Advertisement

Disruptive Behavior Problems, Callous-Unemotional Traits, and Regional Gray Matter Volume in the Adolescent Brain and Cognitive Development Study

Published:January 21, 2020DOI:https://doi.org/10.1016/j.bpsc.2020.01.002

      Abstract

      Background

      Neurobiological differences linked to socioemotional and cognitive processing are well documented in youths with disruptive behavior disorders (DBDs), especially youths with callous-unemotional (CU) traits. The current study expanded this literature by examining gray matter volume (GMV) differences among youths with DBD with CU traits (DBDCU+), youths with DBD without CU traits (DBD-only), and youths that were typically developing (TD).

      Methods

      Data were from the first full sample release of the Adolescent Brain and Cognitive Development Study (mean age = 9.49 years; 49% female). We tested whether the GMVs of 11 regions of interest selected a priori differentiated between our 3 groups: DBDCU+ (n = 288), DBD-only (n = 362), and TD (n = 915). Models accounted for demographic confounders, attention-deficit/hyperactivity disorder, and intracranial volume. We examined two potential moderators of the relationship between GMVs and group membership: sex and clinically significant anxiety (i.e., primary vs. secondary CU traits subtype).

      Results

      Youths in the DBDCU+ group had lower right amygdala GMV, and youths in the DBD-only group had lower bilateral amygdala GMV relative to TD youths. Youths in the DBDCU+ group had lower bilateral hippocampal GMV, and youths in the DBD-only group had lower left hippocampal GMV relative to TD youths. Youths in the DBDCU+ group evidenced lower left insula GMV relative to TD youths. Finally, youths in the DBD-only group had lower left superior frontal gyrus and lower right caudal anterior cingulate cortex GMVs relative to TD youths. There was no moderation of associations between GMV and group membership by sex.

      Conclusions

      Our findings implicate structural aberrations in both the amygdala and hippocampus in the etiology of DBDs, with minimal evidence for differences based on the presence or absence of CU traits.

      Keywords

      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'

