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Callous and uncaring traits are associated with reductions in amygdala volume among youths with varying levels of conduct problems

Published online by Cambridge University Press:  24 August 2018

Elise M. Cardinale ,
Katherine O'Connell ,
Emily L. Robertson ,
Lydia B. Meena ,
Andrew L. Breeden ,
Leah M. Lozier ,
John W. VanMeter  and
Abigail A. Marsh
Elise M. Cardinale*
Affiliation:
Georgetown University Department of Psychology, Washington, DC, USA
Katherine O'Connell
Affiliation:
Georgetown University Interdisciplinary Program in Neuroscience, Washington, DC, USA
Emily L. Robertson
Affiliation:
Georgetown University Department of Psychology, Washington, DC, USA Louisiana State University Department of Psychology, Baton Rouge, LA, USA
Lydia B. Meena
Affiliation:
Georgetown University Department of Psychology, Washington, DC, USA
Andrew L. Breeden
Affiliation:
Georgetown University Interdisciplinary Program in Neuroscience, Washington, DC, USA
Leah M. Lozier
Affiliation:
Georgetown University Interdisciplinary Program in Neuroscience, Washington, DC, USA
John W. VanMeter
Affiliation:
Georgetown University Center for Functional and Molecular Imaging, Washington, DC, USA
Abigail A. Marsh
Affiliation:
Georgetown University Department of Psychology, Washington, DC, USA Georgetown University Interdisciplinary Program in Neuroscience, Washington, DC, USA
*
Author for correspondence: Elise M Cardinale, E-mail: emc62@georgetown.edu
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Abstract

Background

The emergence of callous unemotional (CU) traits, and associated externalizing behaviors, is believed to reflect underlying dysfunction in the amygdala. Studies of adults with CU traits or psychopathy have linked characteristic patterns of amygdala dysfunction to reduced amygdala volume, but studies in youths have not thus far found evidence of similar amygdala volume reductions. The current study examined the association between CU traits and amygdala volume by modeling CU traits and externalizing behavior as independent continuous variables, and explored the relative contributions of callous, uncaring, and unemotional traits.

Methods

CU traits and externalizing behavior problems were assessed in 148 youths using the Inventory of Callous Unemotional Traits (ICU) and the Child Behavior Checklist (CBCL). For a subset of participants (n = 93), high-resolution T1-weighted images were collected and volume estimates for the amygdala were extracted.

Results

Analyses revealed that CU traits were associated with increased externalizing behaviors and decreased bilateral amygdala volume. These results were driven by the callous and uncaring sub-factors of CU traits, with unemotional traits unrelated to either externalizing behaviors or amygdala volume. Results persisted after accounting for covariation between CU traits and externalizing behaviors. Bootstrap mediation analyses indicated that CU traits mediated the relationship between reduced amygdala volume and externalizing severity.

Conclusions

These findings provide evidence that callous-uncaring traits account for reduced amygdala volume among youths with conduct problems. These findings provide a framework for further investigation of abnormal amygdala development as a key causal pathway for the development of callous-uncaring traits and conduct problems.

Keywords

Amygdalacallous unemotional traitsexternalizing behaviors
Type
Original Articles
Information
Psychological Medicine , Volume 49 , Issue 9 , July 2019 , pp. 1449 - 1458
Copyright
Copyright © Cambridge University Press 2018 

