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Externalizing behavior severity in youths with callous–unemotional traits corresponds to patterns of amygdala activity and connectivity during judgments of causing fear

Published online by Cambridge University Press:  24 May 2017

Elise M. Cardinale*
Affiliation:
Georgetown University
Andrew L. Breeden
Affiliation:
Georgetown University
Emily L. Robertson
Affiliation:
Louisiana State University
Leah M. Lozier
Affiliation:
Georgetown University
John W. Vanmeter
Affiliation:
Georgetown University
Abigail A. Marsh
Affiliation:
Georgetown University
*
Address correspondence and reprint request to: Elise M. Cardinale, Department of Psychology, Georgetown University, 3700 O Street NW, Washington, DC 20057; E-mail: emc62@georgetown.edu.

Abstract

Callous–unemotional (CU) traits characterize a subgroup of youths with conduct problems who exhibit low empathy, fearlessness, and elevated externalizing behaviors. The current study examines the role of aberrant amygdala activity and functional connectivity during a socioemotional judgment task in youths with CU traits, and links these deficits to externalizing behaviors. Functional magnetic resonance imaging was used to compare neural responses in 18 healthy youths and 30 youths with conduct problems and varying levels of CU traits as they evaluated the acceptability of causing another person to experience each of several emotions, including fear. Neuroimaging analyses examined blood oxygenation level dependent responses and task-dependent functional connectivity. High-CU youths exhibited left amygdala hypoactivation relative to healthy controls and low-CU youths primarily during evaluations of causing others fear. CU traits moderated the relationship between externalizing behavior and both amygdala activity and patterns of functional connectivity. The present data suggest that CU youths' aberrant amygdala activity and connectivity affect how they make judgments about the acceptability of causing others emotional distress, and that these aberrations represent risk factors for externalizing behaviors like rule breaking and aggression. These findings suggest that reducing externalizing behaviors in high-CU youths may require interventions that influence affective sensitivity.

Type
Regular Articles
Copyright
Copyright © Cambridge University Press 2017 

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Footnotes

This research was supported by NIH/NICHD Grant R03 HD064906-01, the Georgetown-Howard Universities Center for Clinical and Translational Science (NIH/National Center for Advancing Translational Sciences Grant 1KL2RR031974-01), and the Intellectual and Developmental Disabilities Research Center at Children's National Medical Center (NIH/NICHD Grant 2P30HD040677-11).

