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Dissociation between affective sharing and emotion understanding in juvenile psychopaths

Published online by Cambridge University Press:  17 April 2012

Yawei Cheng
Affiliation:
National Yang-Ming University National Yang-Ming University Hospital
An-Yi Hung
Affiliation:
National Yang-Ming University
Jean Decety*
Affiliation:
University of Chicago
*
Address correspondence and reprint requests to: Jean Decety, Department of Psychology and Department of Psychiatry, University of Chicago, 5848 South University Avenue, Chicago, IL 60637; E-mail: decety@uchicago.edu.

Abstract

Empathy dysfunction is one of the core characteristics of youth with callous–unemotional (CU) traits. How such a dysfunction is associated with abnormal neural processing, however, remains to be determined. This study combined assessment of Hare Psychopathy Checklist Youth Version, pressure pain threshold, and event-related brain potentials elicited by the perception of people in pain in 15 young offenders with low CU traits (LCU), 13 with high CU traits (HCU), and 15 typically developing controls. Compared to the controls, LCU and HCU had higher pain thresholds. Although only the central late positive potential (LPP) was reduced in LCU, both the frontal N120 and central LPP were diminished in HCU. When exposed to situations in which someone was harmed by another, HCU retained the LPP, and this response was significantly correlated with their psychopathic traits and pain thresholds. Both groups had no deficit in sensorimotor resonance as assessed by mu suppression. These results demonstrate that youth with HCU exhibit atypical neural dynamics of pain empathy processing in the early stage of affective arousal, which is coupled with their relative insensitivity to actual pain. Their capacity to understand intentionality, however, was not affected. Such uncoupling between affective arousal and emotion understanding may contribute to instigating aggressive behaviors in juvenile psychopaths.

Type
Regular Articles
Copyright
Copyright © Cambridge University Press 2012

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References

Akitsuki, Y., & Decety, J. (2009). Social context and perceived agency affects empathy for pain: An event-related fMRI investigation. NeuroImage, 47, 722734.CrossRefGoogle ScholarPubMed
Benuzzi, F., Lui, F., Duzzi, D., Nichelli, P., & Porro, C. (2008). Does it look painful or disgusting? Ask your parietal and cingulate cortex. Journal of Neuroscience, 28, 923931.CrossRefGoogle ScholarPubMed
Bieri, D., Reeve, R. A., Champion, G. D., Addicoat, L., & Ziegler, J. B. (1990). The Faces Pain Scale for the self-assessment of the severity of pain experienced by children: Development, initial validation, and preliminary investigation for ratio scale properties. Pain, 41, 139150.CrossRefGoogle ScholarPubMed
Birbaumer, N., Veit, R., Lotze, M., Erb, M., Hermann, C., Grodd, W., & Flor, H. (2005). Deficient fear conditioning in psychopathy: A functional magnetic resonance imaging study. Archives of General Psychiatry, 62, 799805.CrossRefGoogle ScholarPubMed
Blair, K. S., Smith, B. W., Mitchell, D. G., Morton, J., Vythilingam, M., Pessoa, L., et al. (2007). Modulation of emotion by cognition and cognition by emotion. NeuroImage, 35, 430440.CrossRefGoogle ScholarPubMed
Blair, R. J. (1995). A cognitive developmental approach to mortality: Investigating the psychopath. Cognition, 57, 129.CrossRefGoogle ScholarPubMed