      References

        • Rivenbark J.G.
        • Odgers C.L.
        • Caspi A.
        • Harrington H.
        • Hogan S.
        • Houts R.M.
        • et al.
        The high societal costs of childhood conduct problems: Evidence from administrative records up to age 38 in a longitudinal birth cohort.
        J Child Psychol Psychiatry. 2018; 59: 703-710
        • Fergusson D.M.
        • John Horwood L.
        • Ridder E.M.
        Show me the child at seven: The consequences of conduct problems in childhood for psychosocial functioning in adulthood.
        J Child Psychol Psychiatry. 2005; 46: 837-849
        • Association A.P.
        Diagnostic and statistical manual of mental disorders (DSM-5®).
        American Psychiatric Publishing, Arlington, VA2013 (2013)
        • Nock M.K.
        • Kazdin A.E.
        • Hiripi E.
        • Kessler R.C.
        Lifetime prevalence, correlates, and persistence of oppositional defiant disorder: results from the National Comorbidity Survey Replication.
        J Child Psychol Psychiatry. 2007; 48: 703-713
        • Berkout O.V.
        • Young J.N.
        • Gross A.M.
        Mean girls and bad boys: Recent research on gender differences in conduct disorder.
        Aggress Violent Behav. 2011; 6: 503-511
        • Demmer D.H.
        • Hooley M.
        • Sheen J.
        • McGillivray J.A.
        • Lum J.A.
        Sex differences in the prevalence of oppositional defiant disorder during middle childhood: A meta-analysis.
        J Abnorm Child Psychol. 2017; 45: 313-325
        • Anderson D.A.
        The cost of crime.
        Foundations and Trends® in Microeconomics. 2012; 7: 209-265
        • Bakker M.
        • Greven C.
        • Buitelaar J.
        • Glennon J.
        Practitioner review: Psychological treatments for children and adolescents with conduct disorder problems—a systematic review and meta-analysis.
        J Child Psychol Psychiatry. 2017; 58: 4-18
        • Hyde L.W.
        • Waller R.
        • Burt S.A.
        Commentary: Improving treatment for youth with callous-unemotional traits through the intersection of basic and applied science—reflections on Dadds et al. (2014).
        J Child Psychol Psychiatry. 2014; 55: 781-783
        • Frick P.J.
        • Ray J.V.
        • Thornton L.C.
        • Kahn R.E.
        Annual research review: A developmental psychopathology approach to understanding callous-unemotional traits in children and adolescents with serious conduct problems.
        J Child Psychol Psychiatry. 2014; 55: 532-548
        • Waller R.
        • Shaw D.S.
        • Neiderhiser J.M.
        • Ganiban J.M.
        • Natsuaki M.N.
        • Reiss D.
        • et al.
        Toward an understanding of the role of the environment in the development of early callous behavior.
        J Pers. 2017; 85: 90-103
        • Waller R.
        • Hyde L.W.
        Callous-unemotional behaviors in early childhood: The development of empathy and prosociality gone awry.
        Curr Opin Psychol. 2018; 20: 11-16
        • Blair R.J.R.
        The amygdala and ventromedial prefrontal cortex in morality and psychopathy.
        Trends Cogn Sci. 2007; 11: 387-392
        • Blair R.J.R.
        Neurocognitive models of aggression, the antisocial personality disorders, and psychopathy.
        J Neurol Neurosurg Psychiatry. 2001; 71: 727-731
        • Blair R.
        Responsiveness to distress cues in the child with psychopathic tendencies.
        Pers Individ Diff. 1999; 27: 135-145
        • Blair R.J.R.
        A cognitive developmental approach to morality: Investigating the psychopath.
        Cognition. 1995; 57: 1-29
        • LeDoux J.E.
        Coming to terms with fear.
        Proc Natl Acad Sci. 2014; 111: 2871-2878
        • Michalska K.J.
        • Zeffiro T.A.
        • Decety J.
        Brain response to viewing others being harmed in children with conduct disorder symptoms.
        J Child Psychol Psychiatry. 2016; 57: 510-519
        • Ochsner K.N.
        • Gross J.J.
        The cognitive control of emotion.
        Trends Cogn Sci. 2005; 9: 242-249
        • Lozier L.M.
        • Cardinale E.M.
        • VanMeter J.W.
        • Marsh A.A.
