kumar, A. M., Kuman, M., et al. (2005). Mood and hormone responses to psychological challenge in adolescent males with conduct problems. Biological Psychiatry, 57(10), 1109–1116. doi:10.1016/j.biopsych.2005.01.041.
Moss, H. B., Yanyukov, M., Yao, J. K., & Kirillova, G. P. (1999). Salivary cortisol responses in prepubertal boys: the effects of parental substance abuse and association with drug use behavior during adolescence. Biological Psychiatry, 45(10), 1293–1299. doi:10.1016/S0006-3223(98)00216-9.
Muñoz, L. C., Frick, P. J., Kimonis, E. R., & Auccoin, K. J. (2008). Types of aggression, responsiveness to provocation, and callous-unemotional traits in detained adolescents. Journal of Abnormal Child Psychology, 36(1), 15–28. doi:10.1007/s10802-007-9137-0.
Nouvion, S. O., Cherek, D. R., Lane, S. D., Tcheremissine, O. V., & Lieving, L. M. (2007). Human proactive aggression: association with personality disorders and psychopathy. Aggressive Behavior, 33(6), 552–562. doi:10.1002/ab.20220.
Olson, S. L., & Sameroff, A. J. (1997). Social risk and self-regulation problems in early childhood. Bethesda, MD: National Institute of Mental Health.
Oosterlaan, J., Geurts, H. M., Knol, D. L., & Sergeant, J. A. (2005). Low basal salivary cortisol is associated with teacher-reported symptoms of conduct disorder. Psychiatry Research, 134(1), 1–10. doi:10.1016/j.psychres.2004.12.005.
Orobio de Castro, B., Brendgen, M., Van Boxtel, H., Vitaro, F., & Schaepers, L. (2007). “Accept me, or else”: disputed overestimation of social competence predicts increases in proactive aggression. Journal of Abnormal Child Psychology, 35(2), 165–178. doi:10.1007/s10802-006-9063-6.
Poulin, F., & Boivin, M. (2000). Reactive and proactive aggression: evidence of a two-factor model. Psychological Assessment, 12(2), 115–122. doi:10.1037/1040-3590.12.2.115.
Scerbo, A. S., & Kolko, D. J. (1994). Salivary testosterone and cortisol in disruptive children: relationship to aggressive, hyperactive, and internalizing behaviors. Journal of the American Academy of Child and Adolescent Psychiatry, 33(8), 1174–1184. doi:10.1097/00004583-199410000-00013.
Schulz, K. P., Halperin, J. M., Newcorn, J. H., & Sharma, V. (1997). Plasma cortisol and aggression in boys with ADHD. Journal of the American Academy of Child and Adolescent Psychiatry, 36(5), 605–609. doi:10.1097/00004583-199705000-00010.
Schulz, P., Kirschbaum, C., Prüssner, J., & Hellhammer, D. (1998). Increased free cortisol secretion after awakening in chronically stressed individuals due to work overload. Stress Medicine, 14(2), 91–97. doi:10.1002/(SICI)1099-1700(199804)14:2<91::AID-SMI765>3.0.CO;2-S.
Schwartz, D., Dodge, K. A., Coie, J. D., Hubbard, J. A., Cillessen, A. H., Lamerise, E. A., et al. (1998). Social-cognitive and behavioral correlates of aggression and victimization in boys’ play groups. Journal of Abnormal Child Psychology, 26(6), 431–440. doi:10.1023/A:1022695601088.
Shoal, G. D., Giancola, P. R., & Kirillova, G. P. (2003). Salivary cortisol, personality, and aggressive behavior in adolescent boys: a 5-year longitudinal study. Journal of the American Academy of Child and Adolescent Psychiatry, 42(9), 1101–1107. doi:10.1097/01.CHI.0000070246.24125.6D.
Snoek, H., Van Goozen, S. M., Matthys, W., Buitelaar, J. K., & van Engeland, H. (2004). Stress responsivity in children with externalizing behavior disorders. Development and Psychopathology, 16(2), 389–406. doi:10.1017/S0954579404044578.
