Hostname: page-component-745bb68f8f-kw2vx Total loading time: 0 Render date: 2025-02-11T16:41:06.122Z Has data issue: false hasContentIssue false
  • English
  • Français

Dual neurocircuitry dysfunctions in disruptive behavior disorders: emotional responding and response inhibition

Published online by Cambridge University Press:  15 February 2016

S. Hwang ,
Z. T. Nolan ,
S. F. White ,
W. C. Williams ,
S. Sinclair  and
R. J. R. Blair
S. Hwang*
Affiliation:
University of Nebraska Medical Center, Omaha, NE, USA
Z. T. Nolan
Affiliation:
Penn State College of Medicine, MD/PhD Program, Hershey, PA, USA
S. F. White
Affiliation:
Boystown National Research Hospital, Boystown, NE, USA
W. C. Williams
Affiliation:
Department of Psychology, Stanford University, Stanford, CA, USA
S. Sinclair
Affiliation:
Department of Health and Human Services, Section on Affective Cognitive Neuroscience, National Institute of Mental Health, National Institutes of Health, Bethesda, MD, USA
R. J. R. Blair
Affiliation:
Department of Health and Human Services, Section on Affective Cognitive Neuroscience, National Institute of Mental Health, National Institutes of Health, Bethesda, MD, USA
*
*Address for correspondence: S. Hwang, M.D., Department of Psychiatry, University of Nebraska Medical Center, 987830 Nebraska Medical Center, Omaha, NE 68198, USA. (Email: [email protected])
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

To determine the functional integrity of the neural systems involved in emotional responding/regulation and response control/inhibition in youth (age 10–18 years) with disruptive behavioral disorders (DBDs: conduct disorder and/or oppositional defiant disorder) as a function of callous-unemotional (CU) traits.

Method

Twenty-eight healthy youths and 35 youths with DBD [high CU (HCU), n = 18; low CU (LCU), n = 17] performed the fMRI Affective Stroop task. Participants viewed positive, neutral, and negative images under varying levels of cognitive load. A 3-way ANOVA (group×emotion by task) was conducted on the BOLD response data.

Results

Youth with DBD-HCU showed significantly less activation of ventromedial prefrontal cortex (vmPFC) and amygdala in response to negative stimuli, compared to healthy youth and youth with DBD-LCU. vmPFC responsiveness was inversely related to CU symptoms in DBD. Youth with DBD-LCU showed decreased functional connectivity between amygdala and regions including inferior frontal gyrus in response to emotional stimuli. Youth with DBD (LCU and HCU) additionally showed decreased insula responsiveness to high load (incongruent trials) compared to healthy youth. Insula responsiveness was inversely related to ADHD symptoms in DBD.

Conclusions

These data reveal two forms of pathophysiology in DBD. One associated with reduced amygdala and vmPFC responses to negative stimuli and related to increased CU traits. Another associated with reduced insula responses during high load task trials and related to ADHD symptoms. Appropriate treatment will need to be individualized according to the patient's specific pathophysiology.

Keywords

Amygdalacallous-unemotional traitdisruptive behavior disorderemotional respondingresponse inhibition
Type
Original Articles
Information
Psychological Medicine , Volume 46 , Issue 7 , May 2016 , pp. 1485 - 1496
Copyright
Copyright © Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

