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.

Highlights

  • Psychopathy is a disorder often associated with blunted emotional responding and increased goaldirected behavior (Blair, 2010; Anderson and Kiehl, 2012)

  • This study indicates that psychopathic offenders show reduced anterior prefrontal cortex (aPFC) activity as well as less aPFC–amygdala connectivity during the control of emotional behavior

  • The current study indicates that psychopathic individuals with especially high testosterone levels recruited the aPFC less when the control of emotional responses was needed

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Summary

Introduction

Psychopathy is a disorder often associated with blunted emotional responding and increased goaldirected behavior (Blair, 2010; Anderson and Kiehl, 2012). Offenders with psychopathy show a paradoxical increase in impulsive behavior and uncontrolled aggression after emotional provocations (Cornell et al, 1996; Hare, 2003; Patrick et al, 2005; Malterer et al, 2008; Blair, 2010; Anderson and Kiehl, 2012), which may be related to heightened testosterone levels (Stålenheim et al, 1998; Dolan et al, 2001). We study those neuroendocrine systems in a group of psychopathic offenders engaged in an experimental paradigm that requires ruledriven control of emotional behavior

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