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Testosterone and Dominance in Humans: Behavioral and Brain Mechanisms

  • Jack van HonkEmail author
  • Peter A. Bos
  • David Terburg
Chapter
Part of the Research and Perspectives in Neurosciences book series (NEUROSCIENCE, volume 21)

Abstract

Most people think that the hormone testosterone especially triggers aggression and antisocial behavior in humans. Mistakenly, the male sex steroid principally underlies each and every aspect of human social behavior but especially social dominance behavior. Testosterone by itself or by way of its metabolite, estradiol, the female sex steroid, is essential in the action of the social peptides oxytocin and vasopressin and regulates the turnover of the social monoamines, dopamine and serotonin. The hormone also has many other actions in the brain; thus the social brain’s main chemical, without exaggeration, is testosterone. Here we review a line of findings with placebo-controlled testosterone administration in the field of social neuroscience in which various techniques are used to investigate social dominance and trustworthiness behaviors. These findings give insights into how and by what biobehavioral mechanisms testosterone acts in humans to motivate them to establish and maintain a dominant status.

Keywords

Social Dominance Interpersonal Trust Social Aggression Testosterone Administration Dominance Behavior 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Adolphs R, Tranel D, Damasio AR (1998) The human amygdala in social judgment. Nature 393:470–474PubMedCrossRefGoogle Scholar
  2. Aubele T, Kritzer MF (2012) Androgen influence on prefrontal dopamine systems in adult male rats: localization of cognate intracellular receptors in medial prefrontal projections to the ventral tegmental area and effects of gonadectomy and hormone replacement on glutamate-stimulated extracellular dopamine level. Cereb Cortex 22:1799–1812PubMedCrossRefGoogle Scholar
  3. Baumgartner T, Heinrichs M, Vonlanthen A, Fischbacher U, Fehr E (2008) Oxytocin shapes the neural circuitry of trust and trust adaptation in humans. Neuron 58:639–650PubMedCrossRefGoogle Scholar
  4. Benarroch EE (2012) Periaqueductal gray: an interface for behavioral control. Neurology 78:210–217PubMedCrossRefGoogle Scholar
  5. Best M (2002) Evidence for a dysfunctional prefrontal circuit in patients with an impulsive aggressive disorder. Proc Natl Acad Sci U S A 99:8448–8453PubMedCrossRefGoogle Scholar
  6. Blair RJ (2003) Facial expressions their communicatory functions and neuro-cognitive substrates. Philos Trans R Soc B Biol Sci 358:561–572CrossRefGoogle Scholar
  7. Blair RJ (2004) The roles of orbital frontal cortex in the modulation of antisocial behavior. Brain Cogn 55:198–208PubMedCrossRefGoogle Scholar
  8. Blasi G, Lo Bianco L, Taurisano P, Gelao B, Romano R, Fazio L, Bertolino A (2009) Functional variation of the dopamine D2 receptor gene is associated with emotional control as well as brain activity and connectivity during emotion processing in humans. J Neurosci 29:14812–14819PubMedCrossRefGoogle Scholar
  9. Boissy A, Bouissou MF (1994) Effects of androgen treatment on behavioral and physiological responses of heifers to fear-eliciting situations. Horm Behav 28:66–83PubMedCrossRefGoogle Scholar
  10. Bos PA, Terburg D, van Honk J (2010) Testosterone decreases trust in socially naïve humans. Proc Natl Acad Sci U S A 107:9991–9995PubMedCrossRefGoogle Scholar
  11. Bos PA, Panksepp J, Bluthé RM, van Honk J (2012) Acute effects of steroid hormones and neuropeptides on human social-emotional behavior: a review of single administration studies. Front Neuroendocrinol 33:17–35PubMedCrossRefGoogle Scholar
