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http://dx.doi.org/10.9758/cpn.2018.16.4.449

Dysfunctional Social Reinforcement Processing in Disruptive Behavior Disorders: An Functional Magnetic Resonance Imaging Study  

Hwang, Soonjo (Department of Psychiatry, University of Nebraska Medical Center)
Meffert, Harma (Center for Neurobehavioral Research, Boys Town National Research Hospital)
VanTieghem, Michelle R. (Department of Psychology, Columbia University)
Sinclair, Stephen (Department of Health and Human Services, Section on Affective Cognitive Neuroscience, National Institute of Mental Health, National Institutes of Health)
Bookheimer, Susan Y. (University of California and Brain Research Institute)
Vaughan, Brigette (Department of Psychiatry, University of Nebraska Medical Center)
Blair, R.J.R. (Center for Neurobehavioral Research, Boys Town National Research Hospital)
Publication Information
Clinical Psychopharmacology and Neuroscience / v.16, no.4, 2018 , pp. 449-460 More about this Journal
Abstract
Objective: Prior functional magnetic resonance imaging (fMRI) work has revealed that children/adolescents with disruptive behavior disorders (DBDs) show dysfunctional reward/non-reward processing of non-social reinforcements in the context of instrumental learning tasks. Neural responsiveness to social reinforcements during instrumental learning, despite the importance of this for socialization, has not yet been previously investigated. Methods: Twenty-nine healthy children/adolescents and 19 children/adolescents with DBDs performed the fMRI social/non-social reinforcement learning task. Participants responded to random fractal image stimuli and received social and non-social rewards/non-rewards according to their accuracy. Results: Children/adolescents with DBDs showed significantly reduced responses within the caudate and posterior cingulate cortex (PCC) to non-social (financial) rewards and social non-rewards (the distress of others). Connectivity analyses revealed that children/adolescents with DBDs have decreased positive functional connectivity between the ventral striatum (VST) and the ventromedial prefrontal cortex (vmPFC) seeds and the lateral frontal cortex in response to reward relative to non-reward, irrespective of its sociality. In addition, they showed decreased positive connectivity between the vmPFC seed and the amygdala in response to non-reward relative to reward. Conclusion: These data indicate compromised reinforcement processing of both non-social rewards and social non-rewards in children/adolescents with DBDs within core regions for instrumental learning and reinforcement-based decision-making (caudate and PCC). In addition, children/adolescents with DBDs show dysfunctional interactions between the VST, vmPFC, and lateral frontal cortex in response to rewarded instrumental actions potentially reflecting disruptions in attention to rewarded stimuli.
Keywords
Disruptive behavior disorder; Social reward; Ventral striatum; Posterior cingulate cortex; Caudate; Ventro-medial prefrontal cortex;
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1 Ma I, van Holstein M, Mies GW, Mennes M, Buitelaar J, Cools R, et al. Ventral striatal hyperconnectivity during rewarded interference control in adolescents with ADHD. Cortex 2016;82:225-236.   DOI
2 Jollans L, Zhipeng C, Icke I, Greene C, Kelly C, Banaschewski T, et al. Ventral striatum connectivity during reward anticipation in adolescent smokers. Dev Neuropsychol 2016;41:6-21.   DOI
3 American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders: DSM-5. Washington D.C.: American Psychiatric Association;2013.
4 White SF, Pope K, Sinclair S, Fowler KA, Brislin SJ, Williams WC, et al. Disrupted expected value and prediction error signaling in youths with disruptive behavior disorders during a passive avoidance task. Am J Psychiatry 2013;170:315-323.   DOI
5 White SF, Tyler PM, Erway AK, Botkin ML, Kolli V, Meffert H, et al. Dysfunctional representation of expected value is associated with reinforcement-based decision-making deficits in adolescents with conduct problems. J Child Psychol Psychiatry 2016;57:938-946.   DOI
6 Matthys W, Vanderschuren LJ, Schutter DJ, Lochman JE. Impaired neurocognitive functions affect social learning processes in oppositional defiant disorder and conduct disorder: implications for interventions. Clin Child Fam Psychol Rev 2012;15:234-246.   DOI
7 Crowley TJ, Dalwani MS, Mikulich-Gilbertson SK, Du YP, Lejuez CW, Raymond KM, et al. Risky decisions and their consequences: neural processing by boys with antisocial substance disorder. PLoS One 2010;5:e12835.   DOI
8 Blair RJ, Leibenluft E, Pine DS. Conduct disorder and callous-unemotional traits in youth. N Engl J Med 2014;371:23:2207-2216.
