Neural Correlates of Social Cooperation and Non-Cooperation as a Function of Psychopathy


      Psychopathy is a disorder involving a failure to experience many emotions that are necessary for appropriate social behavior. In this study, we probed the behavioral, emotional, and neural correlates of psychopathic traits within the context of a dyadic social interaction.


      Thirty subjects were imaged with functional magnetic resonance imaging while playing an iterated Prisoner’s Dilemma game with human confederates who were outside the scanner. Subjects also completed two self-report psychopathy questionnaires.


      Subjects scoring higher on psychopathy, particularly males, defected more often and were less likely to continue cooperating after establishing mutual cooperation with a partner. Further, they experienced more outcomes in which their cooperation was not reciprocated (cooperate–defect outcome). After such outcomes, subjects scoring high in psychopathy showed less amygdala activation, suggesting weaker aversive conditioning to those outcomes. Compared with low-psychopathy subjects, subjects higher in psychopathy also showed weaker activation within orbitofrontal cortex when choosing to cooperate and showed weaker activation within dorsolateral prefrontal and rostral anterior cingulate cortex when choosing to defect.


      These findings suggest that whereas subjects scoring low on psychopathy have emotional biases toward cooperation that can only be overcome with effortful cognitive control, subjects scoring high on psychopathy have an opposing bias toward defection that likewise can only be overcome with cognitive effort.

      Key Words

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'


      Subscribe to Biological Psychiatry
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect


