Skip to main content
Log in

Steroid hormones and some evolutionary-relevant social interactions

  • Original Paper
  • Published:
Motivation and Emotion Aims and scope Submit manuscript

Abstract

The steroid hormones, testosterone and cortisol, have some common characteristics, but they are related to generally antagonic processes at both the physiological and psychological levels. In addition, they are the product of the activation of two axes, the hypothalamic–pituitary–gonadal (HPG) and hypothalamic–pituitary–adrenal (HPA), which are very sensitive to a wide range of stressors. Our review focuses on the role of testosterone and cortisol in some social situations, such as competition and others related to the challenge hypothesis, that are evolutionary-relevant and have a component of social stress. Research findings are presented on these points, especially emphasizing the relevance of how the individual interprets social stimuli and attributes of the other participant in the interaction, producing consequences in the response pattern to the social situation. This paper presents empirical support for the role of the interaction between the reproductive HPG and stress HPA axes in several social behaviors with important adaptive significance.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Adlercreutz, H., Härkönen, M., Kuoppasalmi, K., Näveri, H., Huhtamieni, H., Tikkanen, H., et al. (1986). Effect of training on plasma anabolic and catabolic steroid hormones and their responses during physical exercise. International Journal of Sports Medicine, 7, 27–28.

    Article  PubMed  Google Scholar 

  • Archer, J. (2006). Testosterone and human aggression: An evaluation of the challenge hypothesis. Neuroscience and Biobehavioral Reviews, 30, 319–345.

    Article  PubMed  Google Scholar 

  • Arnedo, M. T., Salvador, A., Martínez-Sanchís, S., & González-Bono, E. (2000). Rewarding properties of testosterone in intact male mice: A pilot study. Pharmacology, Biochemistry and Behavior, 65, 327–332.

    Article  Google Scholar 

  • Arnedo, M. T., Salvador, A., Martínez-Sanchís, S., & Pellicer, O. (2002). Similar rewarding effects of testosterone in mice rated as short and long attack latency individuals. Addiction Biology, 7, 373–379.

    Article  PubMed  Google Scholar 

  • Beach, F. A. (1950). The Snark was a Boojum. American Psychologist, 5, 115–124.

    Article  Google Scholar 

  • Blanchard, R. J., McKittrick, C. R., & Blanchard, D. C. (2001). Animal models of social stress: Effects on behavior and brain neurochemical systems. Physiology & Behavior, 73, 261–271.

    Article  Google Scholar 

  • Cunningham, C. L. (1995). Localization of genes influencing ethanol-induced conditioned place preference and locomotor activity in BDX recombinant inbred mice. Psychopharmacology, 107, 385–393.

    Article  Google Scholar 

  • Derntl, B., Windischberger, C., Robinson, S., Kryspin-Exner, I., Gur, R. C., Moser, E., et al. (2009). Amygdala activity to fear and anger in healthy young males is associated with testosterone. Psychoneuroendocrinology, 34, 687–693.

    Article  PubMed  Google Scholar 

  • Eisenegger, C., Haushofer, J., & Fehr, E. (2011). The role of testosterone in social interaction. Trends in Cognitive Sciences, 15(6), 263–271.

    Article  PubMed  Google Scholar 

  • Engebretson, T. O., Sirota, A. D., Niaura, R. S., Edwards, K., & Brown, W. A. (1999). A simple laboratory method for inducing anger: A preliminary investigation. Journal of Psychosomatic Research, 47, 13–26.

    Article  PubMed  Google Scholar 

  • Fuxjager, M. J., Montgomery, J. L., & Marler, C. A. (2011). Species differences in the winner effect disappear in response to post-victory testosterone manipulations. In Proceedings of the royal academy of biological sciences, doi:10.1098/rspb.2011.0301.

  • Gadea, M., Espert, R., Salvador, A., & Martí-Bonmatí, L. (2011). The sad, the angry, and the asymmetrical brain: Dichotic Listening studies of negative affect and depression. Brain and Cognition, 76, 294–299.

    Article  PubMed  Google Scholar 

  • Gadea, M., Gómez, C., González-Bono, E., Espert, R., & Salvador, A. (2005). Increased cortisol and decreased right ear advantage (REA) in dichotic listening following a negative mood induction. Psychoneuroendocrinology, 30, 129–138.

    Article  PubMed  Google Scholar 

  • Harmon-Jones, E., Lueck, L., Fearn, M., & Harmon-Jones, C. (2006). The effect of personal relevance and approach-related action expectation on relative left frontal cortical activity. Psychological Science, 17, 434–440.

    Article  PubMed  Google Scholar 

  • Henry, J. P. (1992). Biological basis of the stress response. Integrative Physiological and Behavioral Science, 27, 66–83.