9 Clithero JA, Rangel A. Informatic parcellation of the network involved in the computation of subjective value. Soc Cogn Affect Neurosci 2014;9:1289-1302.   DOI
10 Ernst M, Paulus MP. Neurobiology of decision making: a selective review from a neurocognitive and clinical perspective. Biol Psychiatry 2005;58:597-604.   DOI
11 Lozier LM, Cardinale EM, VanMeter JW, Marsh AA. 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.   DOI
12 Marsh AA, Finger EC, Mitchell DG, Reid ME, Sims C, Kosson DS, et al. Reduced amygdala response to fearful expressions in children and adolescents with callous-unemotional traits and disruptive behavior disorders. Am J Psychiatry 2008;165:712-720.   DOI
13 Blair RJ, Colledge E, Murray L, Mitchell DG. A selective impairment in the processing of sad and fearful expressions in children with psychopathic tendencies. J Abnorm Child Psychol 2001;29:491-498.   DOI
14 White SF, Marsh AA, Fowler KA, Schechter JC, Adalio C, Pope K, et al. Reduced amygdala response in youths with disruptive behavior disorders and psychopathic traits: decreased emotional response versus increased top-down attention to nonemotional features. Am J Psychiatry 2012;169:750-758.   DOI
15 Blair RJ, White SF, Meffert H, Hwang S. Disruptive behavior disorders: taking an RDoC(ish) approach. Curr Top Behav Neurosci 2014;16:319-336.
16 Insel T, Cuthbert B, Garvey M, Heinssen R, Pine DS, Quinn K, et al. Research domain criteria (RDoC): toward a new classification framework for research on mental disorders. Am J Psychiatry 2010;167:748-751.   DOI
17 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.   DOI
18 Finger EC, Marsh A, Blair KS, Majestic C, Evangelou I, Gupta K, et al. Impaired functional but preserved structural connectivity in limbic white matter tracts in youth with conduct disorder or oppositional defiant disorder plus psychopathic traits. Psychiatry Res 2012;202:239-244.   DOI
19 Marsh AA, Finger EC, Fowler KA, Jurkowitz ITN, Schechter JC, Yu HH, et al. Reduced amygdala-orbitofrontal connectivity during moral judgments in youths with disruptive behavior disorders and psychopathic traits. Psychiatry Res 2011;194:279-286.   DOI
20 Aghajani M, Klapwijk ET, van der Wee NJ, Veer IM, Rombouts SARB, Boon AE, et al. Disorganized amygdala networks in conduct-disordered juvenile offenders with callous-unemotional traits. Biol Psychiatry 2017;82:283-293.   DOI
21 Wechsler D. Wechsler abbreviated scale of intelligence. San Antonio, TX.:Psychological Corporation;1999.
22 Budhani S, Marsh AA, Pine DS, Blair RJ. Neural correlates of response reversal: considering acquisition. Neuroimage 2007;34:1754-1765.   DOI
23 Lin A, Adolphs R, Rangel A. Social and monetary reward learning engage overlapping neural substrates. Soc Cogn Affect Neurosci 2012;7:274-281.   DOI
24 Chang SW, Fagan NA, Toda K, Utevsky AV, Pearson JM, Platt ML. Neural mechanisms of social decision-making in the primate amygdala. Proc Natl Acad Sci U S A 2015;112:16012-16017.   DOI
25 Meder D, Madsen KH, Hulme O, Siebner HR. Chasing probabilities - Signaling negative and positive prediction errors across domains. Neuroimage 2016;134:180-191.   DOI
26 Casey BJ, Forman SD, Franzen P, Berkowitz A, Braver TS, Nystrom LE, et al. Sensitivity of prefrontal cortex to changes in target probability: a functional MRI study. Hum Brain Mapp 2001;13:26-33.   DOI
27 Liu X, Powell DK, Wang H, Gold BT, Corbly CR, Joseph JE. Functional dissociation in frontal and striatal areas for processing of positive and negative reward information. J Neurosci 2007;27:4587-4597.   DOI
28 Kuhnen CM, Knutson B. The neural basis of financial risk taking. Neuron 2005;47:763-770.   DOI
29 Finger EC, Marsh AA, Mitchell DG, Reid ME, Sims C, Budhani S, et al. Abnormal ventromedial prefrontal cortex function in children with psychopathic traits during reversal learning. Arch Gen Psychiatry 2008;65:586-594.   DOI
30 McClure SM, York MK, Montague PR. The neural substrates of reward processing in humans: the modern role of FMRI. Neuroscientist 2004;10:260-268.   DOI
31 White SF, Fowler KA, Sinclair S, Schechter JC, Majestic CM, Pine DS, et al. Disrupted expected value signaling in youth with disruptive behavior disorders to environmental reinforcers. J Am Acad Child Adolesc Psychiatry 2014;53:579-588.e9.   DOI
32 McLaren DG, Ries ML, Xu G, Johnson SC. A generalized form of context-dependent psychophysiological interactions (gPPI): a comparison to standard approaches. Neuroimage 2012;61:1277-1286.   DOI
33 Talairach J, Tournoux P. Co-planar stereotaxic atlas of the human brain: an approch to cerebral imaging. Stuttgart:Thieme; 1988.
