Psychopathic tendency in violent offenders is associated with reduced aversive Pavlovian inhibition of behavior and associated striatal BOLD signal

Dirk E M Geurts; Katinka von Borries; Quentin J M Huys; Berend H Bulten; Robbert-Jan Verkes; Roshan Cools

doi:10.3389/fnbeh.2022.963776

Psychopathic tendency in violent offenders is associated with reduced aversive Pavlovian inhibition of behavior and associated striatal BOLD signal

Front Behav Neurosci. 2022 Oct 14:16:963776. doi: 10.3389/fnbeh.2022.963776. eCollection 2022.

Authors

Dirk E M Geurts^{1

2}, Katinka von Borries³, Quentin J M Huys⁴, Berend H Bulten³, Robbert-Jan Verkes^{1

3}, Roshan Cools^{1

2}

Affiliations

¹ Centre for Cognitive Neuroimaging, Donders Institute for Brain, Cognition and Behaviour, Radboud University, Nijmegen, Netherlands.
² Department of Psychiatry, Radboud University Medical Center, Nijmegen, Netherlands.
³ Pompestichting Center for Forensic Psychiatry, Pro Persona Mental Health, Nijmegen, Netherlands.
⁴ Division of Psychiatry and Max Planck UCL Centre for Computational Psychiatry and Ageing Research, Mental Health Neuroscience Department, Institute of Neurology, University College London, London, United Kingdom.

Abstract

Background: Violent offenders with psychopathic tendencies are characterized by instrumental, i.e., planned, callous, and unemotional (aggressive) behavior and have been shown to exhibit abnormal aversive processing. However, the consequences of abnormal aversive processing for instrumental action and associated neural mechanisms are unclear.

Materials and methods: Here we address this issue by using event-related functional magnetic resonance imaging (fMRI) in 15 violent offenders with high psychopathic tendencies and 18 matched controls during the performance of an aversive Pavlovian-to-instrumental transfer paradigm. This paradigm allowed us to assess the degree to which aversive Pavlovian cues affect instrumental action and associated neural signaling.

Results: Psychopathic tendency scores were associated with an attenuation of aversive Pavlovian inhibition of instrumental action. Moreover, exploratory analyses revealed an anomalous positive association between aversive inhibition of action and aversive inhibition of BOLD signal in the caudate nucleus of violent offenders with psychopathic tendencies. In addition, psychopathic tendency also correlated positively with amygdala reactivity during aversive versus neutral cues in Pavlovian training.

Conclusion: These findings strengthen the hypothesis that psychopathic tendencies in violent offenders are related to abnormal impact of aversive processing on instrumental behavior. The neural effects raise the possibility that this reflects deficient transfer of aversive Pavlovian inhibitory biases onto neural systems that implement instrumental action, including the caudate nucleus.

Keywords: Pavlovian-to-instrumental transfer; amygdala; caudate; fMRI; inhibition; psychopathy; putamen.