  12. Chang LJ, Sanfey AG (2009) Unforgettable ultimatums? Expectation violations promote enhanced social memory following economic bargaining. Front Behav Neurosci 3:36PubMedGoogle Scholar
  13. Dabbs JM, Dabbs MG (2000) Heroes, rogues and lovers: on testosterone and behavior. McGraw-Hill, New YorkGoogle Scholar
  14. Eisenegger C, Knoch D, Ebstein RP, Gianotti LRR, Sándor PS, Fehr E (2010a) Dopamine receptor D4 polymorphism predicts the effect of L-DOPA on gambling behavior. Biol Psychiatry 67:702–706PubMedCrossRefGoogle Scholar
  15. Eisenegger C, Naef M, Snozzi R, Heinrichs M, Fehr E (2010b) Prejudice and truth about the effect of testosterone on human bargaining behaviour. Nature 463:356–359PubMedCrossRefGoogle Scholar
  16. Eisenegger C, Haushofer J, Fehr E (2011) The role of testosterone in social interaction. Trends Cogn Sci 15:263–271PubMedCrossRefGoogle Scholar
  17. Harle KM, Allen JJ, Sanfey AG (2010) The impact of depression on social economic decision making. J Abnorm Psychol 119:440–446PubMedCrossRefGoogle Scholar
  18. Hermans EJ, Ramsey NF, van Honk J (2008) Exogenous testosterone enhances responsiveness to social threat in the neural circuitry of social aggression in humans. Biol Psychiatry 63:263–270PubMedCrossRefGoogle Scholar
  19. Johnson RT, Breedlove SM (2010) Human trust: testosterone raises suspicion. Proc Natl Acad Sci U S A 107:11149–11150PubMedCrossRefGoogle Scholar
  20. Kosfeld M, Heinrichs M, Zak PJ, Fischbacher U, Fehr E (2005) Oxytocin increases trust in humans. Nature 435:673–676PubMedCrossRefGoogle Scholar
  21. Mazur A, Booth A (1998) Testosterone and dominance in men. Behav Brain Sci 21:353–363PubMedGoogle Scholar
  22. Montoya ER, Terburg D, Bos PA, Will GJ, Buskens V, Raub W, van Honk J (2013) Testosterone administration modulates moral judgments depending on second-to-fourth digit ratio. Psychoneuroendocrinology 38:1362–1369PubMedCrossRefGoogle Scholar
  23. Morris JS, Ohman A, Dolan RJ (1999) A subcortical pathway to the right amygdala mediating “unseen” fear. Proc Natl Acad Sci U S A 96:1680–1685PubMedCrossRefGoogle Scholar
  24. O’Doherty J (2003) Can’t learn without you: predictive value coding in orbitofrontal cortex requires the basolateral amygdala. Neuron 39:731–733PubMedCrossRefGoogle Scholar
  25. Öhman A (1986) Face the beast and fear the face: animal and social fears as prototypes for evolutionary analyses of emotion. Psychophysiology 23:123–145PubMedCrossRefGoogle Scholar
  26. Öhman A (1997) As fast as the blink of an eye: evolutionary preparedness for preattentive processing of threat. In: Lang PJ, Simons RF, Balaban MT (eds) Attention and orienting sensory and motivational processes. Lawrence Erlbaum Associates, Mahwah, pp 165–184Google Scholar
  27. Remage-Healey L, Maidment NT, Schlinger BA (2008) Forebrain steroid levels fluctuate rapidly during social interactions. Nat Neurosci 11:1327–1334PubMedCrossRefGoogle Scholar
  28. Sanfey AG, Rilling JK, Aronson JA, Nystrom LE, Cohen JD (2003) The neural basis of economic decision-making in the ultimatum game. Science 300:1755–1758PubMedCrossRefGoogle Scholar
  29. Sapolsky RM (2011) Sympathy for the CEO. Science 333:293–294PubMedCrossRefGoogle Scholar
  30. Schutter DJ, van Honk J (2004) Decoupling of midfrontal delta-beta oscillations after testosterone administration. Int J Psychophysiol 53:71–73PubMedCrossRefGoogle Scholar
  31. Terburg D, van Honk J (2013) Approach-avoidance versus dominance-submissiviness: a multilevel neural framework on how testosterone promotes social status. Emot Rev 5:296–302CrossRefGoogle Scholar
  32. Terburg D, Hooiveld N, Aarts H, Kenemans JL, van Honk J (2011) Eyetracking unconscious face-to-face confrontations: dominance motives prolong gaze to masked angry faces. Psychol Sci 22:314–319PubMedCrossRefGoogle Scholar
