Social status & testosterone

We’ve discussed signaling and status endlessly on LW; I think this is right up our vein: a 2011 review of research on the connections between famous male hormone testosterone and various forms of social interaction and especially social status, Eisenegger et al’s “The role of testosterone in social interaction”. (I grabbed this PDF in the short time Elsevier left full-text available, but only now, with some modafinil-powered spare time, have gotten around to excerpting it for you guys.)

1 Abstract

Although animal researchers established the role of testosterone as a ‘social hormone’ decades ago, the investigation of its causal influence on human social behaviors has only recently begun. Here, we review and discuss recent studies showing the causal effects of testosterone on social interactions in animals and humans, and outline the basic neurobiological mechanisms that might underlie these effects. Based on these recent findings, we argue that the role of testosterone in human social behavior might be best understood in terms of the search for, and maintenance of, social status.

2 Excerpts

Is testosterone simply aggression promoting (a sort of ‘roid rage’)?

Early evidence for the role of testosterone in social behavior suggested that it facilitates overt physical aggression (see Glossary) in social contexts. For instance, castrated rodents, which have little, if any, testosterone circulating in their blood, show a near-complete absence of physical fights; however, fights can be fully restored by providing testosterone supplementation to these animals [03]…high testosterone levels in male prisoners have been linked to having a history of rape, murder and armed robbery, and relatively lower levels to a history of theft and drug abuse [08]. A similar pattern was observed in a study of female prison inmates [9]. However, the causality in these studies remains unclear

Probably not:

the existing evidence for a link between aggression and testosterone in humans is relatively weak, but positive [12]. Even if one accepts the fact that reactive aggression can be measured in a controlled laboratory environment, results are similarly inconclusive: recent studies found a positive relationship between baseline testosterone levels and laboratory measures of reactive aggression (reviewed in [11]), but others also reported null findings (in larger samples) [13]. Most importantly, however, a causal role for testosterone in forms of reactive aggression could not be confirmed, as neither long-term nor acute administration of testosterone had an effect [13,14].

This may come as a surprise:

Folk wisdom holds that testosterone causes antisocial, egoistic, or even aggressive behaviors in humans. However, the correlational studies discussed above already suggest that this simple folk view probably requires revision [34,56]. A recent placebo-controlled testosterone administration study found support for the idea that the testosterone-aggression link might be based upon ‘folk’ views: individuals given placebo who believed they had been given testosterone showed less fair bargaining offers compared with those who believed that they had received placebo, thus confirming people’s stereotypes about the behavioral effects of testosterone.

The null findings may be due to a possible confounding effect of homeostasis, but that wouldn’t cover the null on acute administration:

The first study to use a causal testosterone administration procedure in an experimental economic setting did not find any effects on several economic social interactions [14]. Because the study used long-term administration of testosterone, this null finding might be due to secondary feedback effects on the neuroendocrine axis (i.e. suppression of endogenous testosterone production owing to chronic administration). In general, acute administration shows greater reliability in the production of both behavioral and neurophysiological effects (reviewed in [55]).

‘Dominant’ looks like a better perspective than ‘aggressive’:

rhesus monkeys with high testosterone levels use stares, threats and displacements, rather than overtly aggressive interactions, to ascertain high social status [16]…[saliva] measurements of testosterone at a single time-point correlate positively with high dominance in both adolescents [19,20] and adults [21,22]. In addition, salivary testosterone levels correlate with implicit measures of power motivation [23] and increased vigilance for status threats [24,25]. As a result of these relationships, and the moderate stability of testosterone levels over time, some have suggested that baseline testosterone levels reflect a personality trait [26]

men show a larger increase in testosterone when exposed to the scent of an ovulating woman compared with that of a non-ovulating woman or a control [27]. Apart from sexual social stimuli, which are reliable inductors of a testosterone response [28,29], social interactions outside a direct reproductive context have also been shown to induce a testosterone response [01]. In particular, testosterone levels rise within minutes in anticipation of both physical and non-physical competitive situations; for example, dyadic food competition in chimpanzees [30], or tennis, chess or domino tournaments in humans (reviewed in [31]). Testosterone also reacts to contest outcomes [32], and not just to anticipation: for instance, stock traders show higher testosterone levels if their daily profits are above average, and winners of soccer matches show higher testosterone levels than do the losers [33]….causal manipulation of social context (e.g. rigged contests) confirms a causal effect of winning situations on testosterone levels (e.g. [34–38]). These effects can be large; for example, merely watching oneself win a competitive interaction on video produces a 40% testosterone surge from baseline [37].