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References

Achenbach, TM (1991) Manual for the Child Behavior Checklist: 4-18. Burlington: University of Vermont.Google Scholar
Aghajani, M, Klapwijk, ET, van der Wee, NJ, Veer, IM, Rombouts, SA, Boon, AE, van Beelen, P, Popma, A, Vermeiren, R, and Colins, OF (2016) Disorganized amygdala networks in conduct-disordered juvenile offenders With callous-unemotional traits. Biological Psychiatry 82, 283–293.Google Scholar
Biederman, J, Faraone, SV, Doyle, A, Lehman, BK, Kraus, I, Perrin, J and Tsuang, MT (1993) Convergence of the Child Behavior Checklist with structured interview-based psychiatric diagnoses of ADHD children with and without comorbidity. Journal of Child Psychology and Psychiatry 34, 1241–1251.Google Scholar
Blair, RJ (2013) The neurobiology of psychopathic traits in youths. Nature Reviews Neuroscience 14, 786–799.Google Scholar
Blair, RJ, Peschardt, KS, Budhani, S, Mitchell, DGV and Pine, DS (2006) The development of psychopathy. Journal of Child Psychology and Psychiatry 47, 262–276.Google Scholar
Blair, RJR (2005) Applying a cognitive neuroscience perspective to the disorder of psychopathy. Development and Psychopathology 17, 865–891.Google Scholar
Breeden, AL, Cardinale, EM, Lozier, LM, VanMeter, JW and Marsh, AA (2015) Callous-unemotional traits drive reduced white-matter integrity in youths with conduct problems. Psychological Medicine 45, 3033–3046.Google Scholar
Burke, JD, Loeber, R and Lahey, BB (2007) Adolescent conduct disorder and interpersonal callousness as predictors of psychopathy in young adults. Journal of Clinical Child and Adolescent Psychology 35, 334–346.Google Scholar
Byrd, AL, Kahn, RE and Pardini, DA (2013) A validation of the Inventory of Callous-Unemotional Traits in a community sample of young adult males. Journal of Psychopathology Behavioral Assessment 35, 20–34.Google Scholar
Cardinale, EM, Breeden, AL, Robertson, EL, Lozier, LM, VanMeter, JW and Marsh, AA (2018) Externalizing behavior severity in youths with callous–unemotional traits corresponds to patterns of amygdala activity and connectivity during judgments of causing fear. Development and Psychopathology 30, 191–201.Google Scholar
Cardinale, EM and Marsh, AA (2017) The Reliability and Validity of the Inventory of Callous Unemotional Traits. A Meta-Analytic Review. Assessment, 1073191117747392.Google Scholar
Ciucci, E, Baroncelli, A, Franchi, M, Golmaryami, FN and Frick, PJ (2014) The association between callous-unemotional traits and behavioral and academic adjustment in children: further validation of the Inventory of Callous-Unemotional Traits. Journal of Psychopathology and Behavioral Assessment 36, 189–200.Google Scholar
Cohn, MD, Viding, E, McCrory, E, Pape, L, van den Brink, W, Doreleijers, TAH, Veltman, DJ and Popma, A (2016) Regional grey matter volume and concentration in at-risk adolescents: untangling associations with callous-unemotional traits and conduct disorder symptoms. Psychiatry Research 254, 180–187.Google Scholar
Cope, LM, Ermer, E, Nyalakanti, PK, Calhoun, VD and Kiehl, KA (2014) Paralimbic gray matter reductions in incarcerated adolescent females with psychopathic traits. Journal of Abnormal Child Psychology 42, 659–668.Google Scholar
Dawel, A, O'Kearney, R, McKone, E and 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, 2288–2304.Google Scholar
De Brito, SA, Mechelli, A, Wilke, M, Laurens, KR, Jones, AP, Barker, GJ, Hodgins, S and Viding, E (2009) Size matters: increased grey matter in boys with conduct problems and callous-unemotional traits. Brain 132, 843–852.Google Scholar
Essau, CA, Sasagawa, S and Frick, PJ (2006) Callous-unemotional traits in a community sample of adolescents. Assessment 13, 454–469.Google Scholar
Fairchild, G, Hagan, CC, Walsh, ND, Passamonti, L, Calder, AJ and Goodyer, IM (2013) Brain structure abnormalities in adolescent girls with conduct disorder. Journal of Child Psychology and Psychiatry 54, 86–95.Google Scholar
Fischl, B (2012) Freesurfer. Neuroimage 62, 774–781.Google Scholar
Fischl, B, Salat, DH, Busa, E, Albert, M, Dieterich, M, Haselgrove, C, van der Kouwe, A, Killiany, R, Kennedy, D, Klaveness, S, Montillo, A, Makris, N, Rosen, B and Dale, AM (2002) Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 33, 341–355.Google Scholar