Blair, R. J. (2003). Facial expressions, their communicatory functions and neuro-cognitive substrates. Philosophical Transactions of the Royal Society B: Biological Sciences, 358, 561572.CrossRefGoogle ScholarPubMed
Blair, R. J. (2005). Responding to the emotions of others: Dissociating forms of empathy through the study of typical and psychiatric populations. Consciousness and Cognition, 14, 698718.CrossRefGoogle Scholar
Blair, R. J., Colledge, E., Murray, L., & Mitchell, D. G. (2001). A selective impairment in the processing of sad and fearful expressions in children with psychopathic tendencies. Journal of Abnormal Child Psychology, 29, 491498.CrossRefGoogle ScholarPubMed
Blair, R. J. R., & Blair, K. S. (2009). Empathy, morality, and social convention: Evidence from the study of psychopathy and other psychiatric disorders. In Decety, J. & Ickes, W. (Eds.), The social neuroscience of empathy (pp. 139152). Cambridge: MIT Press.CrossRefGoogle Scholar
Cacioppo, J. T., & Gardner, W. L. (1999). Emotion. Annual Review of Psychology, 50, 191214.CrossRefGoogle ScholarPubMed
Carretie, L., Hinojosa, J. A., Martin-Loeches, M., Mercado, F., & Tapia, M. (2004). Automatic attention to emotional stimuli: Neural correlates. Human Brain Mapping, 22, 290299.CrossRefGoogle ScholarPubMed
Cheng, Y., Chen, C., Lin, C. P., Chou, K. H., & Decety, J. (2010). Love hurts: An fMRI study. NeuroImage, 51, 923929.CrossRefGoogle ScholarPubMed
Cheng, Y., Lin, C. P., Liu, H. L., Hsu, Y. Y., Lim, K. E., Hung, D., et al. (2007). Expertise modulates the perception of pain in others. Current Biology, 17, 17081713.CrossRefGoogle ScholarPubMed
Cheng, Y., Yang, C. Y., Lin, C. P., Lee, P. L., & Decety, J. (2008). The perception of pain in others suppresses somatosensory oscillations: A magnetoencephalography study. NeuroImage, 40, 18331840.CrossRefGoogle ScholarPubMed
Cleckley, H. M. (1976). The mask of sanity: An attempt to clarify some issues about the so-called psychopathic personality. St. Louis, MO: Mosby.Google Scholar
Cooke, D. J., & Michie, C. (1999). Psychopathy across cultures: North America and Scotland compared. Journal of Abnormal Psychology, 108, 5868.CrossRefGoogle ScholarPubMed
Cuthbert, B. N., Schupp, H. T., Bradley, M. M., Birbaumer, N., & Lang, P. J. (2000). Brain potentials in affective picture processing: Covariation with autonomic arousal and affective report. Biological Psychology, 52, 95111.CrossRefGoogle ScholarPubMed
Davidson, R. J., Putnam, K. M., & Larson, C. L. (2000). Dysfunction in the neural circuitry of emotion regulation—A possible prelude to violence. Science, 289, 591594.CrossRefGoogle ScholarPubMed
Davis, M. H. (1996). Empathy: A social psychological approach. Madison, WI: Westview Press.Google Scholar
Day, A., Casey, S., & Gerace, A. (2010). Interventions to improve empathy awareness in sexual and violent offenders: Conceptual, empirical, and clinical issues. Aggression and Violent Behavior, 15, 201208.CrossRefGoogle Scholar
de Wied, M., Gispen-de Wied, C., & van Boxtel, A. (2010). Empathy dysfunction in children and adolescents with disruptive behavior disorders. European Journal of Pharmacology, 626, 97103.CrossRefGoogle ScholarPubMed
Decety, J. (2010a). To what extent is the experience of empathy mediated by shared neural circuits? Emotion Review, 2, 204207.CrossRefGoogle Scholar
Decety, J. (2010b). The neurodevelopment of empathy in humans. Developmental Neuroscience, 32, 257267.CrossRefGoogle ScholarPubMed
