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Callous-unemotional traits drive reduced white-matter integrity in youths with conduct problems

  • A. L. Breeden (a1), E. M. Cardinale (a1), L. M. Lozier (a2), J. W. VanMeter (a2) and A. A. Marsh (a1)...
Abstract
Background.

Callous-unemotional (CU) traits represent a significant risk factor for severe and persistent conduct problems in children and adolescents. Extensive neuroimaging research links CU traits to structural and functional abnormalities in the amygdala and ventromedial prefrontal cortex. In addition, adults with psychopathy (a disorder for which CU traits are a developmental precursor) exhibit reduced integrity in uncinate fasciculus, a white-matter (WM) tract that connects prefrontal and temporal regions. However, research in adolescents has not yet yielded similarly consistent findings.

Method.

We simultaneously modeled CU traits and externalizing behaviors as continuous traits, while controlling for age and IQ, in order to identify the unique relationship of each variable with WM microstructural integrity, assessed using diffusion tensor imaging. We used tract-based spatial statistics to evaluate fractional anisotropy, an index of WM integrity, in uncinate fasciculus and stria terminalis in 47 youths aged 10–17 years, of whom 26 exhibited conduct problems and varying levels of CU traits.

Results.

Whereas both CU traits and externalizing behaviors were negatively correlated with WM integrity in bilateral uncinate fasciculus and stria terminalis/fornix, simultaneously modeling both variables revealed that these effects were driven by CU traits; the severity of externalizing behavior was not related to WM integrity after controlling for CU traits.

Conclusions.

These results indicate that WM abnormalities similar to those observed in adult populations with psychopathy may emerge in late childhood or early adolescence, and may be critical to understanding the social and affective deficits observed in this population.