This interest in dominance leads to mental changes (I am reminded of self-deception):

individuals who generally have higher scores on self-reported dominance and higher basal levels of testosterone show vigilant responses to angry facial expressions (reviewed in [42]). Furthermore, exogenous administration of testosterone increases the sympathetic heart-rate response to angry, but not to happy facial expressions [43] (Figure 2). Although this could theoretically also reflect autonomic arousal as part of a fear response, testosterone has been shown to reduce fear [44], suggesting that dominant people perceive an angry face as a challenge….a recent testosterone administration study has shown that facial mimicry [“a precursor of empathy-related processes occurring automatically”] in response to emotional facial expressions is relatively suppressed after a single dose of testosterone [48]…a single administration of testosterone to young females leads to a significant impairment in the ability to infer emotions, intentions and feelings from the eye region of the face [49]. In addition, the same study established that subjects’ second-to-fourth digit ratio, which is thought to be a marker of prenatal testosterone exposure, is largely able to predict this effect…In line with this are findings of decreased trustworthiness ratings of facial photographs in subjects who received a single dose of testosterone [51]. Crucially, this effect was driven most strongly by those who trusted easily, suggesting that testosterone adaptively increases social vigilance in these trusting individuals to better prepare them for competition over status and valued resources

(The jokes about women and men almost make themselves.)

Not all of these changes are what one would naively expect (see previously about the ‘folk theory’ of testosterone):

one acute dose of testosterone in women increased the fairness of proposers’ bargaining offers in an ultimatum game [13] (Figure 3). An important motive driving proposer behavior is to avoid the rejection of the offer. Thus, if testosterone increases the concern for status, subjects who received testosterone might have perceived a rejection as more aversive, inducing them to make fairer offers…Another study [57] found that testosterone administration prior to an ultimatum game resulted in decreased generosity in a sample of healthy males if repeated measures were not controlled for. The results are insignificant, however, if the fact that the same subject participated in the ultimatum game several time is correctly controlled for statistically. Moreover, a recent study suggests that a low second-to-fourth digit ratio (high prenatal testosterone exposure) is associated with unfair proposer offers if subjects had previously received an unfair offer when in the responder role [58]. Many possible spill-over effects can thus occur in a within-subject design such as that used in [57], where subjects repeatedly play as a proposer and a responder, rendering the interpretation of the results difficult.

I found interesting the material starting page 267, “Neurobiological mechanisms underlying the role of testosterone in social status hierarchies” (due to my own musings about the possible effects of masturbation went that it might be misinterpreted as reproductive ‘success’ which reduces risk-taking or activity in general):

Maintaining a high status position requires an increased sensitivity for aversive events and impending social threats, particularly those that challenge the high social status of an individual. As we show below, testosterone appears to be able to influence such processes; in particular, it appears to confer high motivational drive, low fearfulness and high stress-resilience, either directly or via interactions with other hormones and neurotransmitter systems.

Fear & stress:

Among healthy young men, the blood oxygen level-dependent (BOLD) response in the amygdala to fearful and angry faces co-varies positively with individual differences in serum testosterone concentrations ([63,64], but see [65]). Exogenous testosterone has been shown to activate the amygdala in young women viewing angry facial expressions [66] (Figure 4). A mechanism underlying these observations might be that testosterone induces a functional decoupling between OFC and amygdala activity [67,68]…In humans, single acute doses of testosterone have been shown to reduce subconscious fear (Figure 5) and fear-potentiated startle [44,89].

…In face-to-face interactions, individuals are assumed to compete for status in fairly well-defined contests, each trying to ‘outstress’ the other with verbal and facial cues, and the fact that low-ranked members show more stress symptoms than higher-ranked members during mutual interaction is a common feature of status hierarchies [40]. Stress probably also plays an important role in anonymous competition. Hence, stress resilience might enable an individual to cope with a challenge adaptively. Studies in animals have confirmed that testosterone downregulates the hypothalamic-pituitary-adrenal stress response [90]. It has also been shown to attenuate the sympathetically mediated stress response to aversive stimuli in humans [91].

Motivation & learning:

Reward-based reinforcement effects in animals have been observed within short time periods (30 min) after systemic administration of testosterone [79], suggesting that a testosterone surge following a status-relevant social stimulus might reinforces any behavior that led to that testosterone response in the first place. In humans, patients who are hypogonadal (testosterone levels too low) show apathy and lack of motivation [80], whereas testosterone administration in healthy subjects induces motivation to act [81] and upregulates activity in the ventral striatum [82]

Summary of foregoing:

