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Chronotype, Longitudinal Volumetric Brain Variations Throughout Adolescence, and Depressive Symptom Development - 27/12/22

Doi : 10.1016/j.jaac.2022.06.003 
Hélène Vulser, MD, PhD a, d, , Hervé S. Lemaître, PhD e, Stella Guldner, MSc a, Pauline Bezivin-Frère, PhD f, Martin Löffler, PhD a, Anna S. Sarvasmaa, MD, PhD h, Jessica Massicotte-Marquez, PhD f, Eric Artiges, MD, PhD f, g, Marie-Laure Paillère Martinot, MD, PhD d, f, Irina Filippi, PhD f, Ruben Miranda, MPsych d, Argyris Stringaris, MD, PhD, FRCPsych i, Betteke Maria van Noort, PhD j, Jani Penttilä, MD, PhD k, Yvonne Grimmer, MD l, Andreas Becker, PhD, Dipl-Psych m, Tobias Banaschewski, MD, PhD l, Arun L.W. Bokde, PhD n, Sylvane Desrivières, PhD o, Juliane H. Fröhner, MSc u, Hugh Garavan, PhD q, Antoine Grigis, PhD p, Penny A. Gowland, PhD r, Andreas Heinz, MD, PhD s, Dimitri Papadopoulos Orfanos, PhD p, Luise Poustka, MD t, Michael N. Smolka, MD u, Philip A. Spechler, PhD q, Henrik Walter, MD, PhD s, Robert Whelan, PhD v, Gunter Schumann, MD, PhD w, Herta Flor, PhD a, c, Jean-Luc Martinot, MD, PhD f, Frauke Nees, PhD a, b
for the

IMAGEN Consortium

a Institute of Cognitive and Clinical Neuroscience, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Germany 
b Institute of Medical Psychology and Medical Sociology, University Medical Center Schleswig Holstein, Kiel University, Kiel, Germany, and the Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Germany 
c School of Social Sciences, University of Mannheim, Germany 
d AP-HP Sorbonne Université, Pitié-Salpêtrière Hospital, France 
e Institut des Maladies Neurodégénératives, UMR 5293, CNRS, CEA, Université de Bordeaux, Bordeaux, France 
f Institut National de la Santé et de la Recherche Médicale, INSERM U1299 A10 “Trajectoires développementales en psychiatrie,” Ecole Normale supérieure Paris-Saclay, Université Paris-Saclay, Université de Paris, CNRS UMR9010, Centre Borelli, Gif-sur-Yvette, France 
g EPS Barthélémy Durand, Etampes, France 
h National Institute for Health and Welfare, Mental Health Unit, Helsinki, Finland, and the University of Helsinki and Helsinki University Hospital, Helsinki, Finland 
i National Institute of Mental Health, Bethesda, Maryland 
j MSB Medical School Berlin, Hochschule für Gesundheit und Medizin, Siemens Villa, Berlin 
k Psychosocial Services Adolescent Outpatient Clinic, Lahti, Finland 
l Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany 
m University Medical Center, Göttingen 
n School of Medicine and Trinity College Institute of Neuroscience, Trinity College Dublin, Dublin, Ireland 
o Centre for Population Neuroscience and Precision Medicine (PONS), Institute of Psychiatry, Psychology & Neuroscience, SGDP Centre, King’s College London, London, United Kingdom 
p NeuroSpin, Commissariat à l’Energie Atomique, Université Paris-Saclay, Gif-sur-Yvette, France 
q University of Vermont, Burlington 
r Sir Peter Mansfield Imaging Centre School of Physics and Astronomy, University of Nottingham, University Park, Nottingham, United Kingdom 
s Charité – Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany 
t University Medical Centre Göttingen, Göttingen, Germany 
u Technische Universität Dresden, Dresden, Germany 
v School of Psychology and Global Brain Health Institute, Trinity College Dublin, Ireland 
w Centre for Population Neuroscience and Precision Medicine (PONS), Institute of Psychiatry, Psychology & Neuroscience, SGDP Centre, King’s College London, London, United Kingdom, the PONS Research Group, Campus Charite Mitte, Humboldt University, Berlin, Leibniz Institute for Neurobiology, Magdeburg, Germany and the Institute for Science and Technology of Brain-inspired Intelligence (ISTBI), Fudan University, Shanghai, P.R. China 

