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

  • S. Hwang (a1), Z. T. Nolan (a2), S. F. White (a3), W. C. Williams (a4), S. Sinclair (a5) and R. J. R. Blair (a5)...

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.

Copyright

Corresponding author

*Address for correspondence: S. Hwang, M.D., Department of Psychiatry, University of Nebraska Medical Center, 987830 Nebraska Medical Center, Omaha, NE 68198, USA. (Email: soonjo.hwang@unmc.edu)

References

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APA (2013). Diagnostic and Statistical Manual 5. American Psychiatric Association: Washington, D.C.
Baker, RH, Clanton, RL, Rogers, JC, De Brito, SA (2015). Neuroimaging findings in disruptive behavior disorders. CNS Spectrums 20, 369381.
Blair, RJ (2013). The neurobiology of psychopathic traits in youths. Nature Reviews Neuroscience 14, 786799.
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, 430440.
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, 8595.
Blair, RJ, Leibenluft, E, Pine, DS (2014). Conduct disorder and callous-unemotional traits in youth. New England Journal of Medicine 371, 22072216.
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, 29812990.
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, 126.
Chambers, CD, Garavan, H, Bellgrove, MA (2009). Insights into the neural basis of response inhibition from cognitive and clinical neuroscience. Neuroscience & Biobehavioral Reviews 33, 631646.
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, 257268.
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, 1123.
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, 93105.
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.
Cuthbert, BN, Insel, TR (2013). Toward the future of psychiatric diagnosis: the seven pillars of RDoC. BMC Medicine 11, 126.
Davidson, RJ, Putnam, KM, Larson, CL (2000). Dysfunction in the neural circuitry of emotion regulation – a possible prelude to violence. Science 289, 591594.
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, 388395.
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, 677687.
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, 152162.
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 (2004). The Inventory of Callous-Unemotional Traits. University of New Orleans: New Orleans.
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, 532548.
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, 418432.
Gold, AL, Morey, RA, McCarthy, G (2015). Amygdala-prefrontal cortex functional connectivity during threat-induced anxiety and goal distraction. Biological Psychiatry 77, 394403.
Gyurak, A, Gross, JJ, Etkin, A (2011). Explicit and implicit emotion regulation: a dual-process framework. Cognition and Emotion 25, 400412.
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, 245273.
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, 277285.
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, 748751.
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, 980988.
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.
Koenigs, M, Grafman, J (2009). Posttraumatic stress disorder: the role of medial prefrontal cortex and amygdala. Neuroscientist 15, 540548.
Lang, PJBM, Cuthbert, BN (2005). International Affective Picture System (IAPS): Affective Ratings of Pictures and Instruction Manual. University of Florida: Gainesville, FL.
Loeber, R, Burke, J, Pardini, DA (2009). Perspectives on oppositional defiant disorder, conduct disorder, and psychopathic features. Journal of Child Psychology and Psychiatry 50, 133142.
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, 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, 279286.
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, 712720.
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, 12771286.
Milad, MR, Quirk, GJ (2012). Fear extinction as a model for translational neuroscience: ten years of progress. Annual Review of Psychology 63, 129151.
Mitchell, DG, Nakic, M, Fridberg, D, Kamel, N, Pine, DS, Blair, RJ (2007). The impact of processing load on emotion. Neuroimage 34, 12991309.
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, 559566.
Miyake, A, Friedman, NP (2012). The nature and organization of individual differences in executive functions: four general conclusions. Current Directions in Psychological Science 21, 814.
Motzkin, JC, Newman, JP, Kiehl, KA, Koenigs, M (2011). Reduced prefrontal connectivity in psychopathy. Journal of Neuroscience 31, 1734817357.
Patrick, CJ, Fowles, DC, Krueger, RF (2009). Triarchic conceptualization of psychopathy: developmental origins of disinhibition, boldness, and meanness. Development and Psychopathology 21, 913938.
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, 902916.
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, 1145811463.
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, 249255.
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.
Schoenbaum, G, Roesch, MR, Stalnaker, TA (2006). Orbitofrontal cortex, decision-making and drug addiction. Trends in Neuroscience 29, 116124.
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, 99109.
Talairach, J, Tournoux, P (1988). Co-Planar Stereotaxic Atlas of the Human Brain. Thieme: Stuttgart.
Thomas, LA, Hall, JM, Skup, M, Jenkins, SE, Pine, DS, Leibenluft, E (2011). A developmental neuroimaging investigation of the change paradigm. Developmental Science 14, 148161.
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, 11091116.
Wechsler, D (1999). Wechsler Abbreviated Scale of Intelligence. Psychological Corporation: San Antonio, TX.
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, 910928.
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, 579588 e9.
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, 750758.
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, 315323.
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, 117130.

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

  • S. Hwang (a1), Z. T. Nolan (a2), S. F. White (a3), W. C. Williams (a4), S. Sinclair (a5) and R. J. R. Blair (a5)...

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