APA (2013). Diagnostic and Statistical Manual 5. American Psychiatric Association: Washington, D.C.Google Scholar
Baker, RH, Clanton, RL, Rogers, JC, De Brito, SA (2015). Neuroimaging findings in disruptive behavior disorders. CNS Spectrums 20, 369–381.Google Scholar
Blair, RJ (2013). The neurobiology of psychopathic traits in youths. Nature Reviews Neuroscience 14, 786–799.Google Scholar
Blair, KS, Smith, BW, Mitchell, DG, Morton, J, Vythilingam, M, Pessoa, L, Fridberg, D, Zametkin, A, Sturman, D, Nelson, EE, Drevets, WC, Pine, DS, Martin, A, Blair, RJ (2007). Modulation of emotion by cognition and cognition by emotion. Neuroimage 35, 430–440.Google Scholar
Blair, KS, Vythilingam, M, Crowe, SL, McCaffrey, DE, Ng, P, Wu, CC, Scaramozza, M, Mondillo, K, Pine, DS, Charney, DS, Blair, RJ (2013). Cognitive control of attention is differentially affected in trauma-exposed individuals with and without post-traumatic stress disorder. Psychological Medicine 43, 85–95.Google Scholar
Blair, RJ, Leibenluft, E, Pine, DS (2014). Conduct disorder and callous-unemotional traits in youth. New England Journal of Medicine 371, 2207–2216.Google Scholar
Buhle, JT, Silvers, JA, Wager, TD, Lopez, R, Onyemekwu, C, Kober, H, Weber, J, Ochsner, KN (2014). Cognitive reappraisal of emotion: a meta-analysis of human neuroimaging studies. Cerebral Cortex 24, 2981–2990.Google Scholar
Byrd, AL, Kahn, RE, Pardini, DA (2013). A validation of the inventory of callous-unemotional traits in a community sample of young adult males. Journal of Psychopathology and Behavioral Assessment 35, 1–26.CrossRefGoogle Scholar
Chambers, CD, Garavan, H, Bellgrove, MA (2009). Insights into the neural basis of response inhibition from cognitive and clinical neuroscience. Neuroscience & Biobehavioral Reviews 33, 631–646.Google Scholar
Conners, CK, Sitarenios, G, Parker, JD, Epstein, JN (1998). The revised Conners’ Parent Rating Scale (CPRS-R): factor structure, reliability, and criterion validity. Journal of Abnormal Child Psychology 26, 257–268.CrossRefGoogle ScholarPubMed
Criaud, M, Boulinguez, P (2013). Have we been asking the right questions when assessing response inhibition in go/no-go tasks with fMRI? A meta-analysis and critical review. Neuroscience & Biobehavioral Reviews 37, 11–23.Google Scholar
Critchley, H, Daly, E, Phillips, M, Brammer, M, Bullmore, E, Williams, S, Van Amelsvoort, T, Robertson, D, David, A, Murphy, D (2000). Explicit and implicit neural mechanisms for processing of social information from facial expressions: a functional magnetic resonance imaging study. Human Brain Mapping 9, 93–105.Google Scholar
Crowley, TJ, Dalwani, MS, Mikulich-Gilbertson, SK, Du, YP, Lejuez, CW, Raymond, KM, Banich, MT (2010). Risky decisions and their consequences: neural processing by boys with antisocial substance disorder. PLoS ONE 5, e12835.CrossRefGoogle ScholarPubMed
Cuthbert, BN, Insel, TR (2013). Toward the future of psychiatric diagnosis: the seven pillars of RDoC. BMC Medicine 11, 126.Google Scholar
Davidson, RJ, Putnam, KM, Larson, CL (2000). Dysfunction in the neural circuitry of emotion regulation – a possible prelude to violence. Science 289, 591–594.Google Scholar
Erthal, FS, de Oliveira, L, Mocaiber, I, Pereira, MG, Machado-Pinheiro, W, Volchan, E, Pessoa, L (2005). Load-dependent modulation of affective picture processing. Cognitive, Affective & Behavioral Neuroscience 5, 388–395.Google Scholar
Fairchild, G, Hagan, CC, Passamonti, L, Walsh, ND, Goodyer, IM, Calder, AJ (2014). Atypical neural responses during face processing in female adolescents with conduct disorder. Journal of the American Academy of Child & Adolescent Psychiatry 53, 677–687.Google Scholar
Finger, EC, Marsh, AA, Blair, KS, Reid, ME, Sims, C, Ng, P, Pine, DS, Blair, RJ (2011). Disrupted reinforcement signaling in the orbitofrontal cortex and caudate in youths with conduct disorder or oppositional defiant disorder and a high level of psychopathic traits. American Joujrnal of Psychiatry 168, 152–162.Google Scholar