Correspondence to Hélène Vulser, MD, PhD, Centre du Neurodéveloppement Adulte, Service de Psychiatrie d’Adultes, Hôpital Pitié-Salpêtrière, 47-83 Boulevard de l’Hôpital, 75013 Paris, FranceCentre du Neurodéveloppement AdulteService de Psychiatrie d’AdultesHôpital Pitié-Salpêtrière47-83 Boulevard de l’HôpitalParis75013France

Abstract

Objective

Adolescence is a critical period for circadian rhythm, with a strong shift toward eveningness around age 14. Also, eveningness in adolescence has been found to predict later onset of depressive symptoms. However, no previous study has investigated structural variations associated with chronotype in early adolescence and how this adds to the development of depressive symptoms.

Method

Assessment of 128 community-based adolescents (51% girls) at age 14 and 19 years was performed. Using whole-brain voxel-based morphometry, baseline (at age 14) regional gray matter volumes (GMVs), follow-up (at age 19) regional GMVs, and longitudinal changes (between 14 and 19) associated with Morningness/Eveningness Scale in Children score and sleep habits at baseline were measured. The association of GMV with depressive symptoms at 19 years was studied, and the role of potential clinical and genetic factors as mediators and moderators was assessed.

Results

Higher eveningness was associated with larger GMV in the right medial prefrontal cortex at ages 14 and 19 in the whole sample. GMV in this region related to depressive symptoms at age 19 in catechol-O-methyltransferase (COMT) Val/Val, but not in Met COMT, carriers. Larger GMV also was observed in the right fusiform gyrus at age 14, which was explained by later wake-up time during weekends.

Conclusion

In adolescence, eveningness and its related sleep habits correlated with distinct developmental patterns. Eveningness was specifically associated with GMV changes in the medial prefrontal cortex; this could serve as a brain vulnerability factor for later self-reported depressive symptoms in COMT Val/Val carriers.

Le texte complet de cet article est disponible en PDF.