        Mediation of the relationship between callous-unemotional traits and proactive aggression by amygdala response to fear among children with conduct problems.
        JAMA Psychiatry. 2014; 71: 627-636
        • Aghajani M.
        • Klapwijk E.T.
        • van der Wee N.J.
        • Veer I.M.
        • Rombouts S.A.
        • Boon A.E.
        • et al.
        Disorganized amygdala networks in conduct-disordered juvenile offenders with callous-unemotional traits.
        Biol Psychiatry. 2017; 82: 283-293
        • Lockwood P.L.
        • Sebastian C.L.
        • McCrory E.J.
        • Hyde Z.H.
        • Gu X.
        • De Brito S.A.
        • et al.
        Association of callous traits with reduced neural response to others’ pain in children with conduct problems.
        Curr Biol. 2013; 23: 901-905
        • Sebastian C.L.
        • McCrory E.J.
        • Cecil C.A.
        • Lockwood P.L.
        • De Brito S.A.
        • Fontaine N.M.
        • et al.
        Neural responses to affective and cognitive theory of mind in children with conduct problems and varying levels of callous-unemotional traits.
        Arch Gen Psychiatry. 2012; 69: 814-822
        • Marsh A.A.
        • Finger E.C.
        • Fowler K.A.
        • Adalio C.J.
        • Jurkowitz I.T.
        • Schechter J.C.
        • et al.
        Empathic responsiveness in amygdala and anterior cingulate cortex in youths with psychopathic traits.
        J Child Psychol Psychiatry. 2013; 54: 900-910
        • Schwenck C.
        • Ciaramidaro A.
        • Selivanova M.
        • Tournay J.
        • Freitag C.M.
        • Siniatchkin M.
        Neural correlates of affective empathy and reinforcement learning in boys with conduct problems: fMRI evidence from a gambling task.
        Behav Brain Res. 2017; 320: 75-84
        • Veroude K.
        • von Rhein D.
        • Chauvin R.J.
        • van Dongen E.V.
        • Mennes M.J.
        • Franke B.
        • et al.
        The link between callous-unemotional traits and neural mechanisms of reward processing: An fMRI study.
        Psychiatry Res Neuroimaging. 2016; 255: 75-80
        • Blair R.
        • Veroude K.
        • Buitelaar J.
        Neuro-cognitive system dysfunction and symptom sets: A review of fMRI studies in youth with conduct problems.
        Neurosci Biobehav Rev. 2016; 91: 69-90
        • Hyde L.W.
        • Shaw D.S.
        • Hariri A.R.
        Understanding youth antisocial behavior using neuroscience through a developmental psychopathology lens: Review, integration, and directions for research.
        Dev Rev. 2013; 33: 168-223
        • Rogers J.C.
        • De Brito S.A.
        Cortical and subcortical gray matter volume in youths with conduct problems: A meta-analysis.
        JAMA Psychiatry. 2016; 73: 64-72
        • Cohn M.D.
        • Viding E.
        • McCrory E.
        • Pape L.
        • van den Brink W.
        • Doreleijers T.A.
        • et al.
        Regional gray matter volume and concentration in at-risk adolescents: Untangling associations with callous-unemotional traits and conduct disorder symptoms.
        Psychiatry Res Neuroimaging. 2016; 254: 180-187
        • Cardinale E.M.
        • O’Connell K.
        • Robertson E.L.
        • Meena L.B.
        • Breeden A.L.
        • Lozier L.M.
        • et al.
        Callous and uncaring traits are associated with reductions in amygdala volume among youths with varying levels of conduct problems.
        Psychol Med. 2019; 49: 1449-1458
        • Foulkes L.
        • Blakemore S.J.
        Studying individual differences in human adolescent brain development.
        Nat Neurosci 2018. 2018; 21: 315-323
        • Giedd J.N.
        • Blumenthal J.
        • Jeffries N.O.
        • Castellanos F.X.
        • Liu H.
        • Zijdenbos A.
        • et al.
        Brain development during childhood and adolescence: A longitudinal MRI study.
        Nat Neurosc. 1999; 2: 861
        • Falk E.
        • Hyde L.
        • Mitchell C.
        • Faul J.
        • Gonzalez R.
        • Heitzeg M.
        • et al.
        What is a representative brain? Neuroscience meets population science.
        Proc Natl Acad Sci. 2013; 110: 17615-17622
        • Hyde L.W.
        • Shaw D.S.
        • Murray L.
        • Gard A.