Fischl, B, Salat, DH, van der Kouwe, AJ, Makris, N, Segonne, F, Quinn, BT and Dale, AM (2004) Sequence-independent segmentation of magnetic resonance images. Neuroimage 23, S69–S84.Google Scholar
Finger, EC, Marsh, AM, Blair, KS, Majestic, C, Evangelou, I, Gupta, K, Schneider, MR, Sims, C, Pope, K, Fowler, K, Sinclair, S, Tovar-Moll, F, Pine, D and 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, 239–244.Google Scholar
Frick, PJ, Cornell, AH, Bodin, SD, Dane, HE, Barry, CT and Loney, BR (2003) Callous-unemotional traits and developmental pathways to severe conduct problems. Developmental Psychology 39, 246–260.Google Scholar
Frick, PJ and Hare, RD (2001) Antisocial Process Screening Device: APSD. Toronto: Multi-Health Systems.Google Scholar
Frick, PJ and Morris, AS (2004) Temperament and developmental pathways to conduct problems. Journal of Clinical Child and Adolescent Psychology 33, 54–68.Google Scholar
Frick, PJ and Ray, JV (2015) Evaluating callous-unemotional traits as a personality construct. Journal of personality 83, 710–722.Google Scholar
Frick, PJ, Stickle, TR, Dandreaux, DM, Farrell, JM and Kimonis, ER (2005) Callous–unemotional traits in predicting the severity and stability of conduct problems and delinquency. Journal of Abnormal Child Psychology 33, 471–487.Google Scholar
Giedd, JN, Blumenthal, J, Jeffries, NO, Castellanos, FX, Liu, H, Zijdenbos, A, Paus, T, Evans, AC and Rapoport, JL (1999) Brain development during childhood and adolescence: a longitudinal MRI study. Nature Neuroscience 2, 861–863.Google Scholar
Gluckman, NS, Hawes, DJ and Russell, AM (2016) Are callous-unemotional traits associated with conflict adaptation in childhood. Child Psychiatry & Human Development 47, 583–592.Google Scholar
Grimm, O, Pohlack, S, Cacciaglia, R, Winkelmann, T, Plichta, MM, Demirakca, T and Flor, H (2015) Amygdalar and hippocampal volume: a comparison between manual segmentation, FreeSurfer and VBM. Journal of Neuroscience Methods 253, 254–261.Google Scholar
Guay, JP, Ruscio, J, Knight, RA and Hare, RD (2007) A taxometric analysis of the latent structure of psychopathy: evidence for dimensionality. Journal of Abnormal Psychology 116, 701–716.Google Scholar
Hawes, SW, Byrd, AL, Henderson, CE, Gazda, RL, Burke, JD, Loeber, R and Pardini, DA (2014) Refining the parent-reported Inventory of Callous-Unemotional Traits in boys with conduct problems. Psychological Assessment 26, 256–266.Google Scholar
Heinen, R, Bouvy, WH, Mendrik, AM, Viergever, MA, Biessels, GJ and de Bresser, J (2016) Robustness of automated methods for brain volume measurements across different MRI field strengths. PLoS ONE 11, e0165719.Google Scholar
Henry, J, Pingault, JB, Boivin, M, Rijsdijk, F and Viding, E (2016) Genetic and environmental aetiology of the dimensions of callous-unemotional traits. Psychological Medicine 46, 405–414.Google Scholar
Herpers, PC, Scheepers, FE, Bons, DMA, Buitelaar, JK and Rommelse, NNJ (2014) The cognitive and neural correlates of psychopathy and especially callous-unemotional traits in youths: a systematic review of the evidence. Development and Psychopathology 26, 245–273.Google Scholar
Huebner, T, Vloet, TD, Marx, I, Konrad, K, Fink, GR, Herpertz, SC and Herpertz-Dahlmann, B (2008) Morphometric brain abnormalities in boys with conduct disorder. Journal of the American Academy of Child Adolescent Psychiatry 47, 540–547.Google Scholar
Jones, AP, Happe, FG, Gilbert, F, Burnett, S and 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, 1188–1197.Google Scholar
Jones, AP, Laurens, KR, Herba, CM, Barker, GJ and Viding, E (2009) Amygdala hypoactivity to fearful faces in boys with conduct problems and callous-unemotional traits. American Journal of Psychiatry 166, 95–102.Google Scholar
Kahn, RE, Byrd, AL and Pardini, DA (2013) Callous-unemotional traits robustly predict future criminal offending in young men. Law and Human Behavior 37, 87–97.Google Scholar
Katuwal, GJ, Baum, SA, Cahill, ND, Dougherty, CC, Evans, E, Evans, DW, Moore, GJ and Michael, AM (2016) Inter-method discrepancies in brain volume estimation may drive inconsistent findings in autism. Frontiers in Neuroscience 10, 1–16.Google Scholar
Kaufman, AS and Kaufman, NL (2004) Kaufman brief intelligence test (2nd ed.). In Encyclopedia of Special Education. Hoboken, NJ: John Wiley & Sons, Inc.Google Scholar