Decety, J. (2011). Dissecting the neural mechanisms mediating empathy. Emotion Review, 3, 92108.CrossRefGoogle Scholar
Decety, J., & Jackson, P. L. (2004). The functional architecture of human empathy. Behavioral and Cognitive Neuroscience Reviews, 3, 71100.CrossRefGoogle ScholarPubMed
Decety, J., & Meyer, M. (2008). From emotion resonance to empathic understanding: A social developmental neuroscience account. Development and Psychopathology, 20, 10531080.CrossRefGoogle ScholarPubMed
Decety, J., & Michalska, K. J. (2010). Neurodevelopmental changes in the circuit underlying empathy and sympathy from childhood to adulthood. Developmental Science, 13, 886899.CrossRefGoogle ScholarPubMed
Decety, J., Michalska, K. J., & Akitsuki, Y. (2008). Who caused the pain? An fMRI investigation of empathy and intentionality in children. Neuropsychologia, 46, 26072614.CrossRefGoogle ScholarPubMed
Decety, J., Michalska, K. J., Akitsuki, Y., & Lahey, B. B. (2009). Atypical empathic responses in adolescents with aggressive conduct disorder: A functional MRI investigation. Biological Psychology, 80, 203211.CrossRefGoogle ScholarPubMed
Decety, J., Michalska, K. J., & Kinzler, K. D. (2011). The developmental neuroscience of moral sensitivity. Emotion Review, 3, 305307.CrossRefGoogle Scholar
Decety, J., Yang, C. Y., & Cheng, Y. (2010). Physicians down-regulate their pain empathy response: An event-related brain potential study. NeuroImage, 50, 16761682.CrossRefGoogle ScholarPubMed
Dennis, T. A., & Hajcak, G. (2009). The late positive potential: A neurophysiological marker for emotion regulation in children. Journal of Child Psychology and Psychiatry, 50, 13731383.CrossRefGoogle ScholarPubMed
Doallo, S., Cadaveira, F., & Rodriguez Holguin, S. (2007). Time course of attentional modulations on automatic emotional processing. Neuroscience Letter, 418, 111116.CrossRefGoogle ScholarPubMed
Dolan, M., & Fullam, R. (2004). Theory of mind and mentalizing ability in antisocial personality disorders with and without psychopathy. Psychological Medicine, 34, 10931102.CrossRefGoogle ScholarPubMed
Eisenberg, M. E., & Aalsma, M. C. (2005). Bullying and peer victimization: Position paper of the Society for Adolescent Medicine. Journal of Adolescent Health, 36, 8891.CrossRefGoogle ScholarPubMed
Fan, Y., & Han, S. (2008). Temporal dynamic of neural mechanisms involved in empathy for pain: An event-related brain potential study. Neuropsychologia, 46, 160173.CrossRefGoogle ScholarPubMed
Fan, Y. T., Decety, J., Yang, C. Y., Liu, J. L., & Cheng, Y. (2010). Unbroken mirror neurons in autism spectrum disorders. Journal of Child Psychology and Psychiatry, 51, 981988.CrossRefGoogle ScholarPubMed
Forth, A. E., Kosson, D. S., & Hare, R. D. (2003). The Hare Psychopathy Checklist: Youth version. Technical manual. Toronto, Canada: Multi-Health Systems.Google Scholar
Frick, P. J., & White, S. F. (2008). Research review: The importance of callous–unemotional traits for developmental models of aggressive and antisocial behavior. Journal of Child Psychology and Psychiatry, 49, 359375.CrossRefGoogle ScholarPubMed
Frick, P. J., & Viding, E. (2009). Antisocial behavior from a developmental psychopathology perspective. Development and Psychopathology, 21, 11111131.CrossRefGoogle ScholarPubMed
Gao, Y., & Raine, A. (2009). P3 event-related potential impairments in antisocial and psychopathic individuals: A meta-analysis. Biological Psychology, 82, 199210.CrossRefGoogle ScholarPubMed