Copyright
Corresponding author
* Address for correspondence: Dr A. A. Marsh, Department of Psychology, Georgetown University, 37th and O Streets NW, Washington, DC 20057, USA. (Email: aam72@georgetown.edu)
References
Hide All
Achenbach, TM (1991). Integrative Guide for the 1991 CBCL/4-18, Ysr, and Trf Profiles. University of Vermont/Department of Psychiatry: Burlington, VT.
Anastassiou-Hadjicharalambous, X, Warden, D (2008). Physiologically-indexed and self-perceived affective empathy in Conduct-Disordered children high and low on Callous-Unemotional traits. Child Psychiatry and Human Development 39, 503517.
Andershed, H, Gustafson, SB, Kerr, M, Stattin, H (2002). The usefulness of self-reported psychopathy-like traits in the study of antisocial behaviour among non-referred adolescents. European Journal of Personality 16, 383402.
Aoki, Y, Abe, O, Nippashi, Y, Yamasue, H (2013). Comparison of white matter integrity between autism spectrum disorder subjects and typically developing individuals: a meta-analysis of diffusion tensor imaging tractography studies. Molecular Autism 4, 25.
Babinski, LM, Hartsough, CS, Lambert, NM (1999). Childhood conduct problems, hyperactivity-impulsivity, and inattention as predictors of adult criminal activity. Journal of Child Psychology and Psychiatry, and Allied Disciplines 40, 347355.
Barry, CT, Frick, PJ, DeShazo, TM, McCoy, MG, Ellis, M, Loney, BR (2000). The importance of callous-unemotional traits for extending the concept of psychopathy to children. Journal of Abnormal Psychology 109, 335340.
Blair, RJR (2007). The amygdala and ventromedial prefrontal cortex in morality and psychopathy. Trends in Cognitive Sciences 11, 387392.
Breiman, L, Freedman, D (1983). How many variables should be entered in a regression equation? Journal of the American Statistical Association 78, 131136.
Byrd, AL, Loeber, R, Pardini, DA (2012). Understanding desisting and persisting forms of delinquency: the unique contributions of disruptive behavior disorders and interpersonal callousness. Journal of Child Psychology and Psychiatry 53, 371380.
Cardinal, RN, Parkinson, JA, Hall, J, Everitt, BJ (2002). Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex. Neuroscience and Biobehavioral Reviews 26, 321352.
Craig, MC, Catani, M, Deeley, Q, Latham, R, Daly, E, Kanaan, R, Picchioni, M, McGuire, PK, Fahy, T, Murphy, DGM (2009). Altered connections on the road to psychopathy. Molecular Psychiatry 14, 946953.
Crowe, SL, Blair, RJR (2008). The development of antisocial behavior: what can we learn from functional neuroimaging studies? Development and Psychopathology 20, 11451159.
Davis, M, Walker, DL, Lee, Y (1997). Amygdala and bed nucleus of the stria terminalis: differential roles in fear and anxiety measured with the acoustic startle reflex. Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences 352, 16751687.
De Brito, SA, McCrory, EJ, Mechelli, A, Wilke, M, Jones, AP, Hodgins, S, Viding, E (2011). Small, but not perfectly formed: decreased white matter concentration in boys with psychopathic tendencies. Molecular Psychiatry 16, 476477.
Decety, J, Chen, C, Harenski, C, Kiehl, KA (2013). An fMRI study of affective perspective taking in individuals with psychopathy: imagining another in pain does not evoke empathy. Frontiers in Human Neuroscience 7, 489.
Ekman, P, Friesen, W (1976). Pictures of Facial Affect. Consulting Psychologists: Palo Alto, CA.
Eyberg, SM, Nelson, MM, Boggs, SR (2008). Evidence-based psychosocial treatments for children and adolescents with disruptive behavior. Journal of Clinical Child and Adolescent Psychology 37, 215237.
Finger, EC, Marsh, A, Blair, KS, Majestic, C, Evangelou, I, Gupta, K, Schneider, MR, Sims, C, Pope, K, Fowler, K, Sinclair, S, Tovar-Moll, F, Pine, D, Blair, RJ (2012). Impaired functional but preserved structural connectivity in limbic white matter tracts in youth with conduct disorder or oppositional defiant disorder plus psychopathic traits. Psychiatry Research 202, 239244.
Finger, EC, Marsh, AA, Mitchell, DG, Reid, ME, Sims, C, Budhani, S, Kosson, DS, Chen, G, Towbin, KE, Leibenluft, E, Pine, DS, Blair, JR (2008). Abnormal ventromedial prefrontal cortex function in children with psychopathic traits during reversal learning. Archives of General Psychiatry 65, 586594.
Frick, PJ (2012). Developmental pathways to conduct disorder: implications for future directions in research, assessment, and treatment. Journal of Clinical Child and Adolescent Psychology 41, 378389.