        • Angrilli A.
        • Mauri A.
        • Palomba D.
        • Flor H.
        • Birbaumer N.
        • Sartori G.
        • di Paola F.
        Startle reflex and emotion modulation impairment after a right amygdala lesion.
        Brain. 1996; 119: 1991-2000
        • Axelrod R.M.
        The Evolution of Cooperation. Basic Books, New York1984
        • Bechara A.
        The role of emotion in decision-making: Evidence from neurological patients with orbitofrontal damage.
        Brain Cogn. 2004; 55: 30-40
        • Bechara A.
        • Damasio H.
        • Damasio A.R.
        Emotion, decision making and the orbitofrontal cortex.
        Cereb Cortex. 2000; 10: 295-307
        • Bechara A.
        • Tranel D.
        • Damasio H.
        • Adolphs R.
        • Rockland C.
        • Damasio A.R.
        Double dissociation of conditioning and declarative knowledge relative to the amygdala and hippocampus in humans.
        Science. 1995; 269: 1115-1118
        • Benning S.D.
        • Patrick C.J.
        • Hicks B.M.
        • Blonigen D.M.
        • Krueger R.F.
        Factor structure of the Psychopathic Personality Inventory: Validity and implications for clinical assessment.
        Psychol Assess. 2003; 15: 340-350
        • Birbaumer N.
        • Veit R.
        • Lotze M.
        • Erb M.
        • Hermann C.
        • Grodd W.
        • Flor H.
        Deficient fear conditioning in psychopathy: A functional magnetic resonance imaging study.
        Arch Gen Psychiatry. 2005; 62: 799-805
        • Bishop S.
        • Duncan J.
        • Brett M.
        • Lawrence A.D.
        Prefrontal cortical function and anxiety: Controlling attention to threat-related stimuli.
        Nat Neurosci. 2004; 7: 184-188
        • Blair R.J.
        Neurobiological basis of psychopathy.
        Br J Psychiatry. 2003; 182: 5-7
        • Blair R.J.
        Applying a cognitive neuroscience perspective to the disorder of psychopathy.
        Dev Psychopathol. 2005; 17: 865-891
        • Cleckley H.
        The Mask of Sanity. Mosby, Augusta, GA1976
        • Davis M.
        Neurobiology of fear responses: The role of the amygdala.
        J Neuropsychiatry Clin Neurosci. 1997; 9: 382-402
        • Duvernoy H.M.
        The Human Brain: Surface, Blood Supply and Three-Dimensional Sectional Anatomy. Springer Wien New York, New York1999
        • Edens J.F.
        • Marcus D.K.
        • Lilienfeld S.O.
        • Poythress N.G.
        Psychopathic, not psychopath: Taxometric evidence for the dimensional structure of psychopathy.
        J Abnorm Psychol. 2006; 115: 131-144
        • Ericcson K.A.
        • Simon H.A.
        Verbal reports as data.
        Psychol Rev. 1980; 87: 215-251
        • Fehr E.
        • Fischbacher U.
        The nature of human altruism.
        Nature. 2003; 425: 785-791
        • Flor H.
        • Birbaumer N.
        • Hermann C.
        • Ziegler S.
        • Patrick C.J.
        Aversive Pavlovian conditioning in psychopaths: Peripheral and central correlates.
        Psychophysiology. 2002; 39: 505-518
        • Frank R.H.
        Passions Within Reason: The Strategic Role of the Emotions. 1st ed. Norton, New York1988
        • Gordon H.L.
        • Baird A.A.
        • End A.
        Functional differences among those high and low on a trait measure of psychopathy.
        Biol Psychiatry. 2004; 56: 516-521
        • Greene J.D.
        • Nystrom L.E.
        • Engell A.D.
        • Darley J.M.
        • Cohen J.D.
        The neural bases of cognitive conflict and control in moral judgment.
        Neuron. 2004; 44: 389-400
        • Hare R.D.
        Psychopathy and electrodermal responses to non signal stimulation.
        Biol Psychol. 1978; 6: 237-246
        • Hare R.D.
        Psychopaths and their nature: Implications for the mental health and criminal justice systems.
        in: Millon T. Simonsen E. Biket-Smith M. Davis R.D. Psychopathy: Antisocial, Criminal and Violent Behavior. Guilford Press, New York1998: 188-212
        • Hare R.D.
        • Harpur T.J.
        • Hakstian A.R.
        • Forth A.E.
        • Hart S.D.
        • Newman J.P.
        The Revised Psychopathy Checklist: Reliability and factor structure.
        Psychol Assess. 1990; 2: 338-341
        • Hare R.D.
        • Quinn M.J.
        Psychopathy and autonomic conditioning.
        J Abnorm Psychol. 1971; 77: 223-235
        • Kiehl K.A.
        • Smith A.M.
        • Hare R.D.
        • Mendrek A.
        • Forster B.B.
        • Brink J.
        • Liddle P.F.
        Limbic abnormalities in affective processing by criminal psychopaths as revealed by functional magnetic resonance imaging.
        Biol Psychiatry. 2001; 50: 677-684
        • Ledoux J.
        Fear and the brain: Where have we been, and where are we going?.
        Biol Psychiatry. 1998; 44: 1229-1238