Testosterone administration studies confirm that the hormone also has fear-reducing properties in humans. A further important function of testosterone is its role in motivation; animal models have shown a tight link with the dopaminergic system within striatal areas. Thus, together with the ability to reduce fear and buffer stress responses, testosterone might have a pivotal role in promoting upward movement in a status hierarchy by facilitating the engagement in a competition for status. By contrast, testosterone can promote threat vigilance, which enables an individual to not only detect potential status challenges, but also, as a consequence of, and facilitated through the mechanisms detailed above, act accordingly to defend its high status position. These effects might be mediated by the amygdala

3 References

  • 01: Mazur, A. and Booth, A. (1998) Testosterone and dominance in men. Behav. Brain Sci. 21, 353–363 discussion 363–397

  • 03: Beeman, E.A. (1947) The relation of the interval between castration and 1st encounter to the aggressive behavior of mice. Anat. Rec. 99, 570–571

  • 08: Dabbs, J.M. et al. (1995) Testosterone, crime, and misbehavior among 692 male prison-inmates. Pers. Indiv. Differ. 18, 627–633

  • 11: Carre, J.M. et al. (2011) The social neuroendocrinology of human aggression. Psychoneuroendocrinology DOI: 10.1016/​J.PSYNEUEN. 2011.02.001

  • 12: Archer, J. et al. (2005) Testosterone and aggression: a reanalysis of Book, Starzyk, and Quinsey’s (2001) study. Aggress. Violent Behav. 10, 241–261

  • 13: Eisenegger, C. et al. (2010) Prejudice and truth about the effect of testosterone on human bargaining behaviour. Nature 463, 356–359

  • 14: Zethraeus, N. et al. (2009) A randomized trial of the effect of estrogen and testosterone on economic behavior. Proc. Natl. Acad. Sci. U.S.A. 106, 6535–6538

  • 16: Higley, J.D. et al. (1996) CSF testosterone and 5-HIAA correlate with different types of aggressive behaviors. Biol. Psychiatry 40, 1067–1082

  • 19: Vermeersch, H. et al. (2010) Gender ideology, same-sex peer group affiliation and the relationship between testosterone and dominance in adolescent boys and girls. J. Biosoc. Sci. 42, 463–475

  • 20: Rowe, R. et al. (2004) Testosterone, antisocial behavior, and social dominance in boys: pubertal development and biosocial interaction. Biol. Psychiatry 55, 546–552

  • 21: Grant, V.J. and France, J.T. (2001) Dominance and testosterone in women. Biol. Psychol. 58, 41–47

  • 22: Carre, J.M. et al. (2009) Testosterone responses to competition predict future aggressive behaviour at a cost to reward in men. Psychoneuroendocrinology 34, 561–570

  • 23: Stanton, S.J. and Schultheiss, O.C. (2009) The hormonal correlates of implicit power motivation. J. Res. Pers. 43, 942

  • 24: van Honk, J. et al. (1999) Correlations among salivary testosterone, mood, and selective attention to threat in humans. Horm. Behav. 36, 17–24

  • 25: Wirth, M.M. and Schultheiss, O.C. (2007) Basal testosterone moderates responses to anger faces in humans. Physiol. Behav. 90, 496–505

  • 26: Sellers, J.G. et al. (2007) Hormones and personality: testosterone as a marker of individual differences. J. Res. Pers. 41, 126–138

  • 27: Miller, S.L. and Maner, J.K. (2010) Scent of a woman: men’s testosterone responses to olfactory ovulation cues. Psychol. Sci. 21, 276–283

  • 28: Roney, J.R. et al. (2007) Rapid endocrine responses of young men to social interactions with young women. Horm. Behav. 52, 326–333

  • 29: Lopez, H.H. et al. (2009) Attractive men induce testosterone and cortisol release in women. Horm. Behav. 56, 84–92

  • 30: Wobber, V. et al. (2010) Differential changes in steroid hormones before competition in bonobos and chimpanzees. Proc. Natl. Acad. Sci. U.S.A. 107, 12457–12462

  • 31: Salvador, A. (2005) Coping with competitive situations in humans. Neurosci. Biobehav. Rev. 29, 195–205

  • 32: Mehta, P.H. and Josephs, R.A. (2006) Testosterone change after losing predicts the decision to compete again. Horm. Behav. 50, 684–692

  • 33: Oliveira, T. et al. (2009) Testosterone responsiveness to winning and losing experiences in female soccer players. Psychoneuroendocrinology 34, 1056–1064

  • 34: Josephs, R.A. et al. (2006) The mismatch effect: when testosterone and status are at odds. J. Pers. Soc. Psychol. 90, 999–1013

  • 35: Josephs, R.A. et al. (2003) Status, testosterone, and human intellectual performance: stereotype threat as status concern. Psychol. Sci. 14, 158–163

  • 36: Newman, M.L. et al. (2005) Testosterone, cognition, and social status. Horm. Behav. 47, 205–211