Ghashghaei, H. T., & Barbas, H. (2002). Pathways for emotion: Interactions of prefrontal and anterior temporal pathways in the amygdala of the rhesus monkey. Neuroscience, 115, 12611279.CrossRefGoogle ScholarPubMed
Hajcak, G., Moser, J. S., & Simons, R. F. (2006). Attending to affect: Appraisal strategies modulate the electrocortical response to arousing pictures. Emotion, 6, 517522.CrossRefGoogle ScholarPubMed
Hajcak, G., & Nieuwenhuis, S. (2006). Reappraisal modulates the electrocortical response to unpleasant pictures. Cognitive, Affective, and Behavioral Neuroscience, 6, 291297.CrossRefGoogle ScholarPubMed
Han, S., Fan, Y., & Mao, L. (2008). Gender difference in empathy for pain: An electrophysiological investigation. Brain Research, 1196, 8593.CrossRefGoogle ScholarPubMed
Hare, R., Glass, S. J., & Newman, J. P. (2006). Current perspectives on psychopathy. Annual Review of Clinical Psychology, 4, 207246.Google Scholar
Hastings, P. D., Zahn-Waxler, C., Robinson, J., Usher, B., & Bridges, D. (2000). The development of concern for others in children with behavior problems. Developmental Psychology, 36, 531546.CrossRefGoogle ScholarPubMed
Herpertz, S. C., Huebner, T., Marx, I., Vloet, T. D., Fink, G. R., Stoecker, T., et al. (2008). Emotional processing in male adolescents with childhood-onset conduct disorder. Journal of Child Psychology and Psychiatry, 49, 781791.CrossRefGoogle ScholarPubMed
Hicks, B. M., Bernat, E., Malone, S. M., Iacono, W. G., Patrick, C. J., Krueger, R. F., et al. (2007). Genes mediate the association between P3 amplitude and externalizing disorders. Psychophysiology, 44, 98105.CrossRefGoogle ScholarPubMed
Hildebrain, D., & Pithers, W. D. (1989). Enhancing offender empathy for sexual abuse victims. In Laws, D. R. (Ed.), Relapse prevention with sex offenders (pp. 236243). New York: Guilford Press.Google Scholar
Jackson, P. L., Meltzoff, A. N., & Decety, J. (2005). How do we perceive the pain of others: A window into the neural processes involved in empathy. NeuroImage, 24, 771779.CrossRefGoogle ScholarPubMed
Jackson, P. L., Rainville, P., & Decety, J. (2006). To what extent do we share the pain of others? Insight from the neural bases of pain empathy. Pain, 125, 59.CrossRefGoogle ScholarPubMed
Jones, A. P., Laurens, K. R., Herba, C. M., Barker, G. J., & Viding, E. (2009). Amygdala hypoactivity to fearful faces in boys with conduct problems and callous–unemotional traits. American Journal of Psychiatry, 166, 95102.CrossRefGoogle ScholarPubMed
Kiehl, K. A., Smith, A. M., Hare, R. D., Mendrek, A., Forster, B. B., Brink, J., et al. (2001). Limbic abnormalities in affective processing by criminal psychopaths as evealed by functional magnetic resonance imaging. Biological Psychiatry, 50, 677684.CrossRefGoogle Scholar
Kosson, D. S., Lorenz, A. R., & Newman, J. P. (2006). Effects of comorbid psychopathy on criminal offending and emotion processing in male offenders with antisocial personality disorder. Journal of Abnormal Psychology, 115, 798806.CrossRefGoogle ScholarPubMed
Lahey, B. B., & Waldman, I. D. (2003). A developmental propensity model of the origins of conduct problems during childhood and adolescence. In Lahey, B. B., Moffitt, T. E., & Caspi, A. (Eds.), Causes of conduct disorder and juvenile delinquency (pp. 76117). New York: Guilford Press.Google Scholar