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, 586–594.CrossRefGoogle ScholarPubMed
Frick, PJ (2004). The Inventory of Callous-Unemotional Traits. University of New Orleans: New Orleans.Google Scholar
Frick, PJ, Ray, JV, Thornton, LC, Kahn, RE (2014). Annual research review: a developmental psychopathology approach to understanding callous-unemotional traits in children and adolescents with serious conduct problems. Journal of Child Psychology and Psychiatry 55, 532–548.CrossRefGoogle ScholarPubMed
Fusar-Poli, P, Placentino, A, Carletti, F, Landi, P, Allen, P, Surguladze, S, Benedetti, F, Abbamonte, M, Gasparotti, R, Barale, F, Perez, J, McGuire, P, Politi, P (2009). Functional atlas of emotional faces processing: a voxel-based meta-analysis of 105 functional magnetic resonance imaging studies. Journal of Psychiatry & Neuroscience 34, 418–432.Google ScholarPubMed
Gold, AL, Morey, RA, McCarthy, G (2015). Amygdala-prefrontal cortex functional connectivity during threat-induced anxiety and goal distraction. Biological Psychiatry 77, 394–403.Google Scholar
Gyurak, A, Gross, JJ, Etkin, A (2011). Explicit and implicit emotion regulation: a dual-process framework. Cognition and Emotion 25, 400–412.Google Scholar
Herpers, PC, Scheepers, FE, Bons, DM, Buitelaar, JK, Rommelse, NN (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
Hwang, S, White, SF, Nolan, ZT, Sinclair, S, Blair, RJ (2014). Neurodevelopmental changes in the responsiveness of systems involved in top down attention and emotional responding. Neuropsychologia 62, 277–285.Google Scholar
Insel, T, Cuthbert, B, Garvey, M, Heinssen, R, Pine, DS, Quinn, K, Sanislow, C, Wang, P (2010). Research domain criteria (RDoC): toward a new classification framework for research on mental disorders. American Journal of Psychiatry 167, 748–751.Google Scholar
Kaufman, J, Birmaher, B, Brent, D, Rao, U, Flynn, C, Moreci, P, Williamson, D, Ryan, N (1997). Schedule for Affective Disorders and Schizophrenia for School-Age Children-Present and Lifetime version (K-SADS-PL): initial reliability and validity data. Journal of the American Academy of Child & Adolescent Psychiatry 36, 980–988.CrossRefGoogle ScholarPubMed
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, 241–252.Google Scholar
Koenigs, M, Grafman, J (2009). Posttraumatic stress disorder: the role of medial prefrontal cortex and amygdala. Neuroscientist 15, 540–548.Google Scholar
Lang, PJBM, Cuthbert, BN (2005). International Affective Picture System (IAPS): Affective Ratings of Pictures and Instruction Manual. University of Florida: Gainesville, FL.Google Scholar
Loeber, R, Burke, J, Pardini, DA (2009). Perspectives on oppositional defiant disorder, conduct disorder, and psychopathic features. Journal of Child Psychology and Psychiatry 50, 133–142.Google Scholar
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, 627–636.CrossRefGoogle ScholarPubMed
Marsh, AA, Finger, EC, Fowler, KA, Jurkowitz, IT, Schechter, JC, Yu, HH, Pine, DS, Blair, RJ (2011). 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, DG, Reid, ME, Sims, C, Kosson, DS, Towbin, KE, Leibenluft, E, Pine, DS, Blair, RJ (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
McLaren, DG, Ries, ML, Xu, G, Johnson, SC (2012). A generalized form of context-dependent psychophysiological interactions (gPPI): a comparison to standard approaches. Neuroimage 61, 1277–1286.CrossRefGoogle ScholarPubMed
Milad, MR, Quirk, GJ (2012). Fear extinction as a model for translational neuroscience: ten years of progress. Annual Review of Psychology 63, 129–151.Google Scholar
Mitchell, DG, Nakic, M, Fridberg, D, Kamel, N, Pine, DS, Blair, RJ (2007). The impact of processing load on emotion. Neuroimage 34, 1299–1309.CrossRefGoogle ScholarPubMed