        • Hariri A.R.
        • Forbes E.E.
        Dissecting the role of amygdala reactivity in antisocial behavior in a sample of young, low-income, urban men.
        Clin Psychol Sci. 2016; 4: 527-544
        • Dotterer H.L.
        • Hyde L.W.
        • Swartz J.R.
        • Hariri A.R.
        • Williamson D.E.
        Amygdala reactivity predicts adolescent antisocial behavior but not callous-unemotional traits.
        Dev Cogn Neurosci. 2017; 24: 84-92
        • Noble K.G.
        • Houston S.M.
        • Brito N.H.
        • Bartsch H.
        • Kan E.
        • Kuperman J.M.
        • et al.
        Family income, parental education and brain structure in children and adolescents.
        Nat Neurosci. 2015; 18: 773-778
        • Gianaros P.J.
        • Manuck S.B.
        • Sheu L.K.
        • Kuan D.C.
        • Votruba-Drzal E.
        • et al.
        Parental education predicts corticostriatal functionality in adulthood.
        Cereb Cortex. 2010; 21: 896-910
        • Barker E.D.
        • Tremblay R.E.
        • van Lier P.A.
        • Vitaro F.
        • Nagin D.S.
        • Assaad J.M.
        • et al.
        The neurocognition of conduct disorder behaviors: Specificity to physical aggression and theft after controlling for ADHD symptoms.
        Aggress Behav. 2011; 37: 63-72
        • Raschle N.M.
        • Menks W.M.
        • Fehlbaum L.V.
        • Steppan M.
        • Smaragdi A.
        • Gonzalez-Madruga K.
        • et al.
        Callous-unemotional traits and brain structure: Sex-specific effects in anterior insula of typically-developing youths.
        Neuroimage Clin. 2018; 17: 856-864
        • Smaragdi A.
        • Cornwell H.
        • Toschi N.
        • Riccelli R.
        • Gonzalez-Madruga K.
        • Wells A.
        • et al.
        Sex differences in the relationship between conduct disorder and cortical structure in adolescents.
        J Am Acad Child Adolesc Psychiatry. 2017; 56: 703-712
        • Sibley M.H.
        • Pelham W.E.
        • Molina B.S.
        • Gnagy E.M.
        • Waschbusch D.A.
        • Biswas A.
        • et al.
        The delinquency outcomes of boys with ADHD with and without comorbidity.
        J Abnorm Child Psychol. 2011; 39: 21-32
        • Stevens M.C.
        • Haney-Caron E.
        Comparison of brain volume abnormalities between ADHD and conduct disorder in adolescence.
        J Psychiatry Neurosci. 2012; 37: 389
        • Kahn R.E.
        • Frick P.J.
        • Youngstrom E.A.
        • Kogos Youngstrom J.
        • Feeny N.C.
        • Findling R.L.
        Distinguishing primary and secondary variants of callous-unemotional traits among adolescents in a clinic-referred sample.
        Psychol Assess. 2013; 25: 966-978
        • Kimonis E.R.
        • Frick P.J.
        • Cauffman E.
        • Goldweber A.
        • Skeem J.
        Primary and secondary variants of juvenile psychopathy differ in emotional processing.
        Dev Psychopathol. 2012; 24: 1091-1103
        • Lee Z.
        • Salekin R.T.
        • Iselin A.-M.R.
        Psychopathic traits in youth: Is there evidence for primary and secondary subtypes?.
        J Abnorm Child Psychol. 2010; 38: 381-393
        • Waller R.
        • Hicks B.M.
        Trajectories of alcohol and marijuana use among primary versus secondary psychopathy variants within an adjudicated adolescents male sample.
        Personal Disord. 2019; 10: 87-96
        • Garavan H.
        • Bartsch H.
        • Conway K.
        • Decastro A.
        • Goldstein R.
        • Heeringa S.
        • et al.
        Recruiting the ABCD sample: Design considerations and procedures.
        Dev Cogn Neurosci. 2018; : 16-22
        • Volkow N.D.
        • Koob G.F.
        • Croyle R.T.
        • Bianchi D.W.
        • Gordon J.A.
        • Koroshetz W.J.
        • et al.
        The conception of the ABCD study: From substance use to a broad NIH collaboration.
        Dev Cogn Neurosci. 2018; 32: 4-7
        • Achenbach T.
        • Ruffle T.
        The Child Behavior Checklist and related forms for assessing behavioral/emotional problems and competencies.
        Pediatr Rev. 2000; 21: 265-271
        • Kaufman J.
        • Birmaher B.
        • Brent D.A.
        • Rao U.
