Testosterone and cortisol have been proposed to influence aggressive behavior by altering the neu... more Testosterone and cortisol have been proposed to influence aggressive behavior by altering the neural processing of facial threat signals. However, this has not been investigated in direct social interactions. Here, we explored the joint impact of testosterone, cortisol, and brain reactivity to anger expressions on women's reactive aggression in the Social Threat Aggression Paradigm (STAP). The STAP is a competitive reaction time task in which the purported opponent displays either an angry or a neutral facial expression at the beginning of each trial and delivers increasingly loud sound blasts to the participants, successfully provoking them. Strikingly, salivary testosterone at scan-time was negatively related to both aggression and basolateral amygdala (BLA) reactivity to angry faces, whereas cortisol had no effect. When the opponent looked angry, BLA-orbitofrontal coupling was reduced, and BLA reactivity was positively related to aggression. The latter relationship was fully mediated by bilateral superior temporal gyrus (STG) activation. Our results thus support previous neurobiological models of aggression, and extend them by demonstrating that fast amygdala responses to threat modulate STG activity in order to favor aggressive retaliation. Furthermore, our study agrees with recent evidence underscoring a fear-reducing and strategically prosocial effect of testosterone on human social behavior. Reactive aggression is a phylogenetically ancient behavior by which organisms respond to threat or provocation with an overt intent to harm the attacker 1. Reactive-aggressive impulses are thought to arise from subcortical structures such as the amygdala and the periaqueductal gray, which are in turn regulated by the orbitofrontal cortex (OFC) and other prefrontal regions 2. The steroid hormones testosterone (T) and cortisol (C) have been suggested as important factors for the regulation of reactive aggression, and have been shown to act on the afore-mentioned brain areas by binding to androgen and glucocorticoid receptors, respectively 3–5. Both hormones are considered to have a mutually opposing action 6–8 , and this divide is also apparent in human social behavior: T generally favors approach and aggression, while C leads to fear and avoidance 9,10. This notion is supported by numerous findings in correlational 11–14 and experimental settings 15–17 , though not all evidence agrees. For instance, some studies in women have linked high, rather than low C concentrations with aggression 18,19 , and high T with prosocial behavior 20–22. Moreover, some controversy remains regarding whether state T and C predict aggression better than baseline values 23. Hence, the dynamics of the relationship between these hormones and aggression are still unclear, especially in women. Several functional magnetic resonance imaging (fMRI) studies have investigated how C and T influence the activity of brain regions involved in aggression. It has been postulated that amygdala activation in response to
The steroid hormone testosterone (T) has been suggested to influence reactive aggression upon its... more The steroid hormone testosterone (T) has been suggested to influence reactive aggression upon its action on the basolateralamygdala (BLA), a key brain region for threat detection. However, it is unclear whether T modulates resting-state functionalconnectivity (rsFC) of the BLA, and whether this predicts subsequent aggressive behavior. Aggressive interactions themselves,which often induce changes in T concentrations, could further alter BLA rsFC, but this too remains untested. Here we investi-gated the effect of endogenous T on rsFC of the BLA at baseline as well as after an aggressive encounter, and whether this wasrelated to behavioral aggression in healthy young women (n = 39). Pre-scan T was negatively correlated with basal rsFC betweenBLA and left superior temporal gyrus (STG; p < .001, p < .05 Family-Wise Error [FWE] cluster-level corrected), which in turnwas associated with increased aggression (r = .37, p = .020). BLA-STG coupling at rest might thus underlie hostile readiness inlow-T women. In addition, connectivity between the BLA and the right superior parietal lobule (SPL), a brain region involved inhigher-order perceptual processes, was reduced in aggressive participants (p < .001, p < .05 FWE cluster-level corrected). On theother hand, post-task increases in rsFC between BLA and medial orbitofrontal cortex (mOFC) were linked to reduced aggression(r = −.36, p = .023), consistent with the established notion that the mOFC regulates amygdala activity in order to curb aggressiveimpulses. Finally, competition-induced changes in T were associated with increased coupling between the BLA and the rightlateral OFC (p < .001, p < .05 FWE cluster-level corrected), but this effect was unrelated to aggression. We thus identifiedconnectivity patterns that prospectively predict aggression in women, and showed how aggressive interactions in turn impactthese neural systems.