  • 37: Carre, J.M. and Putnam, S.K. (2010) Watching a previous victory produces an increase in testosterone among elite hockey players. Psychoneuroendocrinology 35, 475–479

  • 38: Schultheiss, O.C. et al. (2005) Effects of implicit power motivation on men’s and women’s implicit learning and testosterone changes after social victory or defeat. J. Pers. Soc. Psychol. 88, 174–188

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

  • 42: van Honk, J. and Schutter, D.J. (2007) Vigilant and avoidant responses to angry facial expressions. In Social Neuroscience: Integrating Biological and Psychological Explanations of Social Behavior (Harmon-Jones, E. and Winkielman, P., eds), pp. 197–223, The Guilford Press

  • 43: van Honk, J. et al. (2001) A single administration of testosterone induces cardiac accelerative responses to angry faces in healthy young women. Behav. Neurosci. 115, 238–242

  • 44: van Honk, J. et al. (2005) Testosterone reduces unconscious fear but not consciously experienced anxiety: implications for the disorders of fear and anxiety. Biol. Psychiatry 58, 218–225

  • 48: Hermans, E.J. et al. (2006) Testosterone administration reduces empathetic behavior: a facial mimicry study. Psychoneuroendocrinology 31, 859–866

  • 49: Van Honk, J. et al. (2011) Testosterone administration impairs cognitive empathy in women depending on second-to-fourth digit ratio. Proc. Natl. Acad. Sci. U.S.A. DOI: 10.1073/​pnas.1011891108

  • 51: Bos, P.A. et al. (2010) Testosterone decreases trust in socially naive humans. Proc. Natl. Acad. Sci. U.S.A. 107, 9991–9995

  • 55: 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

  • 56: Archer, J. (2006) Testosterone and human aggression: an evaluation of the challenge hypothesis. Neurosci. Biobehav. Rev. 30, 319–345

  • 57: Zak, P.J. et al. (2009) Testosterone administration decreases generosity in the ultimatum game. PLoS ONE 4, e8330

  • 58: Ronay, R. and Galinsky, A.D. (2011) Lex talionis: testosterone and the law of retaliation. J. Exp. Soc. Psychol. 47, 702–705

  • 63: Derntl, B. et al. (2009) Amygdala activity to fear and anger in healthy young males is associated with testosterone. Psychoneuroendocrinology 34, 687–693

  • 64: Manuck, S.B. et al. (2010) Salivary testosterone and a trinucleotide (CAG) length polymorphism in the androgen receptor gene predict amygdala reactivity in men. Psychoneuroendocrinology 35, 94–104

  • 65: Stanton, S.J. et al. (2009) Endogenous testosterone levels are associated with amygdala and ventromedial prefrontal cortex responses to anger faces in men but not women. Biol. Psychol. 81, 118–122

  • 66: Hermans, E.J. et al. (2008) Exogenous testosterone enhances responsiveness to social threat in the neural circuitry of social aggression in humans. Biol. Psychiatry 63, 263–270

  • 67: van Wingen, G. et al. (2010) Testosterone reduces amygdala-orbitofrontal cortex coupling. Psychoneuroendocrinology 35, 105–113

  • 68: Volman, I. et al. (2011) Endogenous testosterone modulates prefrontal-amygdala connectivity during social emotional behavior. Cereb. Cortex DOI: 10.1093/​cercor/​bhr001

  • 79: Nyby, J.G. (2008) Reflexive testosterone release: a model system for studying the nongenomic effects of testosterone upon male behavior. Front. Neuroendocrinol. 29, 199–210

  • 80: Bhasin, S. et al. (2006) Testosterone therapy in adult men with androgen deficiency syndromes: an endocrine society clinical practice guideline. J. Clin. Endocrinol. Metab. 91, 1995–2010

  • 81: Aarts, H. and van Honk, J. (2009) Testosterone and unconscious positive priming increase human motivation separately. Neuroreport 20, 1300–1303

  • 82: Hermans, E.J. et al. (2010) Effects of exogenous testosterone on the ventral striatal BOLD response during reward anticipation in healthy women. Neuroimage 52, 277–283

  • 89: Hermans, E.J. et al. (2006) A single administration of testosterone reduces fear-potentiated startle in humans. Biol. Psychiatry 59, 872–874

  • 90: Viau, V. (2002) Functional cross-talk between the hypothalamic-pituitary-gonadal and -adrenal axes. J. Neuroendocrinol. 14, 506–513

  • 91: Hermans, E.J. et al. (2007) Exogenous testosterone attenuates the integrated central stress response in healthy young women. Psychoneuroendocrinology 32, 1052–1061