P.2.003 - Endogenous testosterone modulates aggression-related fronto-amygdalar activation in police recruits

Abstract

The ability to regulate emotional actions is essential for adequate social behavior and largely depends on control from the prefrontal cortex (PFC) over the amygdala [1]. Optimal functioning of this circuitry is especially important for police officers, who regularly face emotionally challenging situations. Trait aggression has been associated with reduced prefrontal control over the amygdala in aggressive offenders [2], but it remains unclear whether such relationship holds for high functioning police officers who may have strong compensatory frontal control over their emotional tendencies. On the other hand, socially challenging situations can elicit an increase in testosterone levels [3], which may decrease emotional control abilities. Therefore, we tested whether trait aggression in police recruits is associated with increased rather than decreased prefrontal control over the amygdala. Moreover, we investigated whether this frontal control fails in the context of high state salivary testosterone. 275 healthy police recruits (209 males) participated in a functional MRI (3 Tesla) social-emotional task (the approach-avoidance task [2]) eliciting automatic (impulsive) and controlled actions. During the automatic condition, participants followed their automatic tendencies by approaching happy faces and avoiding angry faces, with pulling or pushing joystick movements, respectively. During the emotional control condition, participants made affect-incongruent responses, by avoiding happy faces and approaching angry faces. Before the scan session, salivary steroid hormone levels and self-reported aggression (Reactive-Proactive questionnaire, [4]) were assessed. The effects of aggression and testosterone on behavioral and neural (BOLD) measures of emotional control were analyzed using repeated measures ANOVA and multiple regression analyses, respectively. The bilateral amygdala and bilateral anterior PFC (aPFC) were used for a volume-of-interest analysis. A psycho-physiological interaction analysis was performed with the bilateral amygdala as seed region. In line with previous findings [5], participants showed increased reaction times, more errors and increased aPFC activation when they were required to control their automatic emotional actions. During this emotion control condition, higher levels of aggression were associated with relatively increased aPFC and relatively decreased amygdala activation. Moreover, salivary testosterone levels modulated this aggression-dependent aPFC recruitment: during emotional control, police recruits with relatively high trait aggression and high state testosterone showed reduced aPFC activation and reduced amygdala-aPFC functional connectivity. Aggression nor testosterone did modulate the emotional control effects on behavioral reaction times or error rate. These results indicate that trait aggression in police officers is associated with increased recruitment of the aPFC-amygdala network, which is involved in emotional action control. This suggests that relatively aggressive, but mentally healthy individuals are able to compensate their heightened emotional reactivity when required. However, if high trait aggression is coupled to high state testosterone levels, aPFC control over the amygdala is reduced. Therefore, the emotional control system in aggressive individuals may be more vulnerable in situations involving social challenge, which are known to increase testosterone levels. These findings provide an explanation for the paradox that police officers, who are selected for their high emotional control, may sometimes be hindered under emotionally challenging situations.