        • Levenson M.R.
        • Kiehl K.A.
        • Fitzpatrick C.M.
        Assessing psychopathic attributes in a noninstitutionalized population.
        J Pers Soc Psychol. 1995; 68: 151-158
        • Levenston G.K.
        • Patrick C.J.
        • Bradley M.M.
        • Lang P.J.
        The psychopath as observer: Emotion and attention in picture processing.
        J Abnorm Psychol. 2000; 109: 373-385
        • Lilienfeld S.O.
        Assessment of antisocial behavior in adults.
        in: Stroff D. Brieding J. Maser J. Handbook of Antisocial Behavior. Wiley, New York1998: 60-74
        • Lilienfeld S.O.
        • Andrews B.P.
        Development and preliminary validation of a self-report measure of psychopathic personality traits in noncriminal populations.
        J Pers Assess. 1996; 66: 488-524
        • Lilienfeld S.O.
        • Fowler K.A.
        The self-report assessment of psychopathy: Problems, pitfalls, and promises.
        in: Patrick C.J. Handbook of Psychopathy. Guilford Press, New York2006: 107-132
        • Lilienfeld S.O.
        • Widows M.R.
        Professional Manual for the Psychopathic Personality Inventory–Revised: (PPI-R). Psychological Assessment Resources, Lutz, FL2005
        • Lykken D.T.
        A study of anxiety in the sociopathic personality.
        J Abnorm Psychol. 1957; 55: 6-10
        • Lynam D.R.
        • Whiteside S.
        • Jones S.
        Self-reported psychopathy: A validation study.
        J Pers Assess. 1999; 73: 110-132
        • Marcus D.K.
        • John S.L.
        • Edens J.F.
        A taxometric analysis of psychopathic personality.
        J Abnorm Psychol. 2004; 113: 626-635
        • McClure S.M.
        • Laibson D.I.
        • Loewenstein G.
        • Cohen J.D.
        Separate neural systems value immediate and delayed monetary rewards.
        Science. 2004; 306: 503-507
        • Miller E.
        • Cohen J.
        An integrative theory of prefrontal cortex function.
        Annu Rev Neurosci. 2001; 24: 167-202
        • Muller J.L.
        • Sommer M.
        • Wagner V.
        • Lange K.
        • Taschler H.
        • Roder C.H.
        • et al.
        Abnormalities in emotion processing within cortical and subcortical regions in criminal psychopaths: Evidence from a functional magnetic resonance imaging study using pictures with emotional content.
        Biol Psychiatry. 2003; 54: 152-162
        • Patrick C.J.
        Emotion and psychopathy: Startling new insights.
        Psychophysiology. 1994; 31: 319-330
        • Patrick C.J.
        • Bradley M.M.
        • Lang P.J.
        Emotion in the criminal psychopath: Startle reflex modulation.
        J Abnorm Psychol. 1993; 102: 82-92
        • Rilling J.K.
        • Gutman D.A.
        • Zeh T.R.
        • Pagnoni G.
        • Berns G.S.
        • Kilts C.D.
        A neural basis for social cooperation.
        Neuron. 2002; 35: 395-405
        • Rilling J.K.
        • Sanfey A.G.
        • Aronson J.A.
        • Nystrom L.E.
        • Cohen J.D.
        Opposing BOLD responses to reciprocated and unreciprocted altruism in putative reward pathways.
        Neuroreport. 2004; 15: 2539-2543
        • Sanfey A.G.
        • Rilling J.K.
        • Aronson J.A.
        • Nystrom L.E.
        • Cohen J.D.
        The neural basis of economic decision-making in the Ultimatum Game.
        Science. 2003; 300: 1755-1758
        • Talairach J.
        • Tournoux P.
        Co-Planar Stereotaxic Atlas of the Human Brain. Thieme Medical, New York1988
        • Tranel D.
        Emotion, decision making, and the ventromedial prefrontal cortex.
        in: Stuss D.T. Knight R.T. Principles of Frontal Lobe Function. Oxford University Press, New York2002: 338-353
        • Trivers R.L.
        The evolution of reciprocal altruism.
        Q Rev Biol. 1971; 46: 35-57
        • Veit R.
        • Flor H.
        • Erb M.
        • Hermann C.
        • Lotze M.
        • Grodd W.
        • Birbaumer N.
        Brain circuits involved in emotional learning in antisocial behavior and social phobia in humans.
        Neurosci Lett. 2002; 328: 233-236

      Linked Article

      • Erratum
        Biological PsychiatryVol. 67Issue 6
        • Preview
          An error has been discovered in “Neural Correlates of Social Cooperation and Non-Cooperation as a Function of Psychopathy” by Rilling et al., which appeared in Biological Psychiatry, Volume 61, Number 11 (2007;61:1260–1271). Factor 1 and factor 2 scores on the Psychopathic Personality Inventory (PPI) questionnaire were inadvertently interchanged in all of the statistical analyses. Therefore, correlation coefficients listed for PPI factor 1 and PPI factor 2 in Tables 1–7 should be reversed, i.e., correlation coefficients in the factor 1 column should be moved to the factor 2 column, and vice-versa.
        • Full-Text
        • PDF