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Journal of the American Academy of Child & Adolescent Psychiatry

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Neuroimaging Evidence for Right Orbitofrontal Cortex Differences in Adolescents With Emotional and Behavioral Dysregulation - 23/10/19

Doi : 10.1016/j.jaac.2019.01.021 
Philip A. Spechler, MA a, b, ⁎ , Bader Chaarani, PhD a, b, Catherine Orr, PhD a, Scott Mackey, PhD a, Stephen T. Higgins, PhD a, b, Tobias Banaschewski, MD, PhD c, Arun L.W. Bokde, PhD e, Uli Bromberg, PhD f, Christian Büchel, MD f, Erin Burke Quinlan, PhD g, Patricia J. Conrod, PhD h, Sylvane Desrivières, PhD g, Herta Flor, PhD c, d, Vincent Frouin, PhD i, Penny Gowland, PhD j, Andreas Heinz, MD, PhD k, Bernd Ittermann, PhD l, Jean-Luc Martinot, MD, PhD m, Frauke Nees, PhD c, Dimitri Papadopoulos Orfanos, PhD i, Luise Poustka, MD n, Juliane H. Fröhner, MSc o, Michael N. Smolka, MD o, Henrik Walter, MD, PhD k, Robert Whelan, PhD p, Gunter Schumann, MD g, Hugh Garavan, PhD a, b, Robert R. Althoff, MD, PhD a, b
the

IMAGEN Consortium

Tobias Banaschewski, MD, PhD, Gareth Barker, PhD, Arun L.W. Bokde, PhD, Uli Bromberg, Dipl-Psych, Christian Büchel, MD, Erin Burke Quinlan, PhD, Sylvane Desrivières, PhD, Herta Flor, PhD, Vincent Frouin, PhD, Hugh Garavan, PhD, Penny Gowland, PhD, Andreas Heinz, MD, PhD, Bernd Ittermann, PhD, Jean-Luc Martinot, MD, PhD, Marie-Laure Paillère Martinot, MD, PhD, Eric Artiges, MD, PhD, Herve Lemaitre, PhD, Frauke Nees, PhD, Dimitri Papadopoulos Orfanos, PhD, Tomáš Paus, MD, PhD, Luise Poustka, MD, Michael N. Smolka, MD, Nora C. Vetter, PhD, Sarah Jurk, Dipl-Psych, Eva Mennigen, MD, Henrik Walter, MD, PhD, Robert Whelan, PhD, Gunter Schumann, MD

a University of Vermont, Burlington 
b Vermont Center on Behavior and Health, University of Vermont, Burlington 
c Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany 
d School of Social Sciences, University of Mannheim, Mannheim, Germany 
e School of Medicine and Trinity College Institute of Neuroscience, Trinity College Dublin, Ireland 
f University Medical Centre Hamburg-Eppendorf, Hamburg, Germany 
g Centre for Population Neuroscience and Stratified Medicine (PONS) and MRC-SGDP Centre, Institute of Psychiatry, Psychology & Neuroscience, King’s College London, UK 
h Universite de Montreal, CHU Ste Justine Hospital, Canada 
i NeuroSpin, CEA, Université Paris-Saclay, France 
j Sir Peter Mansfield Imaging Centre School of Physics and Astronomy, University of Nottingham, University Park, UK 
k Campus Charité Mitte, Charité, Universitätsmedizin Berlin, Germany 
l Physikalisch-Technische Bundesanstalt (PTB), Berlin, Germany 
m Institut National de la Santé et de la Recherche Médicale, INSERM Unit 1000 “Neuroimaging & Psychiatry”, University Paris Sud – University Paris Saclay, France 
n University Medical Centre Göttingen, Germany, and the Clinic for Child and Adolescent Psychiatry, Medical University of Vienna, Austria 
o Technische Universität Dresden, Germany 
p School of Psychology and Global Brain Health Institute, Trinity College Dublin, Ireland 

∗Correspondence to Philip A. Spechler, MA, 1 South Prospect Street, Burlington, VT 05405.1 South Prospect StreetBurlingtonVT05405

Abstract

Objective

To characterize the structural and functional neurobiology of a large group of adolescents exhibiting a behaviorally and emotionally dysregulated phenotype.

Method

Adolescents aged 14 years from the IMAGEN study were investigated. Latent class analysis (LCA) on the Strengths and Difficulties Questionnaire (SDQ) was used to identify a class of individuals with elevated behavioral and emotional difficulties (“dysregulated”; n = 233) who were compared to a matched sample from a low symptom class (controls, n = 233). Whole-brain gray matter volume (GMV) images were compared using a general linear model with 10,000 random label permutations. Regional GMV findings were then probed for functional differences from three functional magnetic resonance imaging (fMRI) tasks. Significant brain features then informed mediation path models linking the likelihood of psychiatric disorders (DSM-IV) with dysregulation.

