title: Testosterone Modulates Altered Prefrontal Control of Emotional Actions in Psychopathic Offenders(1,2,3).
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.
authors.affiliation: Sobell Department of Motor Neuroscience and Movement Disorders, UCL Institute of Neurology, University College London, London WC1N 3BG, United Kingdom; Behavioural Science Institute, Radboud University Nijmegen, 6525 HR, Nijmegen, The Netherlands; Donders Institute for Brain, Cognition and Behavior, Radboud University Nijmegen, 6525 EN, Nijmegen, The Netherlands.
authors.forename: Inge
authors.identifier: 0000-0003-3467-1841
authors.initials: I
authors.lastname: Volman
authors.affiliation: Behavioural Science Institute, Radboud University Nijmegen, 6525 HR, Nijmegen, The Netherlands; Donders Institute for Brain, Cognition and Behavior, Radboud University Nijmegen, 6525 EN, Nijmegen, The Netherlands; Department of Psychiatry, UMC Sint Radboud, 6525 GA, Nijmegen, The Netherlands; Pompestichting, 6532 CN, Nijmegen, The Netherlands.
authors.forename: Anna Katinka Louise
authors.initials: AK
authors.lastname: von Borries
authors.affiliation: Pompestichting , 6532 CN, Nijmegen, The Netherlands.
authors.forename: Berend Hendrik
authors.initials: BH
authors.lastname: Bulten
authors.affiliation: Donders Institute for Brain, Cognition and Behavior, Radboud University Nijmegen, 6525 EN, Nijmegen, The Netherlands; Department of Psychiatry, UMC Sint Radboud, 6525 GA, Nijmegen, The Netherlands; Pompestichting, 6532 CN, Nijmegen, The Netherlands.
authors.forename: Robbert Jan
authors.initials: RJ
authors.lastname: Verkes
authors.affiliation: Donders Institute for Brain, Cognition and Behavior, Radboud University Nijmegen , 6525 EN, Nijmegen, The Netherlands.
authors.forename: Ivan
authors.identifier: 0000-0003-0936-3601
authors.initials: I
authors.lastname: Toni
authors.affiliation: Behavioural Science Institute, Radboud University Nijmegen, 6525 HR, Nijmegen, The Netherlands; Donders Institute for Brain, Cognition and Behavior, Radboud University Nijmegen, 6525 EN, Nijmegen, The Netherlands.
authors.forename: Karin
authors.identifier: 0000-0002-8863-8978
authors.initials: K
authors.lastname: Roelofs
mesh_terms: D000328:Adult; D000679:Amygdala / Q000503:physiopathology*; D000987:Antisocial Personality Disorder / Q000503:physiopathology*; D001931:Brain Mapping; D057237:Criminals / Q000523:psychology; D004644:Emotions / Q000502:physiology*; D005149:Facial Expression; D000066499:Facial Recognition / Q000502:physiology; D006801:Humans; D007206:Individuality; D008279:Magnetic Resonance Imaging; D008297:Male; D008875:Middle Aged; D009434:Neural Pathways / Q000503:physiopathology; D017397:Prefrontal Cortex / Q000503:physiopathology*; D012919:Social Behavior; D013739:Testosterone / Q000378:metabolism / Q000502:physiology*; D055815:Young Adult
chemical_list: D013739:Testosterone
keywords: amygdala; connectivity; emotion; fMRI; prefrontal; psychopathy