Kimonis, ER, Branch, J, Hagman, B, Graham, N and Miller, C (2013) The psychometric properties of the Inventory of Callous-Unemotional Traits in an undergraduate sample. Psychological Assessment 25, 84–93.Google Scholar
Kimonis, ER, Frick, PJ, Munoz, LC and Aucoin, KJ (2008 a) Callous-unemotional traits and the emotional processing of distress cues in detained boys: testing the moderating role of aggression, exposure to community violence, and histories of abuse. Development and Psychopathology 20, 569–589.Google Scholar
Kimonis, ER, Frick, PJ, Skeem, JL, Marsee, MA, Cruise, K, Munoz, LC, Aucoin, KJ and Morris, AS (2008 b) Assessing callous-unemotional traits in adolescent offenders: validation of the Inventory of Callous-Unemotional Traits. International Journal of Law and Psychiatry 31, 241–252.Google Scholar
Kochanska, G (1993) Toward a synthesis of parental socialization and child temperament in early development of conscience. Child Development 64, 325–347.Google Scholar
Lenroot, RK, Gogtay, N, Greenstein, DK, Wells, EM, Wallace, GL, Clasen, LS, Blumenthal, JD, Lerch, J, Zijdenbos, AP, Evans, AC and Thompson, PM (2007) Sexual dimorphism of brain developmental trajectories during childhood and adolescence. NeuroImage 36, 1065–1073.Google Scholar
Lozier, LM, Cardinale, EM, VanMeter, JW and 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, 627–636.Google Scholar
Marsh, AA (2016) Understanding amygdala responsiveness to fearful expressions through the lens of psychopathy and altruism. Journal of Neuroscience Research 94, 513–525.Google Scholar
Marsh, AA and Blair, RJ (2008) Deficits in facial affect recognition among antisocial populations: a meta-analysis. Neuroscience & Biobehavioral Review 32, 454–465.Google Scholar
Marsh, AA, Finger, EC, Fowler, KA, Jurkowitz, IT, Schechter, JC, Yu, HH, Pine, DS and Blair, RJ (2011 a) Reduced amygdala-orbitofrontal connectivity during moral judgments in youths with disruptive behavior disorders and psychopathic traits. Psychiatry Research 194, 279–286.Google Scholar
Marsh, AA, Finger, EC, Mitchell, DGV, Reid, ME, Sims, C, Kosson, DS, Towbin, KE, Leibenluft, E, Pine, DS and 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, 712–720.Google Scholar
Marsh, AA, Finger, EC, Shechter, JC, Jurkowitz, IT, Reid, ME and Blair, RJ (2011 b) Adolescents with psychopathic traits report reductions in physiological responses to fear. Journal of Child Psychology and Psychiatry 52, 834–841.Google Scholar
Mechelli, A, Price, CJ, Friston, KJ and Ashburner, J (2005) Voxel-based morphometry of the human brain: methods and applications. Current Medical Imaging Reviews 1, 105–113.Google Scholar
Moffitt, TE, Arseneault, L, Jaffee, SR, Kim-Cohen, J, Koenen, KC, Odgers, CL, Slutske, WS and Viding, E (2008) Research review: DSM-V conduct disorder: research needs for an evidence base. Journal of Child Psychology and Psychiatry 49, 3–33.Google Scholar
Morey, RA, Petty, CM, Xu, Y, Hayes, JP, Wagner, HR II, Lewis, DV, LaBar, KS, Styner, M and McCarthy, G (2009) A comparison of automated segmentation and manual tracing for quantifying hippocampal and amygdala volumes. Neuroimage 45, 855–866.Google Scholar
Morey, RA, Selgrade, ES, Wagner, HR, Huettel, SA, Wang, L and McCarthy, G (2010) Scan–rescan reliability of subcortical brain volumes derived from automated segmentation. Human Brain Mapping 31, 1751–1762.Google Scholar
Muñoz, LC, Frick, PJ, Kimonis, ER and Aucoin, KJ (2008) Types of aggression, responsiveness to provocation, and callous-unemotional traits in detained adolescents. Journal of Abnormal Child Psychology 36, 15–28.Google Scholar
Pardini, DA, Raine, A, Erickson, K and Loeber, R (2014) Lower amygdala volume in men is associated with childhood aggression, early psychopathic traits, and future violence. Biological Psychiatry 75, 73–80.Google Scholar
Piacentini, JC, Cohen, P and Cohen, J (1992) Combining discrepant diagnostic information from multiple sources: are complex algorithms better than simple ones. Journal of Abnormal Child Psychology 20, 51–63.Google Scholar
Popescu, V, Schoonheim, MM, Versteeg, A, Chaturvedi, N, Jonker, M, Xavier de Menezes, R, Garre, FG, Uitdehaag, BM, Barkhof, F and Vrenken, H (2016) Grey matter atrophy in multiple sclerosis: clinical interpretation depends on choice of analysis method. PLoS ONE 11, e0143942.Google Scholar
