Aberrant social and cerebral responding in a competitive reaction time paradigm in criminal psychopaths Ralf Veit a, ⁎ ,1 , Martin Lotze b,1 , Sven Sewing a , Heiner Missenhardt c , Tilman Gaber a,d , Niels Birbaumer a,e a Institute of Medical Psychology and Behavioral Neurobiology, University of Tübingen, Germany b Functional Imaging Unit, Center for Diagnostic Radiology and Neuroradiology, University of Greifswald, Germany c Centre of Psychiatry, Forensic Department, Bad Schussenried, Germany d Max Planck Institute for Biological Cybernetics, Tübingen, Germany e Ospedale San Camillo, Instituto di Ricovero e Cura a Carattere Scientifico, Venezia, Italy abstract article info Article history: Received 27 July 2009 Revised 14 October 2009 Accepted 17 November 2009 Available online 4 December 2009 In a previous study (Lotze et al., 2007) we described dorsal medial prefrontal cortex (mPFC) activation in healthy subjects during retaliation in a competitive reaction time task. Interestingly, the less callous the subjects were, the more they responded with ventral mPFC-activation when watching the opponent suffering. In this study we used this paradigm to investigate behavioral and neural responding of ten criminal psychopathic individuals from a forensic psychiatric institution. In contrast to healthy subjects, who show reactive aggressive behavior of inflicting punishment with increasing intensity after experiencing an increasing amount of punishment from a yoked opponent, psychopathic participants did not react with comparable retaliation. However, when psychopaths punished with a high amount they showed increased activation in the hypothalamus, the lateral prefrontal cortex, the posterior cingulate cortex and the amygdala. The trait “physical aggression” showed a positive correlation with hypothalamic activation. Medial prefrontal areas, associated with emotional control and conflict management in healthy subjects performing this paradigm, were inactive in psychopathic subjects during retaliation. When psychopaths observed the yoked opponent being punished they showed increased activation in the dorsal and ventral medial prefrontal cortex, which was positively associated by impulsivity and antisocial behavior of Hare's psychopathy construct. This finding supports the notion that reactive aggression is more related to antisocial behavior and anger management than with emotional and interpersonal characteristics of psychopathy and suggests that two separate brain activation patterns seem to account for these two behavioral dispositions. © 2009 Elsevier Inc. All rights reserved. Introduction The competitive reaction time paradigm (Taylor, 1967) is an excellent methodology employed in the laboratory to study direct physical aggression. This task is a widely used valid measure of aggressive behavior, appropriate to induce reactive aggression in a laboratory setting (Giancola and Zeichner, 1995). In a previous study we used the Taylor paradigm (Lotze et al., 2007) and demonstrated that healthy subjects show increased activity in the medial prefrontal cortex (mPFC) when punishing after being provoked. We interpreted this activation as associated with guilt during performing an aggressive act. Interestingly, the activity of the dorsal part of the mPFC was correlated positively with the strength of the selected aversive stimulus during retaliation, whereas the ventral mPFC was activated independent of the applied stimulus strength. The ventral part was active while observing the suffering opponent. Subjects with higher total psychopathy scores based on the Levenson self report scale (LSRS; Levenson et al., 1995) exhibited less ventral mPFC activation. In light of the above, we were interested in the behavior and functional activation of criminal psychopaths during the performance of this reactive aggression paradigm. These subjects have severe problems in emotional learning and show a failure of differential emotionally conditioned responses in the limbic-prefrontal circuit during Pavlovian classical aversive conditioning (Veit et al., 2002; Birbaumer et al., 2005), and impairment in emotion processing and empathy (Mueller et al., 2003). This callous unconcern for feelings of others is associated with repeated violation of the rights of others as well as a disregard of social norms. It has been demonstrated that damage to orbital and ventrolateral frontal cortex is related to a heightened risk of aggression (Blair, 2006) and there are many studies showing a strong association between psychopathy and engagement in violent and aggressive NeuroImage 49 (2010) 3365–3372 ⁎ Corresponding author. Institut für Medizinische Psychologie und Verhaltensneur- obiologie, Eberhard-Karls-Universität Tübingen, Gartenstraβe 29; D-72074 Tübingen, Germany. Fax: +49 7071 295956. E-mail address: ralf.veit@uni-tuebingen.de (R. Veit). 1 These authors contributed equally to the work. 1053-8119/$ – see front matter © 2009 Elsevier Inc. All rights reserved. doi:10.1016/j.neuroimage.2009.11.040 Contents lists available at ScienceDirect NeuroImage journal homepage: www.elsevier.com/locate/ynimg