Testosterone biases the amygdala toward social threat approach

Abstract

Testosterone administration in human participants increased amygdala responses during threat approach and decreased it during threat avoidance.

Hormonal underpinnings of status conflict: Testosterone and cortisol are related to decisions and satisfaction in the hawk-dove game

“…This low-status prevention mechanism aligns with evidence suggesting that high-testosterone individuals are more comfortable in high-status positions and find low-status positions (e.g., defeat in competition) stressful and aversive Newman et al, 2005;Mehta et al, 2008). This interpretation is also consistent with growing evidence suggesting that exogenous testosterone administration in both men and women increases sensitivity to status threat cues and motivates dominant behaviors (e.g., van Honk et al, 2001;Hermans et al, 2006;Hermans et al, 2008;Wright et al, 2012;Bos et al, 2010Bos et al, , 2012Terburg et al, 2012;Boksem et al, 2013;Goetz et al, 2014;Enter et al, 2014;Radke et al, 2015;Mehta et al, 2015c). In contrast, low-testosterone individuals may find high-status positions uncomfortable and may actually prefer lower status as well as social cooperation (e.g., Wingfield et al, 1990;Josephs et al, 2006;Mehta et al, 2009;Wright et al, 2012;Edelstein et al, 2014).…”

“…More specifically, testosterone's association with decision-making in the hawk-dove game may be explained by activity in neural regions implicated in threat processing (amygdala) as well as self-regulation and impulse control (orbitofrontal cortex). Testosterone enhances amygdala reactivity (Hermans et al, 2008;Gospic et al, 2011;Goetz et al, 2014;Radke et al, 2015), reduces orbitofrontal cortex activity (Mehta and Beer, 2010), and disrupts amygdala-prefrontal cortex connectivity in response to social threat cues (van Wingen et al, 2010;Volman et al, 2011). These neural mechanisms have all been associated with testosterone-dependent aggressive and dominant behaviors .…”

“…Research in humans also demonstrates connections between testosterone and status-seeking behavior (for reviews, see Mazur and Booth, 1998;Archer, 2006;Eisenegger et al, 2011;Hamilton et al, 2015). Both endogenous testosterone and exogenously elevated testosterone are positively related to markers of dominance motivation (van Honk et al, 2001;Schultheiss et al, 2005;Josephs et al, 2006;Hermans et al, 2008;Bos et al, 2012;Terburg et al, 2012;Terburg and van Honk, 2013;Goetz et al, 2014;Enter et al, 2014;Radke et al, 2015;Mehta et al, 2008;Zilioli and Watson, 2013;van der Meij et al, 2016), aggressive behavior (Carré et al, 2009;Carré and Olmstead, 2015), competitive behavior Carré and McCormick, 2008;Mehta et al, 2008Mehta et al, , 2009Slatcher et al, 2011;Mehta et al, 2015bMehta et al, , 2015cReimers and Diekhof, 2015;Hahn et al, 2016;Eisenegger et al, 2016), and reduced prosocial behaviors including trust, perspective-taking, cooperation, and empathy (Hermans et al, 2006;Mehta et al, 2009;Bos et al, 2010;van Honk et al, 2011;Boksem et al, 2013;Wright et al, 2012;Ronay and Carney, 2013;Edelstein et al, 2014).…”

Exogenous Testosterone Rapidly Increases Aggressive Behavior in Dominant and Impulsive Men

“…These findings parallel evidence in women in which a single administration of T increases amygdala and hypothalamic reactivity to angry facial expressions (19)(20)(21). Notably, these subcortical brain structures are rich in both androgen and estrogen receptors (22)(23)(24) and play a key role in potentiating reactive aggression in animal models (1,25).…”

“…The finding that trait dominance and self-control both interacted with drug condition and explained unique variance in aggressive behavior suggests that distinct neural mechanisms may underlie the aggression-potentiating effects of T. It has been hypothesized that heightened amygdala reactivity to social signals of threat and/or social provocation may mediate the link between T and human aggression (3,27,(47)(48). Consistent with this idea, experimental work indicates that exogenous T potentiates amygdala reactivity to angry faces (18)(19)(20)(21), promotes prolonged eye gaze toward masked angry facial expressions (49), and heightened amygdala reactivity to social provocation positively predicts aggressive behavior (50). Notably, people scoring high on measures that tap into the construct of trait dominance (e.g., behavioral activation system; interpersonal/affective dimensions of psychopathy) also demonstrate heightened amygdala reactivity to angry facial expressions (51)(52) and demonstrate prolonged eye gaze toward masked angry faces (53).…”