Key words : adolescent, chronotype, gray matter, longitudinal, MRI


Plan


 Dr. Martinot and Prof. Nees contributed equally to this work.
 This work received support from the following sources: European Union–funded FP6 Integrated Project IMAGEN (Reinforcement-related behaviour in normal brain function and psychopathology) (LSHM-CT-2007-037286), ANR (ANR-12-SAMA-0004 and AAPG2019–GeBra), Eranet Neuron (AF12-NEUR0008-01–WM2NA and ANR-18-NEUR00002-01–ADORe), Fondation de France (00081242), Fondation pour la Recherche Médicale (DPA20140629802), Mission Interministérielle de Lutte-contre-les-Drogues-et-les-Conduites-Addictives (MILDECA), Assistance-Publique-Hôpitaux-de-Paris and INSERM (interface grant), Paris Sud University IDEX 2012, Fondation de l’Avenir (AP-RM-17-013), Fédération pour la Recherche sur le Cerveau, Horizon 2020–funded ERC Advanced Grant STRATIFY (Brain network based stratification of reinforcement-related disorders) (695313), Human Brain Project (HBP SGA 2, 785907 and HBP SGA 3, 945539), National Institute for Health Research (NIHR) Biomedical Research Centre at South London and Maudsley NHS Foundation Trust and King’s College London, Deutsche Forschungsgemeinschaft (SM 80/7-2, SFB 940, TRR 265, NE 1383/14-1), Medical Research Foundation and Medical Research Council (MR/R00465X/1 and MR/S020306/1). The INSERM and the Strasbourg University and SATT CONECTUS provided sponsorship (PI: Jean-Luc Martinot). Dr. Vulser was supported by post-doctoral fellowships from the Fondation Servier and Fondation Pierre Deniker. The funding sources had no involvement in the study design; the collection, analysis, and interpretation of data; the writing of the report; or the decision to submit the article for publication.
 The study protocol was approved by the Ethics Committee of Paris CPP IDF-VII.
 Consent has been provided for descriptions of specific patient information.
 This study was presented as an oral presentation at the 18ème édition du Congrès de l’Encéphale; January 22-24, 2020; Paris, France.
 Dr. Lemaître served as the statistical expert for this research.
 Disclosure: Dr. Stringaris has reported being a coauthor of the Affective Reactivity Index (ARI), a cost-free psychometric instrument. He has received royalties from Cambridge University Press for The Maudsley Reader in Phenomenological Psychiatry and Oxford University Press for Disruptive Mood: Irritability in Children and Adolescents. Dr. Banaschewski has served in an advisory or consultancy role for ADHS digital, InfectoPharm, Lundbeck, Medice, Neurim Pharmaceuticals, Oberberg GmbH, Roche, and Takeda. He has received conference support or speaker’s fees from Medice and Takeda. He has received royalties from Hogrefe, Kohlhammer, CIP Medien, and Oxford University Press. He has been involved in clinical trials conducted by Shire and Viforpharma. Dr. Poustka has served in an advisory or consultancy role for Roche and Viforpharm and has received speaker’s fees from Takeda, Medice, and InfectoPharm. She has received royalties from Hogrefe, Kohlhammer, and Schattauer. Drs. Vulser, Lemaître, Bezivin-Frère, Löffler, Sarvasmaa, Massicotte-Marquez, Artiges, Paillère Martinot, Filippi, van Noort, Penttilä, Grimmer, Becker, Bokde, Desrivières, Garavan, Grigis, Gowland, Heinz, Papadopoulos Orfanos, Smolka, Spechler, Walter, Whelan, Profs. Schumann and Flor, Dr. Martinot, Prof. Nees, Ms. Guldner, Mr. Miranda, and Ms. Fröhner have reported no biomedical financial interests or potential conflicts of interest.
 Author Contributions
 Conceptualization: Vulser, Lemaître, Guldner, Löffler, Sarvasmaa, Massicotte-Marquez, Paillère Martinot, Flor, Martinot
 Data curation: Vulser, Bezivin-Frère, Sarvasmaa, Artiges, Miranda, Garavan, Grigis, Papadopoulos Orfanos, Spechler
 Formal analysis: Vulser, Lemaître
 Funding acquisition: Vulser, Löffler, Flor, Martinot, Nees
 Investigation: Vulser, Guldner, Nees
 Methodology: Vulser, Lemaître, Guldner, Bezivin-Frère, Löffler, Artiges, Filippi, Miranda, Spechler, Flor, Nees
 Project administration: Banaschewski, Bokde, Desrivières, Fröhner, Gowland, Heinz, Papadopoulos Orfanos, Poustka, Smolka, Walter, Whelan, Schumann, Flor, Martinot, Nees
 Resources: Artiges, Filippi, Stringaris, van Noort, Penttilä, Grimmer, Becker, Flor, Martinot, Nees
 Software: Vulser, Lemaître, Bezivin-Frère, Filippi, Miranda
 Supervision: Lemaître, Flor, Nees
 Validation: Lemaître, Löffler, Stringaris, van Noort, Penttilä, Grimmer, Becker, Garavan, Nees
 Visualization: Nees
 Writing – original draft: Vulser, Lemaître, Guldner, Flor, Martinot, Nees
 Writing – review and editing: Vulser, Lemaître, Guldner, Bezivin-Frère, Löffler, Sarvasmaa, Massicotte-Marquez, Artiges, Paillère Martinot, Filippi, Miranda, Banaschewski, Bokde, Desrivières, Fröhner, Grigis, Gowland, Heinz, Papadopoulos Orfanos, Poustka, Smolka, Spechler, Walter, Whelan, Schumann, Flor, Martinot, Nees
 The IMAGEN Consortium collaborators: imagen-project.org/.
 The radiographer staff at Centre de NeuroImagerie de Recherche de l’Institut du Cerveau et de la Moelle épinière (mri.html?lang=en) is acknowledged for support in magnetic resonance imaging datasets acquisition.


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