    Article  PubMed  Google Scholar 

  • Henry, J. P., & Stephens, P. M. (1977). Stress health and the social environment. Berlin: Springer.

    Book  Google Scholar 

  • Henry, J. P., Steven, P. M., & Ely, D. (1986). Psychosocial hypertension and the defense and defeat reactions. Journal of Hypertension, 4, 687–697.

    Article  PubMed  Google Scholar 

  • Herrero, N., Gadea, M., Rodríguez-Alarcón, G., Espert, R., & Salvador, A. (2010). What happens when we get angry? cardiovascular, hormonal and asymmetrical brain responses. Hormones and Behavior, 57, 276–283.

    Article  PubMed  Google Scholar 

  • 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, 115–130.

    Article  PubMed  Google Scholar 

  • Johnson, L. R., & Wood, R. I. (2001). Oral testosterone self-administration in male hamsters. Neuroendocrinology, 73, 285–292.

    Article  PubMed  Google Scholar 

  • Kashkin, K. B., & Kleber, D. (1989). Hooked on hormones? An anabolic steroid addiction hypothesis. Journal of the American Medical Association, 262, 3166–3170.

    Article  PubMed  Google Scholar 

  • Kemper, T. D. (1990). Social structure and testosterone. Explorations of the socio-biosocial chain. New Brunswick: Rutgers University Press.

    Google Scholar 

  • Koolhaas, J. M., & Bohus, B. (1989). Social control in relation to neuroendocrine and immunological responses. In A. Steptoe & A. Appels (Eds.), Stress, personal control and health (pp. 295–305). Chichester: Wiley.

    Google Scholar 

  • Koolhaas, J. M., de Boer, S. F., Buwalda, B., & van Reenen, K. (2007). Individual variation in coping with stress: A multidimensional approach of ultimate and proximate mechanisms. Brain, Behavior and Evolution, 70, 218–226.

    Article  PubMed  Google Scholar 

  • Koolhaas, J. M., de Boer, S. F., Coppens, C. M., & Buwalda, B. (2010). Neuroendocrinology of coping styles: Towards understanding the biology of individual variation. Frontiers in Neuroendocrinology, 31, 307–321.

    Article  PubMed  Google Scholar 

  • Koolhaas, J. M., Korte, S. M., de Boer, S. F., Van der Vegt, B. J., Van Reenen, C. G., Hopster, H., et al. (1999). Coping styles in animals: Current status in behavior and stress-physiology. Neuroscience and Biobehavioral Reviews, 23, 925–935.

    Article  PubMed  Google Scholar 

  • Korte, S. M., Koolhaas, J. M., Wingfield, J. C., & McEwen, B. S. (2005). The Darwinian concept of stress: Benefits of allostasis and costs of allostatic load and the trade-offs in health and disease. Neuroscience and Biobehavioral Reviews, 29, 3–38.

    Article  PubMed  Google Scholar 

  • Kraemer, W. J., & Ratamess, N. A. (2005). Hormonal responses and adaptations to resistance exercise and training. Sports Medicine, 35, 339–361.

    Article  PubMed  Google Scholar 

  • Lazarus, R. S., & Folkman, S. (1984). Stress, appraisal and coping. New York: Springer.

    Google Scholar 

  • Levine, S. (2000). Influence of psychological variables on the activity of the hypothalamic-pituitary-adrenal axis. European Journal of Pharmacology, 405, 149–160.

    Article  PubMed  Google Scholar 

  • Martínez, M., Guillén-Salazar, F., Salvador, A., & Simón, V. M. (1995). Successful intermale aggression and conditioned place preference in mice. Physiology & Behavior, 58, 323–328.

    Article  Google Scholar 

  • Martínez-Sanchís, S., Arnedo, M. T., Salvador, A., Moya-Albiol, L., & González-Bono, E. (2003). Effects of chronic administration with high doses of testosterone propionate on behavioral and physiological parameters in mice with differing basal aggressiveness. Aggressive Behavior, 29, 173–189.

    Article  Google Scholar 

  • Martínez-Sanchís, S., Salvador, A., Moya-Albiol, L., Gonzalez-Bono, E., & Simón, V. M. (1998). Effects of chronic treatment of testosterone propionate on aggression and hormonal levels in intact male mice. Psychoneuroendocrinology, 23, 275–293.

    Article  PubMed  Google Scholar 

  • Mazur, A. (1985). A biosocial model of status in face-to-face primate groups. Social Forces, 64, 377–402.

    Google Scholar 

  • Mazur, A., & Booth, A. (1998). Testosterone and dominance in men. Behavioral and Brain Sciences, 21, 353–397.