Lamm, C., Batson, C. D., & Decety, J. (2007). The neural substrate of human empathy: Effects of perspective-taking and cognitive appraisal. Journal of Cognitive Neuroscience, 19, 4258.CrossRefGoogle ScholarPubMed
Lamm, C., Decety, J., & Singer, T. (2011). Meta-analytic evidence for common and distinct neural networks associated with directly experienced pain and empathy for pain. NeuroImage, 54, 24922502.CrossRefGoogle ScholarPubMed
Loney, B. R., Butler, M. A., Lima, E. N., Counts, C. A., & Eckel, L. A. (2006). The relation between salivary cortisol, callous–unemotional traits, and conduct problems in an adolescent non-referred sample. Journal of Child Psychology and Psychiatry, 47, 3036.CrossRefGoogle Scholar
Loney, B. R., Frick, P. J., Clements, C. B., Ellis, M. L., & Kerlin, K. (2003). Callous–unemotional traits, impulsivity, and emotional processing in adolescents with antisocial behavior problems. Journal of Clinical Child and Adolescent Psychology, 32, 6680.CrossRefGoogle ScholarPubMed
Lynam, D. R., Charnigo, R., Moffitt, T. E., Raine, A., Loeber, R., & Stouthamer-Loeber, M. (2009). The stability of psychopathy across adolescence. Developmental Psychopathology, 21, 11331153.CrossRefGoogle ScholarPubMed
Marsh, A. A., Finger, E. C., Mitchell, D. G., Reid, M. E., Sims, C., Kosson, D. S., et al. (2008). Reduced amygdala response to fearful expressions in children and adolescents with callous–unemotional traits and disruptive behavior disorders. American Journal of Psychiatry, 165, 712720.CrossRefGoogle ScholarPubMed
Olofsson, J. K., Nordin, S., Sequeira, H., & Polich, J. (2008). Affective picture processing: An integrative review of ERP findings. Biological Psychology, 77, 247265.CrossRefGoogle ScholarPubMed
Palomba, D., Angrilli, A., & Mini, A. (1997). Visual evoked potentials, heart rate responses and memory to emotional pictorial stimuli. International Journal of Psychophysiology, 27, 5567.CrossRefGoogle ScholarPubMed
Pardini, D. A., Lochman, J. E., & Frick, P. J. (2003). Callous/unemotional traits and social–cognitive processes in adjudicated youths. Journal of the American Academy of Child & Adolescent Psychiatry, 42, 364371.CrossRefGoogle ScholarPubMed
Patrick, C. J., Bernat, E. M., Malone, S. M., Iacono, W. G., Krueger, R. F., & McGue, M. (2006). P300 amplitude as an indicator of externalizing in adolescent males. Psychophysiology, 43, 8492.CrossRefGoogle ScholarPubMed
Perry, A., & Bentin, S. (2010). Does focusing on hand grasping intentions modulate EEG mu and alpha suppression? NeuroReport, 21, 10501054.CrossRefGoogle Scholar
Pineda, J. A. (2005). The functional significance of mu rhythms: Translating “seeing” and “hearing” into “doing.” Brain Research Reviews, 50, 5768.CrossRefGoogle Scholar
Polich, J., & Comerchero, M. D. (2003). P3a from visual stimuli: Typicality, task, and topography. Brain Topography, 15, 141152.CrossRefGoogle ScholarPubMed
Raine, A. (1997). Antisocial behavior and psychophysiology: A biosocial perspective and a prefrontal dysfunction hypothesis. In Stoff, D. M., Breiling, J., & Maser, J. D. (Eds.), Handbook of antisocial behavior (pp. 289304). New York: Wiley.Google Scholar
Reese, C., & Polich, J. (2003). Alcoholism risk and the P300 event-related brain potential: Modality, task, and gender effects. Brain and Cognition, 53, 4657.CrossRefGoogle ScholarPubMed
Richell, R. A., Mitchell, D. G., Newman, C., Leonard, A., Baron-Cohen, S., & Blair, R. J. (2003). Theory of mind and psychopathy: Can psychopathic individuals read the ‘language of the eyes’? Neuropsychologia, 41, 523526.CrossRefGoogle ScholarPubMed