Rogers, JC and De Brito, SA (2016) Cortical and subcortical gray matter volume in youths with conduct problems: a meta-analysis. JAMA Psychiatry 73, 64–72.Google Scholar
Roose, A, Bijttebier, P, Decoene, S, Claes, L and Frick, PJ (2010) Assessing the affective features of psychopathy in adolescence: a further validation of the inventory of callous and unemotional traits. Assessment 17, 44–57.Google Scholar
Rowe, R, Maughan, B, Moran, P, Ford, T, Briskman, J and Goodman, R (2010) The role of callous and unemotional traits in the diagnosis of conduct disorder. Journal of Child Psychology and Psychiatry 51, 688–695.Google Scholar
Salekin, RT (2006) Factor structure of psychopathy in youth: testing the applicability of the new four-factor model. Criminal Justice and Behavior 33, 135–157.Google Scholar
Schoemaker, D, Buss, C, Head, K, Sandman, CA, Davis, EP, Chakravarty, MM, Gauthier, S and Pruessner, JC (2016) Hippocampus and amygdala volumes from magnetic resonance images in children: assessing accuracy of FreeSurfer and FSL against manual segmentation. NeuroImage 129, 1–14.Google Scholar
Seara-Cardoso, A, Sebastian, CL, Viding, E and Roiser, JP (2016) Affective resonance in response to others’ emotional faces varies with affective ratings and psychopathic traits in amygdala and anterior insula. Social Neuroscience 11, 140–152.Google Scholar
Sebastian, CL, De Brito, SA, McCrory, EJ, Hyde, ZH, Lockwood, PL, Cecil, CA and Viding, E (2016) Grey matter volumes in children with conduct problems and varying levels of callous-unemotional traits. Journal of Abnormal Child Psychology 44, 639–649.Google Scholar
Sebastian, CL, McCrory, EJP, Cecil, CAM, Lockwood, PL, De Brito, SA, Fontaine, NMG and 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, 814–822.Google Scholar
Sterzer, P, Stadler, C, Poustka, F and Kleinschmidt, A (2007) A structural neural deficit in adolescents with conduct disorder and its association with lack of empathy. Neuroimage 37, 335–342.Google Scholar
Vasey, MW, Kotov, R, Frick, PJ and Loney, BR (2005) The latent structure of psychopathy in youth: a taxometric investigation. Journal of Abnormal Child Psychology 33, 411–429.Google Scholar
Viding, E, Sebastian, CL, Dadds, MR, Lockwood, PL, Cecil, CAM, De Brito, SA and McCrory, EJ (2012) Amygdala response to preattentive masked fear in children with conduct problems: the role of callous-unemotional traits. American Journal of Psychiatry 169, 1109–1116.Google Scholar
Vieira, JB, Ferreira-Santos, F, Almeida, PR, Barbosa, F, Marques-Teixeira, J and Marsh, AA (2015) Psychopathic traits are associated with cortical and subcortical volume alterations in healthy individuals. Social Cognitive and Affective Neuroscience 10, 1693–1704.Google Scholar
Wallace, GL, White, SF, Robustelli, B, Sinclair, S, Hwang, S, Martin, A and Blair, RJ (2014) Cortical and subcortical abnormalities in youths with conduct disorder and elevated callous-unemotional traits. Journal of the American Academy of Child and Adolescent Psychiatry 53, 456–465.Google Scholar
Waller, R, Wright, AG, Shaw, DS, Gardner, F, Dishion, TJ, Wilson, MN and Hyde, LW (2015) Factor structure and construct validity of the parent-reported inventory of callous-unemotional traits among high-risk 9-year-olds. Assessment 22, 561–580.Google Scholar
Warnick, EM, Bracken, MB and Kasl, S (2008) Screening efficiency of the Child Behavior Checklist and strengths and difficulties questionnaire: a systematic review. Child and Adolescent Mental Health 13, 140–147.Google Scholar
White, SF, Cruise, KR and Frick, PJ (2009) Differential correlates to self-report and parent-report of callous-unemotional traits in a sample of juvenile sexual offenders. Behavioral Sciences and the Law 27, 910–928.Google Scholar
White, SF, Marsh, AA, Fowler, KA, Schechter, JC, Adalio, CJ, Pope, K, Sinclair, S, Pine, DS and Blair, RJR (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, 750–758.Google Scholar
Yang, Y, Raine, A, Narr, KL, Colletti, P and Toga, AW (2009) Localization of deformations within the amygdala in individuals with psychopathy. Archives of General Psychiatry 66, 986–994.Google Scholar
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