Frick, PJ, Hare, RD (2001). The Antisocial Process Screening Device. Multi-Health Systems: Toronto, Ontario, Canada.
Frick, PJ, Moffitt, TE (2010). A Proposal to the DSM-V Childhood Disorders and the ADHD and Disruptive Behavior Disorders Work Groups to Include a Specifier to the Diagnosis of Conduct Disorder based on the Presence of Callous-Unemotional Traits. American Psychiatric Association: Washington, DC.
Frick, PJ, White, SF (2008). Research review: the importance of callous-unemotional traits for developmental models of aggressive and antisocial behavior. Journal of Child Psychology and Psychiatry, and Allied Disciplines 49, 359375.
Glenn, AL, Raine, A, Schug, RA (2009). The neural correlates of moral decision-making in psychopathy. Molecular Psychiatry 14, 56.
Goodman, R, Scott, S (1999). Comparing the strengths and difficulties questionnaire and the child behavior checklist: is small beautiful? Journal of Abnormal Child Psychology 27, 1724.
Hafeman, DM, Chang, KD, Garrett, AS, Sanders, EM, Phillips, ML (2012). Effects of medication on neuroimaging findings in bipolar disorder: an updated review. Bipolar Disorders 14, 375410.
Haney-Caron, E, Caprihan, A, Stevens, MC (2014). DTI-measured white matter abnormalities in adolescents with Conduct Disorder. Journal of Psychiatric Research 48, 111120.
Harenski, CL, Harenski, KA, Shane, MS, Kiehl, KA (2010). Aberrant neural processing of moral violations in criminal psychopaths. Journal of Abnormal Psychology 119, 863874.
Hawes, DJ, Price, MJ, Dadds, MR (2014). Callous-unemotional traits and the treatment of conduct problems in childhood and adolescence: a comprehensive review. Clinical Child and Family Psychology Review 17, 248267.
Hayes, AF (2013). Introduction to Mediation, Moderation, and Conditional Process Analysis: A Regression-Based Approach, 1st edn. The Guilford Press: New York.
Hicks, BM, Patrick, CJ (2006). Psychopathy and negative emotionality: analyses of suppressor effects reveal distinct relations with emotional distress, fearfulness, and anger-hostility. Journal of Abnormal Psychology 115, 276287.
Hoppenbrouwers, SS, Nazeri, A, de Jesus, DR, Stirpe, T, Felsky, D, Schutter, DJLG, Daskalakis, ZJ, Voineskos, AN (2013). White matter deficits in psychopathic offenders and correlation with factor structure. PLoS ONE 8, e72375.
Jones, AP, Laurens, KR, Herba, CM, Barker, GJ, Viding, E(2009). Amygdala hypoactivity to fearful faces in boys with conduct problems and callous-unemotional traits. American Journal of Psychiatry 166, 95102.
Kahn, RE, Byrd, AL, Pardini, DA (2013). Callous-unemotional traits robustly predict future criminal offending in young men. Law and Human Behavior 37, 8797.
Kaufman, A, Kaufman, N (2004). Kaufman Brief Intelligence Test - Second Edition (KBIT-2). American Guidance Service: Circle Pines, MN.
Kazdin, AE (1995). Conduct Disorders in Childhood and Adolescence, 2nd edn. Sage Publications: London.
Kazdin, AE (2000). Treatments for aggressive and antisocial children. Child and Adolescent Psychiatric Clinics of North America 9, 841858.
Kimonis, ER, Frick, PJ, Skeem, JL, Marsee, MA, Cruise, K, Munoz, LC, Aucoin, KJ, Morris, AS (2008). Assessing callous-unemotional traits in adolescent offenders: validation of the Inventory of Callous-Unemotional Traits. International Journal of Law and Psychiatry 31, 241252.
Kyriakopoulos, M, Samartzis, L, Dima, D, Hayes, D, Corrigall, R, Barker, G, Correll, CU, Frangou, S (2011). P03-111 - Does antipsychotic medication affect white matter in schizophrenia and bipolar disorder? a review of diffusion tensor imaging literature. European Psychiatry 26 (Suppl. 1), 1280.
Le Bihan, D, Mangin, JF, Poupon, C, Clark, CA, Pappata, S, Molko, N, Chabriat, H (2001). Diffusion tensor imaging: concepts and applications. Journal of Magnetic Resonance Imaging 13, 534546.
Lozier, LM, Cardinale, EM, VanMeter, JW, Marsh, AA (2014). Mediation of the relationship between callous-unemotional traits and proactive aggression by amygdala response to fear among children with conduct problems. JAMA Psychiatry 71, 627636.
Marsh, AA, Finger, EC, Mitchell, DGV, Reid, ME, Sims, C, Kosson, DS, Towbin, KE, Leibenluft, E, Pine, DS, Blair, RJR (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.
Marsh, AA, Finger, EC, Schechter, JC, Jurkowitz, ITN, Reid, ME, Blair, RJR (2011). Adolescents with psychopathic traits report reductions in physiological responses to fear. Journal of Child Psychology and Psychiatry, and Allied Disciplines 52, 834841.