Rilling, J. K., Glenn, A. L., Jairam, M. R., Pagnoni, G., Goldsmith, D. R., Elfenbein, H. A., et al. (2007). Neural correlates of social cooperation and non-cooperation as a function of psychopathy. Biological Psychiatry, 61, 12601271.CrossRefGoogle ScholarPubMed
Schupp, H. T., Cuthbert, B. N., Bradley, M. M., Cacioppo, J. T., Ito, T., & Lang, P. J. (2000). Affective picture processing: The late positive potential is modulated by motivational relevance. Psychophysiology, 37, 257261.CrossRefGoogle ScholarPubMed
Semmlow, J. L. (2004). Biosignal and biomedical image processing: Matlab-based applications. Boca Raton, FL: CRC Press.Google Scholar
Shirtcliff, E. A., Vitacco, M. J., Graf, A. R., Gostisha, A. J., Merz, J. L., & Zahn-Waxler, C. (2009). Neurobiology of empathy and callousness: Implications for the development of antisocial behavior. Behavioral Sciences and the Law, 27, 137171.CrossRefGoogle ScholarPubMed
Singer, T., & Lamm, C. (2009). The social neuroscience of empathy. Annals of the New York Academy of Sciences, 1156, 8196.CrossRefGoogle ScholarPubMed
Sterzer, P., Stadler, C., Krebs, A., Kleinschmidt, A., & Poustka, F. (2005). Abnormal neural responses to emotional visual stimuli in adolescents with conduct disorder. Biological Psychiatry, 57, 715.CrossRefGoogle ScholarPubMed
Sterzer, P., Stadler, C., Poustka, F., & Kleinschmidt, A. (2007). A structural neural deficit in adolescents with conduct disorder and its association with lack of empathy. NeuroImage, 37, 335342.CrossRefGoogle ScholarPubMed
Taylor, J., Loney, B. R., Bobadilla, L., Iacono, W. G., & McGue, M. (2003). Genetic and environmental influences on psychopathy trait dimensions in a community sample of male twins. Journal of Abnormal Child Psychology, 31, 633645.CrossRefGoogle Scholar
Van Goozen, S. H. M., Fairchild, G., & Harold, G. T. (2008). The role of neurobiological deficits in childhood antisocial behavior. Current Directions in Psychological Science, 17, 224228.CrossRefGoogle Scholar
Van Heijnsbergen, C.C.R.J., Meeren, H.K.M., Grèzes, J., & de Gelder, B. (2007). Rapid detection of fear in body expressions, an ERP study. Brain Research, 1186, 233241.CrossRefGoogle ScholarPubMed
Viding, E., Blair, R. J., Moffitt, T. E., & Plomin, R. (2005). Evidence for substantial genetic risk for psychopathy in 7-year-olds. Journal of Child Psychology and Psychiatry, 46, 592597.CrossRefGoogle ScholarPubMed
Vuilleumier, P., & Pourtois, G. (2007). Distributed and interactive brain mechanisms during emotion face perception: Evidence from functional neuroimaging. Neuropsychologia, 45, 174194.CrossRefGoogle ScholarPubMed
Wismer Fries, A. B., & Pollak, S. (2009). Emotion processing and the developing brain. In Coch, D., Fisher, K. W., & Dawson, G. (Eds), Human behavior, learning, and the developing brain (pp. 329361). New York: Guilford Press.Google Scholar
Woodworth, M., & Waschbusch, D. (2008). Emotional processing in children with conduct problems and callous/unemotional traits. Child: Care, Health, and Development, 34, 234244.CrossRefGoogle ScholarPubMed
Yang, C. Y., Decety, J., Lee, S., Chen, C., & Cheng, Y. (2009). Gender differences in the mu rhythm during empathy for pain: An electroencephalographic study. Brain Research, 1251, 176184.CrossRefGoogle ScholarPubMed
Zahn-Waxler, C., & Radke-Yarrow, M. (1990). Origins of empathic concern. Motivation and Emotion, 14, 107130.CrossRefGoogle Scholar