34 Lieberman MD, Cunningham WA. Type I and Type II error concerns in fMRI research: re-balancing the scale. Soc Cogn Affect Neurosci 2009;4:423-428.   DOI
35 Eklund A, Nichols TE, Knutsson H. Cluster failure: Why fMRI inferences for spatial extent have inflated false-positive rates. Proc Natl Acad Sci U S A 2016;113:7900-7905.   DOI
36 Hwang S, Nolan ZT, White SF, Williams WC, Sinclair S, Blair RJ. Dual neurocircuitry dysfunctions in disruptive behavior disorders: emotional responding and response inhibition. Psychol Med 2016;46:1485-1496.   DOI
37 Motzkin JC, Newman JP, Kiehl KA, Koenigs M. Reduced prefrontal connectivity in psychopathy. J Neurosci 2011;31:17348-17357.   DOI
38 Frick PJ. The inventory of callous-unemotional traits. New Orleans:University of New Orleans;2004.
39 Silverman MH, Jedd K, Luciana M. Neural networks involved in adolescent reward processing: an activation likelihood estimation meta-analysis of functional neuroimaging studies. Neuroimage 2015;122:427-439.   DOI
40 O'Doherty J, Dayan P, Schultz J, Deichmann R, Friston K, Dolan RJ. Dissociable roles of ventral and dorsal striatum in instrumental conditioning. Science 2004;304:452-454.   DOI
41 Scott-Van Zeeland AA, Dapretto M, Ghahremani DG, Poldrack RA, Bookheimer SY. Reward processing in autism. Autism Res 2010;3:53-67.
42 Rubia K, Smith AB, Halari R, Matsukura F, Mohammad M, Taylor E, et al. Disorder-specific dissociation of orbitofrontal dysfunction in boys with pure conduct disorder during reward and ventrolateral prefrontal dysfunction in boys with pure ADHD during sustained attention. Am J Psychiatry 2009;166:83-94.   DOI
43 Finger EC, Marsh AA, Blair KS, Reid ME, Sims C, Ng P, et al. 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. Am J Psychiatry 2011;168:152-162.   DOI
44 Blakemore SJ. The social brain in adolescence. Nat Rev Neurosci 2008;9:267-277.
45 Blair RJ, White SF, Meffert H, Hwang S. Emotional learning and the development of differential moralities: implications from research on psychopathy. Ann N Y Acad Sci 2013;1299:36-41.   DOI
46 Averill JR. Anger and aggression: an essay on emotion. New York:Springer-Verlag;1982.
47 Blair RJ. Facial expressions, their communicatory functions and neuro-cognitive substrates. Philos Trans R Soc Lond B Biol Sci 2003;358:561-572.   DOI
48 Dawel A, O'Kearney R, McKone E, Palermo R. Not just fear and sadness: meta-analytic evidence of pervasive emotion recognition deficits for facial and vocal expressions in psychopathy. Neurosci Biobehav Rev 2012;36:2288-2304.   DOI
49 Marsh AA, Blair RJ. Deficits in facial affect recognition among antisocial populations: a meta-analysis. Neurosci Biobehav Rev 2008;32:454-465.   DOI
50 Wendler E, Gaspar JC, Ferreira TL, Barbiero JK, Andreatini R, Vital MA, et al. The roles of the nucleus accumbens core, dorsomedial striatum, and dorsolateral striatum in learning: performance and extinction of Pavlovian fear-conditioned responses and instrumental avoidance responses. Neurobiol Learn Mem 2014;109:27-36.   DOI
51 Wrase J, Kahnt T, Schlagenhauf F, Beck A, Cohen MX, Knutson B, et al. Different neural systems adjust motor behavior in response to reward and punishment. Neuroimage 2007;36:1253-1262.   DOI
52 Blair RJ, Jones L, Clark F, Smith M. The psychopathic individual: a lack of responsiveness to distress cues? Psychophysiology 1997;34:192-198.   DOI
53 Passamonti L, Fairchild G, Goodyer IM, Hurford G, Hagan CC, Rowe JB, et al. Neural abnormalities in early-onset and adolescence-onset conduct disorder. Arch Gen Psychiatry 2010;67:729-738.   DOI
54 Blair RJ. The amygdala and ventromedial prefrontal cortex in morality and psychopathy. Trends Cogn Sci 2007;11:387-392.   DOI
55 Blair RJ. A cognitive developmental approach to mortality: investigating the psychopath. Cognition 1995;57:1-29.   DOI
56 Haber SN, Knutson B. The reward circuit: linking primate anatomy and human imaging. Neuropsychopharmacology 2010;35:4-26.   DOI