Mitchell, DG, Richell, RA, Leonard, A, Blair, RJ (2006). Emotion at the expense of cognition: psychopathic individuals outperform controls on an operant response task. Journal of Abnormal Psychology 115, 559–566.CrossRefGoogle Scholar
Miyake, A, Friedman, NP (2012). The nature and organization of individual differences in executive functions: four general conclusions. Current Directions in Psychological Science 21, 8–14.Google Scholar
Motzkin, JC, Newman, JP, Kiehl, KA, Koenigs, M (2011). Reduced prefrontal connectivity in psychopathy. Journal of Neuroscience 31, 17348–17357.Google Scholar
Patrick, CJ, Fowles, DC, Krueger, RF (2009). Triarchic conceptualization of psychopathy: developmental origins of disinhibition, boldness, and meanness. Development and Psychopathology 21, 913–938.Google Scholar
Patrick, CJ, Venables, NC, Yancey, JR, Hicks, BM, Nelson, LD, Kramer, MD (2013). A construct-network approach to bridging diagnostic and physiological domains: application to assessment of externalizing psychopathology. Journal of Abnormal Psychology 122, 902–916.Google Scholar
Pessoa, L, McKenna, M, Gutierrez, E, Ungerleider, LG (2002). Neural processing of emotional faces requires attention. Proceedings of the National Academy of Sciences USA 99, 11458–11463.Google Scholar
Pessoa, L, Padmala, S, Morland, T (2005). Fate of unattended fearful faces in the amygdala is determined by both attentional resources and cognitive modulation. Neuroimage 28, 249–255.CrossRefGoogle ScholarPubMed
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, 44–57.Google Scholar
Schoenbaum, G, Roesch, MR, Stalnaker, TA (2006). Orbitofrontal cortex, decision-making and drug addiction. Trends in Neuroscience 29, 116–124.Google Scholar
Sebastian, CL, McCrory, EJ, Dadds, MR, Cecil, CA, Lockwood, PL, Hyde, ZH, De Brito, SA, Viding, E (2014). Neural responses to fearful eyes in children with conduct problems and varying levels of callous-unemotional traits. Psychological Medicine 44, 99–109.Google Scholar
Talairach, J, Tournoux, P (1988). Co-Planar Stereotaxic Atlas of the Human Brain. Thieme: Stuttgart.Google Scholar
Thomas, LA, Hall, JM, Skup, M, Jenkins, SE, Pine, DS, Leibenluft, E (2011). A developmental neuroimaging investigation of the change paradigm. Developmental Science 14, 148–161.Google Scholar
Viding, E, Sebastian, CL, Dadds, MR, Lockwood, PL, Cecil, CA, De Brito, SA, 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.CrossRefGoogle ScholarPubMed
Wechsler, D (1999). Wechsler Abbreviated Scale of Intelligence. Psychological Corporation: San Antonio, TX.Google Scholar
White, SF, Cruise, KR, Frick, PJ (2009). Differential correlates to self-report and parent-report of callous-unemotional traits in a sample of juvenile sexual offenders. Behavioral Science & the Law 27, 910–928.Google Scholar
White, SF, Fowler, KA, Sinclair, S, Schechter, JC, Majestic, CM, Pine, DS, Blair, RJ (2014). Disrupted expected value signaling in youth with disruptive behavior disorders to environmental reinforcers. Journal of the American Academy of Child and Adolescent Psychiatry 53, 579–588 e9.Google Scholar
White, SF, Marsh, AA, Fowler, KA, Schechter, JC, Adalio, C, Pope, K, Sinclair, S, Pine, DS, Blair, RJ (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
White, SF, Pope, K, Sinclair, S, Fowler, KA, Brislin, SJ, Williams, WC, Pine, DS, Blair, RJ (2013). Disrupted expected value and prediction error signaling in youths with disruptive behavior disorders during a passive avoidance task. American Journal of Psychiatry 170, 315–323.CrossRefGoogle ScholarPubMed
Young, SE, Friedman, NP, Miyake, A, Willcutt, EG, Corley, RP, Haberstick, BC, Hewitt, JK (2009). Behavioral disinhibition: liability for externalizing spectrum disorders and its genetic and environmental relation to response inhibition across adolescence. Journal of Abnormal Psychology 118, 117–130.Google Scholar
Supplementary material: File

Hwang supplementary material

Hwang supplementary material 1

Download Hwang supplementary material(File)
File 161.5 KB