Testosterone Modulates Altered Prefrontal Control of Emotional Actions in Psychopathic Offenders

Abstract

Psychopathic individuals are notorious for their controlled goal-directed aggressive behavior. Yet, during social challenges, they often show uncontrolled emotional behavior. Healthy individuals can control their social emotional behavior through anterior prefrontal cortex (aPFC) downregulation of neural activity in the amygdala, with testosterone modulating aPFC–amygdala coupling. This study tests whether individual differences in this neuroendocrine system relate to the paradoxical lack of emotional control observed in human psychopathic offenders. Emotional control was operationalized with an fMRI-adapted approach–avoidance task requiring rule-driven control over rapid emotional responses. Fifteen psychopathic offenders and 19 matched healthy control subjects made approaching and avoiding movements in response to emotional faces. Control of social emotional behavior was required during affect-incongruent trials, when participants had to override affect-congruent, automatic action tendencies and select the opposite response. Psychopathic offenders showed less control-related aPFC activity and aPFC–amygdala coupling during trials requiring control of emotional actions, when compared with healthy control subjects. This pattern was particularly pronounced in psychopathic individuals with high endogenous testosterone levels. These findings suggest that reduced prefrontal coordination underlies reduced behavioral control in psychopathic offenders during emotionally provoking situations. Even though the modest sample size warrants replication, the modulatory role of endogenous testosterone on the aPFC–amygdala circuit suggests a neurobiological substrate of individual differences that is relevant for the advancement of treatment and the reduction of recidivism.

Human lateral Frontal Pole contributes to control over social-emotional action

“…The findings have implications for structuring mechanism-based interventions in psychopathologies characterized by altered emotional control abilities, e.g. anxiety disorders and psychopathy (Volman et al 2016). The findings are also relevant for understanding the neurobiological and cognitive complexities underlying rule-based regulation of action tendencies, arguably a crucial pre-requisite for the development of human cumulative culture (Hare 2017; Whiten 2017).…”

A Systematic Literature Review of Neuroimaging of Psychopathic Traits

“…Functionally, increased activity in the medial prefrontal cortex and visual cortices were seen in psychopathic subjects in emotion recognition, whereas increased amygdalar activity was seen in healthy controls (51). In a similar vein, Volman et al (116) found decreased functional connectivity between the prefrontal cortex and amygdala in psychopathic subjects in a facial emotion recognition task. Moreover, psychopathic subjects exhibited decreased functional connectivity between bilateral visual prefrontal cortices and the left amygdala, indicative of persistent failure in incorporating emotion into cognition (51).…”

Are There Any Biomarkers for Pedophilia and Sexual Child Abuse? A Review

“…The testosterone-behavior relationship is rather thought to be subject to individual differences and contextual variables, i.e., testosterone influences aggression especially in high dominance men, in those men with low cortisol levels, and it can affect both aggression and prosocial behavior (97,98). In line with this, Volman et al (70) found that psychopathic offenders exhibited less control-related anterior prefrontal activity and anterior prefrontal-amygdala coupling in a task requiring control of emotional actions, when compared with healthy control subjects. This pattern was pronounced in psychopathic individuals with high endogenous testosterone levels (70).…”

“…According to the authors, these findings may support the theory of disturbed fronto-limbic functioning as a possible causal factor for child sexual offending regardless of pedophilia. Interestingly, a reduced fronto-limbic functional connectivity (as a response to provocations) has also been shown for violent and psychopathic offenders (69,70). From studies with healthy subjects, it is known that there is a strong top-down inhibitory control of prefrontal over limbic structures (especially amygdala), mediating responses to provocations [for review see: (71)].…”