Journal of Abnormal Child Psychology

, Volume 37, Issue 2, pp 169–182 | Cite as

Hypothalamic Pituitary Adrenal Axis Functioning in Reactive and Proactive Aggression in Children

  • Nestor L. Lopez-Duran
  • Sheryl L. Olson
  • Nastassia J. Hajal
  • Barbara T. Felt
  • Delia M. Vazquez


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.


Cortisol HPA Aggression Reactive aggression Proactive aggression Children Stress Response Fear Frustration 



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.


  1. Achenbach, T. M. (1992). Manual for the child behavior checklist/2–3 and 1992 profile. Burlington: University of Vermont.Google Scholar
  2. Allison, P. D. (1990). Change scores as dependent variables in regression analysis. Sociological Methodology, 20, 93–114.CrossRefGoogle Scholar
  3. Anderson, C. A., & Bushman, B. J. (2002). Human aggression. Annual Review of Psychology, 53, 27–51.PubMedCrossRefGoogle Scholar
  4. 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.PubMedCrossRefGoogle Scholar
  5. 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.PubMedCrossRefGoogle Scholar
  6. 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.PubMedCrossRefGoogle Scholar
  7. Cicchetti, D., & Rogosch, F. A. (2001). The impact of child maltreatment and psychopathology on neuroendocrine functioning. Development and Psychopathology, 13(4), 783–804.PubMedGoogle Scholar
  8. 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.Google Scholar
  9. 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.CrossRefGoogle Scholar
  10. de Kloet, E. R. (1991). Brain corticosteroid receptor balance and homeostatic control. Frontiers in Neuroendocrinology, 12(2), 95–164.Google Scholar
  11. 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.PubMedCrossRefGoogle Scholar
  12. 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.Google Scholar
  13. 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.PubMedCrossRefGoogle Scholar
  14. 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.PubMedCrossRefGoogle Scholar
  15. 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.PubMedCrossRefGoogle Scholar
  16. 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.PubMedCrossRefGoogle Scholar
  17. 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.PubMedCrossRefGoogle Scholar
  18. 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.PubMedCrossRefGoogle Scholar
  19. 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.PubMedCrossRefGoogle Scholar
  20. 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.PubMedCrossRefGoogle Scholar
  21. 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.PubMedGoogle Scholar
  22. Kalin, N. H. (1999a). Primate models and aggression. Journal of Clinical Psychiatry Monograph Series, 17(2), 22–24.Google Scholar
  23. Kalin, N. H. (1999b). Primate models to understand human aggression. Journal of Clinical Psychiatry, 60(15), 29–32.PubMedGoogle Scholar
  24. 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.PubMedCrossRefGoogle Scholar
  25. 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.PubMedCrossRefGoogle Scholar
  26. 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.CrossRefGoogle Scholar
  27. 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.PubMedCrossRefGoogle Scholar
  28. 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.CrossRefGoogle Scholar
  29. 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.CrossRefGoogle Scholar
  30. 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.PubMedCrossRefGoogle Scholar
  31. 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.PubMedCrossRefGoogle Scholar
  32. 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.PubMedCrossRefGoogle Scholar
  33. 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.PubMedCrossRefGoogle Scholar
  34. 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.PubMedCrossRefGoogle Scholar
  35. 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.PubMedCrossRefGoogle Scholar
  36. Olson, S. L., & Sameroff, A. J. (1997). Social risk and self-regulation problems in early childhood. Bethesda, MD: National Institute of Mental Health.Google Scholar
  37. 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.PubMedCrossRefGoogle Scholar
  38. 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.PubMedCrossRefGoogle Scholar
  39. 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.PubMedCrossRefGoogle Scholar
  40. 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.PubMedCrossRefGoogle Scholar
  41. 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.PubMedCrossRefGoogle Scholar
  42. 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.CrossRefGoogle Scholar
  43. 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.PubMedCrossRefGoogle Scholar
  44. 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.PubMedCrossRefGoogle Scholar
  45. 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.PubMedCrossRefGoogle Scholar
  46. 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.PubMedCrossRefGoogle Scholar
  47. 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.PubMedCrossRefGoogle Scholar
  48. Tennes, K., & Kreye, M. (1985). Children’s adrenocortical responses to classroom activities and tests in elementary school. Psychosomatic Medicine, 47(5), 451–460.PubMedGoogle Scholar
  49. 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.PubMedCrossRefGoogle Scholar
  50. 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.PubMedCrossRefGoogle Scholar
  51. 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.PubMedCrossRefGoogle Scholar
  52. 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.PubMedCrossRefGoogle Scholar
  53. 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.PubMedCrossRefGoogle Scholar
  54. 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.PubMedCrossRefGoogle Scholar
  55. 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.CrossRefGoogle Scholar
  56. 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.PubMedCrossRefGoogle Scholar
  57. 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.PubMedCrossRefGoogle Scholar
  58. 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.PubMedCrossRefGoogle Scholar
  59. 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.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  • Nestor L. Lopez-Duran
    • 1
  • Sheryl L. Olson
    • 2
  • Nastassia J. Hajal
    • 3
  • Barbara T. Felt
    • 2
  • Delia M. Vazquez
    • 2
  1. 1.Western Psychiatric Institute and ClinicUniversity of PittsburghPittsburghUSA
  2. 2.University of MichiganAnn ArborMichigan
  3. 3.Pennsylvania State UniversityState CollegePennsylvania

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