    Article  PubMed  Google Scholar 

  • Mehta, P. J., & Beer, J. (2010). Neural mechanisms of the testosterone–aggression relation: The role of orbitofrontal cortex. Journal of Cognitive Neuroscience, 22, 2357–2368.

    Article  PubMed  Google Scholar 

  • Mehta, P. J., & Gosling, S. D. (2008). Bridging human and animal research: A comparative approach to studies of personality and health. Brain, Behavior, and Immunity, 22, 651–661.

    Article  PubMed  Google Scholar 

  • Mehta, P. J., & Josephs, R. A. (2010). Testosterone and cortisol jointly regulate dominance: Evidence for a dual-hormone hypothesis. Hormones and Behavior, 58, 898–906.

    Article  PubMed  Google Scholar 

  • Miczek, K. A., Thompson, M. L., & Tornatzky, W. (1991). Subordinate animals: Behavioural and physiological adaptations and opioid tolerance. In M. R. Brown, G. F. Koob, & C. River (Eds.), Stress: Neurobiology and neuroendocrinology (pp. 323–357). New York, NY: Marcel Dekker.

    Google Scholar 

  • Moya-Albiol, L., Salvador, A., Costa, R., Martínez-Sanchis, S., González-Bono, E., Ricarte, J., et al. (2001a). Psychophysiological responses to the Stroop task after a maximal cycle ergometry in elite sportsmen and physically active subjects. International Journal of Psychophysiology, 40, 47–59.

    Article  PubMed  Google Scholar 

  • Moya-Albiol, L., Salvador, A., González-Bono, E., Martínez-Sanchís, S., & Costa, R. (2001b). The impact of exercise on hormones is related to autonomic reactivity to a mental task. International Journal of Stress Management, 8, 215–229.

    Article  Google Scholar 

  • Nelson, R. J. (2000). An Introduction to Behavioral Endocrinology (2nd ed.). Sunderland, Massachusetts: Sinauer Associates.

    Google Scholar 

  • Popma, A., Vermeiren, R., Geluk, C. A. M. L., Rinne, T., van den Brink, W., Knol, D. L., et al. (2007). Cortisol moderates the relationship between testosterone and aggression in delinquent male adolescents. Biological Psychiatry, 61, 405–411.

    Article  PubMed  Google Scholar 

  • Rodriguez-Alarcón, G., Canales, J. J., & Salvador, A. (2007). Rewarding effects of 3,4-methylenedioxymethamphetamine (“Ecstasy”) in dominant and subordinate OF-1 mice in the place preference conditioning paradigm. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 31, 191–199.

    Article  PubMed  Google Scholar 

  • Rodriguez-Alarcón, G., & Salvador, A. (in preparation). Rewarding properties of testosterone and sensitization for the social status in male mice exposed to social stress.

  • Salvador, A. (2005). Coping with competitive situations in humans. Neuroscience and Biobehavioral Reviews, 29, 195–205.

    Article  PubMed  Google Scholar 

  • Salvador, A., & Costa, R. (2009). Coping with competition: Neuroendocrine responses and cognitive variables. Neuroscience and Biobehavioral Reviews, 33, 160–170.

    Article  PubMed  Google Scholar 

  • Salvador, A., Ricarte, J., González-Bono, E., & Moya-Albiol, L. (2001). Effects of physical training on endocrine and autonomic responsiveness to acute stress. Journal of Psychophysiology, 15, 114–121.

    Article  Google Scholar 

  • Salvador, A., & Serrano, M. A. (2002). Perspectiva histórica y tendencias de investigación de la Psicoendocrinología. Revista de Psicología General y Aplicada, 55, 285–311.

    Google Scholar 

  • Salvador, A., Serrano, M. A., & González-Bono, E. (2003). Research trends in the Journal Hormones and Behavior (1987–2000). Hormones and Behavior, 43, 375–380.

    Article  PubMed  Google Scholar 

  • Salvador, A., Suay, F., Martinez-Sanchis, S., Simón, V. M., & Brain, P. F. (1999). Correlating testosterone and fighting in male participants in judo contests. Physiology & Behavior, 68, 205–209.

    Article  Google Scholar 

  • Sapolsky, R. (2005). The influence of social hierarchy on primate health. Science, 308, 648–652.

    Article  PubMed  Google Scholar 

  • Serrano, M. A., Salvador, A., González-Bono, E., Sanchís, C., & Suay, F. (2001). Relationships between recall of perceived exertion and blood lactate concentration in a judo competition. Perceptual and Motor Skills, 92, 1139–1148.

    PubMed  Google Scholar 

  • Suay, F., & Salvador, A. (2012). Cortisol. In F. Ehrlenspiel & K. Strahler (Eds.), Psychoneuroendocrinology of sport and exercise (pp. 63–90). London: Routledge.