Results

Whole-brain differences were found in the right orbitofrontal cortex (R.OFC; p < .05; k = 48), with dysregulated individuals exhibiting lower GMV. The dysregulated group also exhibited higher activity in this region during successful inhibitory control (F1,429 = 7.53, p < .05). Path analyses indicated significant direct effects between the likelihood of psychopathologies and dysregulation. Modeling the R.OFC as a mediator returned modest partial effects, suggesting that the path linking the likelihood of an anxiety or conduct disorder diagnoses to dysregulation is partially explained by this anatomical feature.

Conclusion

A large sample of dysregulated adolescents exhibited lower GMV in the R.OFC relative to controls. Dysregulated individuals also exhibited higher regional activations when exercising inhibitory control at performance levels comparable to those of controls. These findings suggest a neurobiological marker of dysregulation and highlight the role of the R.OFC in impaired emotional and behavioral control.

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Key words : dysregulation, SDQ, orbitofrontal cortex, adolescence, VBM


Plan


 This article was reviewed under and accepted by Dr. Argyris Stringaris, MD, PhD.
 This work received support from the following sources: the European Union-funded FP6 Integrated Project IMAGEN (Reinforcement-related behaviour in normal brain function and psychopathology) (LSHM-CT-2007-037286), the Horizon 2020 funded ERC Advanced Grant ‘STRATIFY’ (Brain network based stratification of reinforcement-related disorders) (695313), ERANID (Understanding the Interplay between Cultural, Biological and Subjective Factors in Drug Use Pathways) (PR-ST-0416-10004), BRIDGET (JPND: BRain Imaging, cognition Dementia and next generation GEnomics) (MR/N027558/1), the FP7 projects IMAGEMEND (602450; IMAging GEnetics for MENtal Disorders) and MATRICS (603016), the Innovative Medicine Initiative Project EU-AIMS (115300-2), the Medical Research Council Grant 'c-VEDA’ (Consortium on Vulnerability to Externalizing Disorders and Addictions) (MR/N000390/1), the Swedish Research Council FORMAS, the Medical Research Council, the National Institute for Health Research (NIHR) Biomedical Research Centre at South London and Maudsley NHS Foundation Trust and King’s College London, the Bundesministerium für Bildung und Forschung (BMBF grants 01GS08152; 01EV0711; eMED SysAlc01ZX1311A; Forschungsnetz AERIAL 01EE1406A, 01EE1406B), the Deutsche Forschungsgemeinschaft (DFG grants SM 80/7-2, SFB 940/2), and the Medical Research Foundation and Medical Research Council (grant MR/R00465X/1). Further support was provided by grants from: ANR (project AF12-NEUR0008-01-WM2NA and ANR-12-SAMA-0004), the Fondation de France, the Fondation pour la Recherche Médicale, the Mission Interministérielle de Lutte-contre-les-Drogues-et-les-Conduites-Addictives (MILDECA), the Assistance-Publique-Hôpitaux-de-Paris and INSERM (interface grant), Paris Sud University IDEX 2012; the National Institutes of Health, Science Foundation Ireland (16/ERCD/3797), U.S.A. (Axon, Testosterone and Mental Health during Adolescence; RO1 MH085772-01A1), and by NIH Consortium grant U54 EB020403, supported by a cross-NIH alliance that funds Big Data to Knowledge Centres of Excellence. In addition, Drs. Garavan and Althoff are supported by P20GM103644 (PI: Stephen T. Higgins), Agency: NIGMS Vermont Center on Behavior and Health.
 Disclosure: Dr. Banaschewski has served as an advisor or consultant to Bristol-Myers Squibb, Desitin Arzneimittel, Eli Lilly and Co., Medice, Novartis, Pfizer, Shire, UCB, and Vifor Pharma. He has received conference attendance support, conference support, or speaking fees from Eli Lilly and Co., Janssen McNeil, Medice, Novartis, Shire, and UCB. He has been involved in clinical trials conducted by Eli Lilly and Co., Novartis, and Shire. The present work is unrelated to these relationships. Dr. Althoff is formerly employed, in part, by the nonprofit Research Center for Children, Youth, and Families. He has received grant or research support from the National Institute of Mental Health, the National Institute of General Medical Sciences, the National Institute on Drug Abuse, the Klingenstein Third Generation Foundation, and the Marcus Autism Center. He has served on the editorial board of Child Psychiatry and Human Development and as consulting editor of the Journal of Clinical Child and Adolescent Psychology. He has received honoraria from Oakstone Medical Publishing, Massachusetts General Hospital Psychiatry Academy, and Frontline Medical Communications, Inc. He is a partner of WISER Systems, LLC. Drs. Chaarani, Orr, Mackey, Higgins, Bokde, Bromberg, Büchel, Quinlan, Conrod, Desrivières, Flor, Frouin, Gowland, Heinz, Ittermann, Martinot, Nees, Orfanos, Poustka, Smolka, Walter, Whelan, Schumann, and Garavan, Mr. Spechler, and Ms. Fröhner report no biomedical financial interests or potential conflicts of interest.


© 2019  American Academy of Child and Adolescent Psychiatry. Publié par Elsevier Masson SAS. Tous droits réservés.
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Vol 58 - N° 11

P. 1092-1103 - novembre 2019 Retour au numéro
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