References

Achenbach, T. M., & Rescorla, L. (2000). Child Behavior Checklist. Burlington, VT: University of Vermont.Google Scholar
Blair, R. J. (2005). Applying a cognitive neuroscience perspective to the disorder of psychopathy. Development and Psychopathology, 17, 865891.CrossRefGoogle Scholar
Blair, R. J. (2013). The neurobiology of psychopathic traits in youths. Nature Reviews Neuroscience, 14, 786799.CrossRefGoogle ScholarPubMed
Breeden, A. L., Cardinale, E. M., Lozier, L. M., VanMeter, J. W., & Marsh, A. A. (2015). Callous-unemotional traits drive reduced white-matter integrity in youths with conduct problems. Psychological Medicine, 45, 30333046.CrossRefGoogle ScholarPubMed
Cardinale, E. M., & Marsh, A. A. (2015). Impact of psychopathy on moral judgments about causing fear and physical harm. PLOS ONE, 10, e0125708.Google Scholar
Cohn, M. D., Popma, A., van den Brink, W., Pape, L. E., Kindt, M., van Domburgh, L., … Veltman, D. J. (2013). Fear conditioning, persistence of disruptive behavior and psychopathic traits: An fMRI study. Translational Psychiatry, 3, e319.Google Scholar
Dadds, M. R., El Masry, Y., Wimalaweera, S., & Guastella, A. J. (2008). Reduced eye gaze explains “fear blindness” in childhood psychopathic traits. Journal of the American Acadamy of Child & Adolescent Psychiatry, 47, 455463.Google Scholar
Dawel, A., O'Kearney, R., McKone, E., & Palermo, R. (2012). Not just fear and sadness: Meta-analytic evidence of pervasive emotion recognition deficits for facial and vocal expressions in psychopathy. Neuroscience & Biobehavioral Review, 36, 22882304.Google Scholar
De Brito, S. A., McCrory, E. J., Mechelli, A., Wilke, M., Jones, A. P., Hodgins, S., & Viding, E. (2011). Small, but not perfectly formed: Decreased white matter concentration in boys with psychopathic tendencies. Molecular Psychiatry, 16, 476477.Google Scholar
Decety, J., Skelly, L., Yoder, K. J., & Kiehl, K. A. (2014). Neural processing of dynamic emotional facial expressions in psychopaths. Social Neuroscience, 9, 3649.CrossRefGoogle ScholarPubMed
Dolan, M. C., & Fullam, R. S. (2009). Psychopathy and functional magnetic resonance imaging blood oxygenation level-dependent responses to emotional faces in violent patients with schizophrenia. Biological Psychiatry, 66, 570577.CrossRefGoogle ScholarPubMed
Fairchild, G., Stobbe, Y., van Goozen, S. H., Calder, A. J., & Goodyer, I. M. (2010). Facial expression recognition, fear conditioning, and startle modulation in female subjects with conduct disorder. Biological Psychiatry, 68, 272279.CrossRefGoogle ScholarPubMed
Fanti, K. A., Panayiotou, G., Lazarou, C., Michael, R., & Georgiou, G. (2016). The better of two evils? Evidence that children exhibiting continuous conduct problems high or low on callous–unemotional traits score on opposite directions on physiological and behavioral measures of fear. Development and Psychopathology, 28, 185198.Google Scholar
Finger, E. C., Marsh, A., Blair, K. S., Majestic, C., Evangelou, I., Gupta, K., … Blair, R. J. (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: Neuroimaging, 202, 239244.CrossRefGoogle ScholarPubMed
Frick, P. J., Cornell, A. H., Bodin, D. S., Dane, H. E., Barry, C. T., & Loney, B. R. (2003). Callous-unemotional traits and developmental pathways to severe conduct problems. Developmental Psychology, 39, 246260.CrossRefGoogle ScholarPubMed
Frick, P. J., & Ellis, M. (1999). Callous-unemotional traits and subtypes of conduct disorder. Clinical Child and Family Psychology Review, 2, 149168.Google Scholar
Frick, P. J., & Hare, R. D. (2001). Antisocial Process Screening Device: APSD. Toronto: Multi-Health Systems.Google Scholar
Frick, P. J., Ray, J. V., Thornton, L. C., & Kahn, R. E. (2014). Can callous-unemotional traits enhance the understanding, diagnosis, and treatment of serious conduct problems in children and adolescents? A comprehensive review. Psychological Bulletin, 140, 157.Google Scholar
Gill, A. D., & Stickle, T. R. (2016). Affective differences between psychopathy variants and genders in adjudicated youth. Journal of Abnormal Child Psychology, 44, 295307.Google Scholar
Glenn, A. L., Raine, A., Schug, R. A., Young, L., & Hauser, M. D. (2009). Increased DLPFC activity during moral decision-making in psychopathy. Molecular Psychiatry, 14, 909911.Google Scholar
Goodman, R. (1997). The Strengths and Difficulties Questionnaire: A research note. Journal of Child Psychology and Psychiatry, 38, 581586.Google Scholar
Guay, J. P., Ruscio, J., Knight, R. A., & Hare, R. D. (2007). A taxometric analysis of the latent structure of psychopathy: Evidence for dimensionality. Journal of Abnormal Psychology, 116, 701716.CrossRefGoogle ScholarPubMed
Hawes, D. J., Price, M. J., & Dadds, M. R. (2014). Callous-unemotional traits and the treatment of conduct problems in childhood and adolescence: A comprehensive review. Clinical Child and Family Psychological Review, 17, 248267.Google Scholar
Johnson, P. O., & Neyman, J. (1936). Tests of certain linear hypotheses and their application to some educational problems. Statistical Research Memoirs, 1, 5793.Google Scholar