    Google Scholar 

  • Suay, F., Salvador, A., & Ricarte, J. (1998). Indicadores psicológicos de sobreentrenamiento y agotamiento. [Psychological markers of overtraining and staleness]. Revista de Psicología del Deporte, 13, 7–25.

    Google Scholar 

  • Svare, B. (1988). Some trends in the responses studied and the species employed by behavioral endocrinologists. Hormones and Behavior, 22, 139–142.

    Article  PubMed  Google Scholar 

  • Terburg, D., Morgan, B., & van Honk, J. (2009). The testosterone–cortisol ratio: A hormonal marker for proneness to social aggression. International Journal of Law and Psychiatry, 32, 216–223.

    Article  PubMed  Google Scholar 

  • Urhausen, A., & Kindermann, W. (2002). Diagnosis of overtraining: What tools do we have? Sports Medicine, 32, 95–102.

    Article  PubMed  Google Scholar 

  • Ursin, H., & Eriksen, H. R. (2004). The cognitive activation theory of stress. Psychoneuroendocrinology, 29, 567–592.

    Article  PubMed  Google Scholar 

  • van Anders, S. M., & Watson, N. V. (2006). Social neuroendocrinology. Effects of social contexts and behaviors on sex steroids in humans. Human Nature, 17, 212–237.

    Article  Google Scholar 

  • van der Meij, L., Almela, M., Buunk, A. P., Fawcett, T. W., & Salvador, A. (2011). Men with elevated testosterone levels show more affiliative behaviours during interactions with women. Proceedings of the Royal Society B. doi:10.1098/rspb.2011.0764.

  • van der Meij, L., Buunk, A. P., Almela, M., & Salvador, A. (2010a). Testosterone responses to competition: The opponent’s psychological state makes it challenging. Biological Psychology, 84, 330–335.

    Article  PubMed  Google Scholar 

  • van der Meij, L., Buunk, A. P., & Salvador, A. (2010b). Contact with attractive women affects the release of cortisol in men. Hormones and Behavior, 58, 501–505.

    Article  PubMed  Google Scholar 

  • van der Meij, L., Buunk, A. P., van de Sande, J. P., & Salvador, A. (2008). The presence of a woman increases testosterone in aggressive dominant men. Hormones and Behavior, 54, 640–644.

    Article  PubMed  Google Scholar 

  • van Honk, J., Harmon-Jones, E., Morgan, B. E., & Schutter, D. J. L. G. (2010). Socially explosive minds: The triple imbalance hypothesis of reactive aggression. Journal of Personality, 78(1), 67–94.

    Article  PubMed  Google Scholar 

  • van Honk, J., & Pruessner, J. C. (2010). Psychoneuroendocrine imaging: A special issue of psychoneuroendocrinology (Editorial). Psychoneuroendocrinology, 35, 1–4.

    Article  PubMed  Google Scholar 

  • van Wingen, G., Mattern, C., Verkes, R., Buitelaar, J., & Fernández, G. (2010). Testosterone reduces amygdala–orbitofrontal cortex coupling. Psychoneuroendocrinology, 35, 105–113.

    Article  PubMed  Google Scholar 

  • Viau, V. (2002). Functional cross-talk between the hypothalamic-pituitary-gonadal and -adrenal axes. Journal of Neuroendocrinoly, 14, 506–513.

    Article  Google Scholar 

  • Weiner, H. (1992). Perturbing the organism. The biology of stressful experience. Chicago, Ill: The University of Chicago Press.

    Google Scholar 

  • Windisch, C., Wegner, M., & Budde, H. (2012). Testosterone. In F. Ehrlenspiel & K. Strahler (Eds.), Psychoneuroendocrinology of sport and exercise (pp. 91–128). London: Routledge.

    Google Scholar 

  • Wingfield, J. C., Hegner, R. E., Dufty, A. M., & Ball, G. F. (1990). The challenge hypothesis: ‘Theoretical implications’ for patterns of testosterone secretion, mating systems, and breeding strategies. The American Naturalist, 136, 829–846.

    Article  Google Scholar 

Download references

Acknowledgments

This research was supported by the Spanish Education and Science Ministry (SEJ2004-07191/PSIC, SEJ2006-14086/PSIC, SEJ2007-62019/PSIC) and Generalitat Valenciana (ACOMP2011-166, PROMETEO/2011/048). The author wishes to thank Ms. Cindy DePoy for the revision of the English text and two anonymous referees for constructive feedback on the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Alicia Salvador.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Salvador, A. Steroid hormones and some evolutionary-relevant social interactions. Motiv Emot 36, 74–83 (2012). https://doi.org/10.1007/s11031-011-9265-2

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11031-011-9265-2

Keywords

Navigation