Social status & testosterone

by gwern 10 min read20th Oct 201139 comments


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

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