        • Ryan N.D.
        KIDDIE-SADS—present and lifetime version (K-SADS-PL).
        Instrument developed at Western Psychiatric Institute and Clinic, Pittsburgh, PA1996
        • Kaufman J.
        • Birmaher B.
        • Brent D.
        • Rao U.
        • Flynn C.
        • Moreci P.
        • et al.
        Schedule for affective disorders and schizophrenia for school-age children—present and lifetime version (K-SADS-PL): Initial reliability and validity data.
        J Am Acad Child Adolesc Psychiatry. 1997; 36: 980-988
        • Kobak K.
        • Kratochvil C.
        • Stanger C.
        • Kaufman J.
        Computerized screening of comorbidity in adolescents with substance or psychiatric disorders. Poster presented at the 33rd Annual Anxiety Disorders and Depression Conference, La Jolla, CA.
        (Available at:)
        • Barch D.M.
        • Albaugh M.D.
        • Avenevoli S.
        • Chang L.
        • Clark D.B.
        • Glantz M.D.
        • et al.
        Demographic, physical and mental health assessments in the adolescent brain and cognitive development study: Rationale and description.
        Dev Cogn Neurosci. 2018; 32: 55-66
        • Hawes S.W.
        • Waller R.
        • Thompson W.K.
        • Hyde L.W.
        • Byrd A.L.
        • Burt A.S.
        • et al.
        Assessing callous-unemotional traits: Development of a brief, reliable measure in a large and diverse sample of preadolescent youth.
        Psychol Med. 2020; 50: 456-464
        • Goodman R.
        The Strengths and Difficulties Questionnaire: A research note.
        J Child Psychol Psychiatry. 1997; 38: 581-586
        • Hagler D.J.
        • Hatton S.N.
        • Makowski C.
        • Cornejo M.D.
        • Fair D.A.
        • Dick A.S.
        • et al.
        Image processing and analysis methods for the Adolescent Brain Cognitive Development Study.
        bioRxiv. 2018; (2018:457739)
        • Fischl B.
        FreeSurfer. Neuroimage. 2012; 62: 774-781
        • Chen C.
        • Gutierrez E.
        • Thompson W.
        • Panizzon M.S.
        • Jernigan T.L.
        • Eyler L.T.
        • et al.
        Hierarchical genetic organization of human cortical surface area.
        Science. 2012; 335: 1634-1636
        • Muthén L.K.
        • Muthén B.O.
        Mplus user’s guide.
        7th ed. Muthén & Muthén, Los Angeles, CA1998–2012
        • Sebastian C.L.
        • De Brito S.A.
        • McCrory E.J.
        • Hyde Z.H.
        • Lockwood P.L.
        • Cecil C.A.M.
        • et al.
        Gray matter volumes in children with conduct problems and varying levels of callous-unemotional traits.
        J Abnorm Child Psychol. 2016; 44: 639-649
        • Ermer E.
        • Cope L.M.
        • Nyalakanti P.K.
        • Calhoun V.D.
        • Kiehl K.A.
        Aberrant paralimbic gray matter in criminal psychopathy.
        J Abnorm Psychol. 2012; 121: 649
        • Cope L.M.
        • Shane M.S.
        • Segall J.M.
        • Nyalakanti P.K.
        • Stevens M.C.
        • Pearlson G.D.
        • et al.
        Examining the effect of psychopathic traits on gray matter volume in a community substance abuse sample.
        Psychiatry Res Neuroimaging. 2012; 204: 91-100
        • Steele V.R.
        • Rao V.
        • Calhoun V.D.
        • Kiehl K.A.
        Machine learning of structural magnetic resonance imaging predicts psychopathic traits in adolescent offenders.
        Neuroimage. 2017; 145: 265-273
        • Tyborowska A.
        • Volman I.
        • Niermann H.C.
        • Pouwels J.L.
        • Smeekens S.
        • Cillessen A.H.
        • et al.
        Early-life and pubertal stress differentially modulate gray matter development in human adolescents.
        Sci Rep. 2018; 8: 9201
        • Winkler A.M.
        • Kochunov P.
        • Blangero J.
        • Almasy L.
        • Zilles K.
        • Fox P.T.
        • et al.
        Cortical thickness or gray matter volume? The importance of selecting the phenotype for imaging genetics studies.
        Neuroimage. 2010; 53: 1135-1146
        • Benjamini Y.
        • Krieger A.M.
        • Yekutieli D.
        Adaptive linear step-up procedures that control the false discovery rate.
        Biometrika. 2006; 93: 491-507