Testosterone and cortisol have been proposed to influence aggressive behavior by altering the neu... more Testosterone and cortisol have been proposed to influence aggressive behavior by altering the neural processing of facial threat signals. However, this has not been investigated in direct social interactions. Here, we explored the joint impact of testosterone, cortisol, and brain reactivity to anger expressions on women's reactive aggression in the Social Threat Aggression Paradigm (STAP). The STAP is a competitive reaction time task in which the purported opponent displays either an angry or a neutral facial expression at the beginning of each trial and delivers increasingly loud sound blasts to the participants, successfully provoking them. Strikingly, salivary testosterone at scan-time was negatively related to both aggression and basolateral amygdala (BLA) reactivity to angry faces, whereas cortisol had no effect. When the opponent looked angry, BLA-orbitofrontal coupling was reduced, and BLA reactivity was positively related to aggression. The latter relationship was fully mediated by bilateral superior temporal gyrus (STG) activation. Our results thus support previous neurobiological models of aggression, and extend them by demonstrating that fast amygdala responses to threat modulate STG activity in order to favor aggressive retaliation. Furthermore, our study agrees with recent evidence underscoring a fear-reducing and strategically prosocial effect of testosterone on human social behavior. Reactive aggression is a phylogenetically ancient behavior by which organisms respond to threat or provocation with an overt intent to harm the attacker 1. Reactive-aggressive impulses are thought to arise from subcortical structures such as the amygdala and the periaqueductal gray, which are in turn regulated by the orbitofrontal cortex (OFC) and other prefrontal regions 2. The steroid hormones testosterone (T) and cortisol (C) have been suggested as important factors for the regulation of reactive aggression, and have been shown to act on the afore-mentioned brain areas by binding to androgen and glucocorticoid receptors, respectively 3–5. Both hormones are considered to have a mutually opposing action 6–8 , and this divide is also apparent in human social behavior: T generally favors approach and aggression, while C leads to fear and avoidance 9,10. This notion is supported by numerous findings in correlational 11–14 and experimental settings 15–17 , though not all evidence agrees. For instance, some studies in women have linked high, rather than low C concentrations with aggression 18,19 , and high T with prosocial behavior 20–22. Moreover, some controversy remains regarding whether state T and C predict aggression better than baseline values 23. Hence, the dynamics of the relationship between these hormones and aggression are still unclear, especially in women. Several functional magnetic resonance imaging (fMRI) studies have investigated how C and T influence the activity of brain regions involved in aggression. It has been postulated that amygdala activation in response to
The steroid hormone testosterone (T) has been suggested to influence reactive aggression upon its... more The steroid hormone testosterone (T) has been suggested to influence reactive aggression upon its action on the basolateralamygdala (BLA), a key brain region for threat detection. However, it is unclear whether T modulates resting-state functionalconnectivity (rsFC) of the BLA, and whether this predicts subsequent aggressive behavior. Aggressive interactions themselves,which often induce changes in T concentrations, could further alter BLA rsFC, but this too remains untested. Here we investi-gated the effect of endogenous T on rsFC of the BLA at baseline as well as after an aggressive encounter, and whether this wasrelated to behavioral aggression in healthy young women (n = 39). Pre-scan T was negatively correlated with basal rsFC betweenBLA and left superior temporal gyrus (STG; p < .001, p < .05 Family-Wise Error [FWE] cluster-level corrected), which in turnwas associated with increased aggression (r = .37, p = .020). BLA-STG coupling at rest might thus underlie hostile readiness inlow-T women. In addition, connectivity between the BLA and the right superior parietal lobule (SPL), a brain region involved inhigher-order perceptual processes, was reduced in aggressive participants (p < .001, p < .05 FWE cluster-level corrected). On theother hand, post-task increases in rsFC between BLA and medial orbitofrontal cortex (mOFC) were linked to reduced aggression(r = −.36, p = .023), consistent with the established notion that the mOFC regulates amygdala activity in order to curb aggressiveimpulses. Finally, competition-induced changes in T were associated with increased coupling between the BLA and the rightlateral OFC (p < .001, p < .05 FWE cluster-level corrected), but this effect was unrelated to aggression. We thus identifiedconnectivity patterns that prospectively predict aggression in women, and showed how aggressive interactions in turn impactthese neural systems.
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Papers by Christin Engelke