Stetler, C., & Miller, G. E. (2005). Blunted cortisol response to awakening in mild to moderate depression: regulatory influences of sleep patterns and social contacts. Journal of Abnormal Psychology, 114(4), 697–705. doi:10.1037/0021-843X.114.4.697.
Tarullo, A. R., & Gunnar, M. R. (2006). Child maltreatment and the developing HPA-axis. Hormones and Behavior, 50(4), 632–639. doi:10.1016/j.yhbeh.2006.06.010.
Tennes, K., & Kreye, M. (1985). Children’s adrenocortical responses to classroom activities and tests in elementary school. Psychosomatic Medicine, 47(5), 451–460.
Tennes, K., Kreye, M., Avitable, N., & Wells, R. (1986). Behavioral correlates of excreted catecholamines and cortisol in second-grade children. Journal of the American Academy of Child Psychiatry, 25(6), 764–770.
Van Bokhoven, I., Van Goozen, S. M., van Engeland, H., Schaal, B., Arseneault, L., Séguin, J. R., et al. (2005). Salivary cortisol and aggression in a population-based longitudinal study of adolescent males. Journal of Neural Transmission, 112(8), 1083–1096. doi:10.1007/s00702-004-0253-5.
Van Goozen, S. M., Fairchild, G., Snoek, H., & Harold, G. T. (2007). The evidence for a neurobiological model of childhood antisocial behavior. Psychological Bulletin, 133(1), 149–182. doi:10.1037/0033-2909.133.1.149.
Van Goozen, S. M., 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(7), 531–539. doi:10.1016/S0006-3223(97)00253-9.
Vanyukov, M. M., Moss, H. B., Plail, J. A., & Blackson, T. (1993). Antisocial symptoms in preadolescent boys and in their parents: associations with cortisol. Psychiatry Research, 46(1), 9–17. doi:10.1016/0165-1781(93)90003-Y.
Vazquez, D. M. (1998). Stress and the developing limbic-hypothalamic-pituitary-adrenal axis. Psychoneuroendocrinology, 23(7), 663–700. doi:10.1016/S0306-4530(98)00029-8.
Vitaro, F., Brendgen, M., & Barker, E. D. (2006). Subtypes of aggressive behaviors: a developmental perspective. International Journal of Behavioral Development, 30(1), 12–19. doi:10.1177/0165025406059968.
Vitaro, F., Brendgen, M., & Tremblay, R. E. (2002). Reactively and proactively aggressive children: antecedent and subsequent characteristics. Journal of Child Psychology and Psychiatry, and Allied Disciplines, 43(4), 495–505. doi:10.1111/1469-7610.00040.
Vitaro, F., Gendreau, P. L., Tremblay, R. E., & Oligny, P. (1998). Reactive and proactive aggression differentially predict later conduct problems. Journal of Child Psychology and Psychiatry, and Allied Disciplines, 39(3), 377–385. doi:10.1017/S0021963097002102.
Vitiello, B., & Stoff, D. M. (1997). Subtypes of aggression and their relevance to child psychiatry. Journal of the American Academy of Child and Adolescent Psychiatry, 36(3), 307–315. doi:10.1097/00004583-199703000-00008.
Wessa, M., Rohleder, N., Kirschbaum, C., & Flor, H. (2006). Altered cortisol awakening response in posttraumatic stress disorder. Psychoneuroendocrinology, 31(2), 209–215. doi:10.1016/j.psyneuen.2005.06.010.
Acknowledgments
Funding for this project was provided by NIMH grants R01MH57489 awarded to Dr. Sheryl Olson, NIMH P50 and MH59396 awarded to Dr. Arnold Sameroff and Dr. Delia M. Vazquez, and by the University of Michigan C.S. Mott Research Fund awarded to Dr. Delia M. Vazquez.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Lopez-Duran, N.L., Olson, S.L., Hajal, N.J. et al. Hypothalamic Pituitary Adrenal Axis Functioning in Reactive and Proactive Aggression in Children. J Abnorm Child Psychol 37, 169–182 (2009). https://doi.org/10.1007/s10802-008-9263-3
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10802-008-9263-3