Further notes on testosterone as a social hormoneCopyright © 2011 Elsevier Ltd All rights reserved.
Trends in Cognitive Sciences, 15 June 2011doi:10.1016/j.tics.2011.05.003
Jack van Honk1,2,, David Terburg1andPeter A. Bos11 Department of Experimental Psychology, Utrecht University, Heidelberglaan 2, 3584 CS, Utrecht, Netherlands
2 Department of Psychiatry, University of Cape Town, Groote Schuur Hospital, Anzio Road, Observatory 792, Cape Town, South Africa[h=3]Further notes on testosterone as a social hormone[/h]The hormone testosterone has a bad reputation in terms of how it influences our social behavior. According to the general public, testosterone induces violence and aggression , and in the scientific literature the hormone is victimized as the chemical source of antisocial and immoral behavior, with high-testosterone individuals having psychological profiles that compare to sociopaths . In their passionate and insightful book, Heroes, Rogues and Lovers: On Testosterone and Behavior, James and Mary Dabbs show that these views are mistaken. Dabbs and Dabbs argue that testosterone can in certain conditions motivate rebellious, aggressive and violent behavior but these conditions will mostly involve social dominance competition. However, in other conditions, testosterone can motivate behaviors that are extremely prosocial and altruistic, especially in individuals holding socially protective positions in society, such as firefighters, police officers and soldiers . The effects of the steroid hormone testosterone heavily depend on the social situation, and it is unlikely that this natural bodily fluid has instant antisocial or prosocial properties. Similarly, the peptide hormone oxytocin, popularly known as the ‘love-drug’, is not unconditionally a prosocial hormone. Oxytocin promotes ethnocentrism: its love is biased to the in-group and can come at the expense of out-group hate .
In their TiCS review ‘The role of testosterone in social interaction’ Eisenegger et al. correctly shift the discussion on testosterone and human behavior away from the simple context of social aggression. They discuss the steroid as an adaptive social hormone fulfilling a vital role in status-seeking behaviors, and the subsequent formation of social hierarchies. In this status seeking the authors distinguish between anonymous social–economical interactions, which are their main research interest, and direct face-to-face dominance contests, a focus area in our research. Our behavioral, psycho-physiological and neuroimaging data in this respect have repeatedly shown that testosterone upregulates social vigilance in response to status threats, and that in this process the amygdala seems to play a key role [5,6]. In this commentary we would like to propose two distinct neurobiological mechanisms in which interaction of the hormone and the social environment could increase social vigilance (Figure 1). Firstly, in social confrontations with low threats to status, that is most of human (economic) interaction, testosterone’s upregulation of dopamine action in the orbitofrontal cortex (OFC) functionally decouples the OFC and the amygdala [7,8]. Accordingly, there is loss of OFC inhibition over the amygdala and the brain runs in a safeguarding mode [6,9] that can have antisocial but also prosocial outcomes [1,3]. Testosterone also upregulates the gene expression of vasopressin neurons in the amygdala that, when individuals encounter major threats to status or resources, results in increased activation in the social alarm pathway to the brainstem. Testosterone by way of this ultimate mechanism upholds individuals’ readiness to defend status and resources with physical aggression .
Figure 1:Actions of testosterone on the brain under increasing status threat. (a) Testosterone’s action on the brain during low status threat. Testosterone upregulates dopamine action in the OFC that induces decoupling of the OFC and the amygdala. Consequently, there is impaired inhibitory control of the OFC over the amygdala and the brain runs in ‘safeguarding mode’. (b)Testosterone’s action on the brain during high status threat. In addition to the decoupling of the OFC and amygdala, testosterone, by upregulating vasopressin gene expression in the amygdala, induces hyper-coupling of the amygdala and the brainstem. Under the hyper-coupling of the amygdala and brainstem the brain is in ‘social alarm mode’. AM = amygdala; Bst = brainstem; da = dopamine and avp = vasopressin.
In sum, testosterone, in a stepwise manner and under rising status threat, facilitates a processing shift from the OFC towards the brainstem. This processing shift can ultimately lead to social aggression and compares to a brain-processing shift observed in the case of fear of a proximate threat . The neurobiological processes by which testosterone modulates the social brain can be strongly comparable in rodents and humans but whereas rodents rigidly dominate with social aggression utilizing the social alarm pathway, the twofold mechanism allows for behavioral variation in human dominance contests . Nonetheless, there are several other pathways by which testosterone can act on our social behavior as also discussed in the review of Eisenegger et al. . That these manifold mechanisms by which the hormone can act on our social brains depend on, or are selected by, the social context, throws some light on the vast complexities of hormone–behavior relations, especially in humans. To advance our understanding of these multifaceted processes is the great challenge facing the field of social neuroendocrinology.
[h=3]References[/h]1 Eisenegger, C., et al. (2011). The role of testosterone in social interaction. Trends in Cognitive Sciences 15, 263–271. Abstract | Full Text | PDF (563 kb) | CrossRef | PubMed2 Carney, D.R., and Mason, M.F. (2010). Decision making and testosterone: when the ends justify the means. J. Exp. Soc. Psychol. 46, 668–671. PubMed3 Dabbs, J.M., and Dabbs, M.G. (2000). Heroes, Rogues and Lovers: On Testosterone and Behavior. (: McGraw-Hill). PubMed
4 De Dreu, C.K.W., et al. (2010). Oxytocin promotes etnocentrism. Proc. Natl. Acad. Sci. U.S.A.108, 1262–1266. CrossRef | PubMed5 van Honk, J., and Schutter, D.J. (2007). Vigilant and avoidant responses to angry facial perceptions: dominance and submission motives. In Social Neuroscience: Integrating Biological and Psychological Explanations of Social Behavior. Harmon-Jones, E., Winkielman, P., eds. (: Guilford Press), pp. 197–223. PubMed
6 Bos, P.A., et al. (2011). Acute effects of steroid hormones and neuropeptides on human social-emotional behavior: a review of single administration studies. Front. Neuroendocrinol. . doi:10.1016/j.yfrne.2011.01.002 | PubMed
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