Masi, G, Muratori, P, Manfredi, A, Lenzi, F, Polidori, L, Ruglioni, L, Muratori, F, Milone, A (2013). Response to treatments in youth with disruptive behavior disorders. Comprehensive Psychiatry 54, 10091015.
Meier, MH, Slutske, WS, Heath, AC, Martin, NG (2011). Sex differences in the genetic and environmental influences on childhood conduct disorder and adult antisocial behavior. Journal of Abnormal Psychology 120, 377388.
Moffitt, TE, Arseneault, L, Jaffee, SR, Kim-Cohen, J, Koenen, KC, Odgers, CL, Slutske, WS, Viding, E (2008). Research review: DSM-V conduct disorder: research needs for an evidence base. Journal of Child Psychology and Psychiatry, and Allied Disciplines 49, 3.
Mori, S, Wakana, S, van Zijl, PCM, Nagae-Poetscher, LM (2005). MRI Atlas of Human White Matter. Elsevier: Amsterdam.
Motzkin, JC, Newman, JP, Kiehl, KA, Koenigs, M (2011). Reduced prefrontal connectivity in psychopathy. The Journal of Neuroscience 31, 1734817357.
Oishi, K, Faria, AV, Hsu, J, Tippett, D, Mori, S, Hillis, AE (2015). Critical role of the right uncinate fasciculus in emotional empathy. Annals of Neurology 77, 6874.
Oishi, K, Zilles, K, Amunts, K, Faria, A, Jiang, H, Li, X, Akhter, K, Hua, K, Woods, R, Toga, AW, Pike, GB, Rosa-Neto, P, Evans, A, Zhang, J, Huang, H, Miller, MI, van Zijl, PCM, Mazziotta, J, Mori, S (2008). Human brain white matter atlas: identification and assignment of common anatomical structures in superficial white matter. NeuroImage 43, 447457.
Pardini, DA (2006). The callousness pathway to severe violent delinquency. Aggressive Behavior 32, 590598.
Pardini, D, Frick, PJ (2013). Multiple developmental pathways to conduct disorder: current conceptualizations and clinical implications. Journal of the Canadian Academy of Child and Adolescent Psychiatry 22, 2025.
Passamonti, L, Fairchild, G, Fornito, A, Goodyer, IM, Nimmo-Smith, I, Hagan, CC, Calder, AJ (2012). Abnormal anatomical connectivity between the amygdala and orbitofrontal cortex in conduct disorder. PLoS ONE 7, e48789.
Petrides, M, Pandya, DN (2007). Efferent association pathways from the rostral prefrontal cortex in the macaque monkey. Journal of Neuroscience 27, 1157311586.
Roose, A, Bijttebier, P, Decoene, S, Claes, L, Frick, PJ (2010). Assessing the affective features of psychopathy in adolescence: a further validation of the inventory of callous and unemotional traits. Assessment 17, 4457.
Sarkar, S, Craig, MC, Catani, M, Dell'Acqua, F, Fahy, T, Deeley, Q, Murphy, DGM (2013). Frontotemporal white-matter microstructural abnormalities in adolescents with conduct disorder: a diffusion tensor imaging study. Psychological Medicine 43, 401411.
Seara-Cardoso, A, Viding, E, Lickley, RA, Sebastian, CL (in press). Neural responses to others’ pain vary with psychopathic traits in healthy adult males. Cognitive, Affective & Behavioral Neuroscience.
Sebastian, CL, McCrory, EJP, Cecil, CAM, Lockwood, PL, De Brito, SA, Fontaine, NMG, Viding, E (2012). Neural responses to affective and cognitive theory of mind in children with conduct problems and varying levels of callous-unemotional traits. Archives of General Psychiatry 69, 814822.
Sylvers, PD, Brennan, PA, Lilienfeld, SO (2011). Psychopathic traits and preattentive threat processing in children: a novel test of the fearlessness hypothesis. Psychological Science 22, 12801287.
Turgay, A (2004). Aggression and disruptive behavior disorders in children and adolescents. Expert Review of Neurotherapeutics 4, 623632.
Van Ewijk, H, Heslenfeld, DJ, Zwiers, MP, Buitelaar, JK, Oosterlaan, J (2012). Diffusion tensor imaging in attention deficit/hyperactivity disorder: a systematic review and meta-analysis. Neuroscience & Biobehavioral Reviews 36, 10931106.
Viding, E, Blair, RJR, Moffitt, TE, Plomin, R (2005). Evidence for substantial genetic risk for psychopathy in 7-year-olds. Journal of Child Psychology and Psychiatry, and Allied Disciplines 46, 592597.
Viding, E, Jones, AP, Frick, PJ, Moffitt, TE, Plomin, R (2008). Heritability of antisocial behaviour at 9: do callous-unemotional traits matter? Developmental Science 11, 1722.
Viding, E, Sebastian, CL, Dadds, MR, Lockwood, PL, Cecil, CAM, De Brito, SA, McCrory, EJ (2012). Amygdala response to preattentive masked fear in children with conduct problems: the role of callous-unemotional traits. The American Journal of Psychiatry 169, 11091116.
Walker, DL, Toufexis, DJ, Davis, M (2003). Role of the bed nucleus of the stria terminalis versus the amygdala in fear, stress, and anxiety. European Journal of Pharmacology 463, 199216.
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