Jones, A. P., Happé, F. G., Gilbert, F., Burnett, S., & Viding, E. (2010). Feeling, caring, knowing: Different types of empathy deficit in boys with psychopathic tendencies and autism spectrum disorder. Journal of Child Psychology and Psychiatry, 51, 11881197.Google Scholar
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.Google Scholar
Kimonis, E. R., Fanti, K. A., Anastassiou-Hadjicharalambous, X., Mertan, B., Goulter, N., & Katsimicha, E. (2016). Can callous-unemotional traits be reliably measured in preschoolers. Journal of Abnormal Child Psychology, 44, 625638.Google Scholar
Kimonis, E. R., Frick, P. J., Skeem, J. L., Marsee, M. A., Cruise, K., Munoz, L. C., … Morris, A. S. (2008). Assessing callous-unemotional traits in adolescent offenders: Validation of the Inventory of Callous-Unemotional Traits. International Journal of Law and Psychiatry, 31, 241252.CrossRefGoogle ScholarPubMed
Lozier, L. M., Cardinale, E. M., VanMeter, J. W., & Marsh, A. A. (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.Google Scholar
Marsh, A. A. (2013). What can we learn about emotion by studying psychopathy. Frontiers in Human Neuroscience, 7, 181.Google Scholar
Marsh, A. A., & Blair, R. J. (2008). Deficits in facial affect recognition among antisocial populations: A meta-analysis. Neuroscience & Biobehavioral Reviews, 32, 454465.Google Scholar
Marsh, A. A., & Cardinale, E. M. (2012). Psychopathy and fear: Specific impairments in judging behaviors that frighten others. Emotion, 12, 892898.Google Scholar
Marsh, A. A., & Cardinale, E. M. (2014). When psychopathy impairs moral judgments: Neural responses during judgments about causing fear. Social Cognitive and Affective Neuroscience, 9, 311.CrossRefGoogle ScholarPubMed
Marsh, A. A., Finger, E. C., Mitchell, D. G., Reid, M. E., Sims, C., Kosson, D. S., … Blair, R. J. (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.Google Scholar
Marsh, A. A., Finger, E. C., Schechter, J. C., Jurkowitz, I. T., Reid, M. E., & Blair, R. J. (2011). Adolescents with psychopathic traits report reductions in physiological responses to fear. Journal of Child Psychology and Psychiatry, 52, 834841.Google Scholar
McLaren, D. G., Ries, M. L., Xu, G., & Johnson, S. C. (2012). A generalized form of context-dependent psychophysiological interactions (gPPI): A comparison to standard approaches. NeuroImage, 61, 12771286.Google Scholar
Muñoz, L. C., Frick, P. J., Kimonis, E. R., & Aucoin, K. J. (2008). Types of aggression, responsiveness to provocation, and callous-unemotional traits in detained adolescents. Journal of Abnormal Child Psychology, 36, 1528.Google Scholar
Nichols, S. (2001). Mindreading and the cognitive architecture underlying altruistic motivation. Journal of the American Academy of Child & Adolescent Psychiatry, 48, 554562.Google Scholar
Pardini, D., & Fite, P. (2010). Symptoms of conduct disorder, oppositional defiant disorder, attention-deficit/hyperactivity disorder, and callous-unemotional traits as unique predictors of psychosocial maladjustment in boys: Advancing an evidence base for DSM-V. Journal of the American Academy of Child & Adolescent Psychiatry, 49, 11341144.Google ScholarPubMed
Piacentini, J. C., Cohen, P., & Cohen, J. (1992). Combining discrepant diagnostic information from multiple sources: Are complex algorithms better than simple ones. Journal of Abnormal Child Psychology, 20, 5163.Google Scholar
Sebastian, C. L., McCrory, E. J., Cecil, C. A., Lockwood, P. L., De Brito, S. A., Fontaine, N. M., & 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.Google Scholar
Sylvers, P. D., Brennan, P. A., & Lilienfeld, S. O. (2011). Psychopathic traits and preattentive threat processing in children: A novel test of the fearlessness hypothesis. Psychological Science, 22, 12801287.Google Scholar
Syngelaki, E. M., Fairchild, G., Moore, S. C., Savage, J. C., & van Goozen, S. H. (2013). Affective startle potentiation in juvenile offenders: The role of conduct problems and psychopathic traits. Social Neuroscience, 8, 112121.Google Scholar
Viding, E., Sebastian, C. L., Dadds, M. R., Lockwood, P. L., Cecil, C. A., De Brito, S. A., & McCrory, E. J. (2012). Amygdala response to preattentive masked fear in children with conduct problems: The role of callous-unemotional traits. American Journal of Psychiatry, 169, 11091116.CrossRefGoogle ScholarPubMed
Waller, R., Gardner, F., & Hyde, L. W. (2013). What are the associations between parenting, callous–unemotional traits, and antisocial behavior in youth? A systematic review of evidence. Clinical Psychology Review, 33, 593608.CrossRefGoogle ScholarPubMed
Warnick, E. M., Bracken, M. B., & Kasl, S. (2008). Screening efficiency of the Child Behavior Checklist and Strengths and Difficulties Questionnaire: A systematic review. Child and Adolescent Mental Health, 13, 140147.Google Scholar
White, S. F., Marsh, A. A., Fowler, K. A., Schechter, J. C., Adalio, C., Pope, K., … Blair, R. J. (2012). Reduced amygdala response in youths with disruptive behavior disorders and psychopathic traits: Decreased emotional response versus increased top-down attention to nonemotional features. American Journal of Psychiatry, 169, 750758.Google Scholar
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