  33. Terburg D, Aarts H, van Honk J (2012) Testosterone affects gaze-aversion from angry faces outside of conscious awareness. Psychol Sci 23:459–463PubMedCrossRefGoogle Scholar
  34. Toates F (2006) A model of the hierarchy of behaviour cognition and consciousness. Conscious Cogn 15:75–118PubMedCrossRefGoogle Scholar
  35. Tuiten A, van Honk J, Koppeschaar H, Bernaards C, Thijssen J, Verbaten R (2000) Time course of effects of testosterone administration on sexual arousal in women. Arch Gen Psychiatry 57:149–153PubMedCrossRefGoogle Scholar
  36. van Honk J (2009) Neuroendocrine manipulation of the sexually dimorphic human social brain. In: Harmon-Jones E, Beer JS (eds) Methods in social neuroscience. Guilford Press, New York, pp 45–69Google Scholar
  37. van Honk J, Schutter DJ (2006) Unmasking feigned sanity: a neurobiological model of emotion processing in primary psychopathy. Cogn Neuropsychiat 11:285–306CrossRefGoogle Scholar
  38. van Honk J, Schutter DJ (2007a) Testosterone reduces conscious detection of signals serving social correction: implications for antisocial behavior. Psychol Sci 18:663–667PubMedCrossRefGoogle Scholar
  39. van Honk J, Schutter DJ (2007b) Vigilant and avoidant responses to angry facial perceptions: dominance and submission motives. In: Harmon-Jones E, Winkielman P (eds) Social neuroscience: integrating biological and psychological explanations of social behavior. Guilford Press, New York, pp 197–223Google Scholar
  40. van Honk J, Tuiten A, Verbaten R, van den Hout M, Koppeschaar H, Thijssen J, de Haan E (1999) Correlations among salivary testosterone mood and selective attention to threat in humans. Horm Behav 36:17–24PubMedCrossRefGoogle Scholar
  41. van Honk J, Tuiten A, van den Hout M, Koppeschaar H, Thijssen J, de Haan E, Verbaten R (2000) Conscious and preconscious selective attention to social threat: different neuroendocrine response patterns. Psychoneuroendocrinology 25:577–591PubMedCrossRefGoogle Scholar
  42. van Honk J, Tuiten A, Hermans E, Putman P, Koppeschaar H, Thijssen J, van Doornen L (2001) A single administration of testosterone induces cardiac accelerative responses to angry faces in healthy young women. Behav Neurosci 115:238–242PubMedCrossRefGoogle Scholar
  43. van Honk J, Schutter DJ, Bos PA, Kruijt AW, Lentjes EG, Baron-Cohen S (2011a) Testosterone administration impairs cognitive empathy in women depending on second-to-fourth digit ratio. Proc Natl Acad Sci U S A 108:3448–3452PubMedCrossRefGoogle Scholar
  44. van Honk J, Terburg D, Bos PA (2011b) Further notes on testosterone as a social hormone. Trends Cogn Sci 15:291–292PubMedGoogle Scholar
  45. van Honk J, Montoya ER, Bos PA, van Vugt M, Terburg D (2012) New evidence on testosterone and cooperation. [Comment]. Nature 485:E4–E5PubMedCrossRefGoogle Scholar
  46. van Wingen G, Mattern C, Verkes RJ, Buitelaar J, Fernandez G (2010) Testosterone reduces amygdala-orbitofrontal cortex coupling. Psychoneuroendocrinology 35:105–113PubMedCrossRefGoogle Scholar
  47. Wirth MM, Schultheiss OC (2007) Basal testosterone moderates responses to anger faces in humans. Physiol Behav 90:496–505PubMedCrossRefGoogle Scholar
  48. Wood RI (1996) Functions of the steroid-responsive neural network in the control of male hamster sexual behavior. Trends Endocrinol Metab 7:338–344PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  • Jack van Honk
    • 1
    • 2
    Email author
  • Peter A. Bos
    • 1
    • 2
  • David Terburg
    • 1
    • 2
  1. 1.Department of PsychologyUtrecht UniversityUtrechtThe Netherlands
  2. 2.Department of PsychiatryUniversity of Cape TownCape TownSouth Africa

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