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Chronotype, Longitudinal Volumetric Brain Variations Throughout Adolescence, and Depressive Symptom Development

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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.

Section snippets

Participants

Neuroimaging and clinical data were obtained from an existing large European multisite longitudinal study of adolescent development, IMAGEN (https://imagen-project.org/). A detailed description of recruitment and assessment procedures, with exclusion and inclusion criteria, has been published elsewhere.23 Notably, any obvious psychopathology at baseline (eg, bipolar disorder, schizophrenia, or major neurodevelopmental disorders), any severe medical somatic conditions, any history of head

Baseline Characteristics

Significant MESC-by-sex interaction was found for age and bedtime during weekdays. At baseline, MESC score (continuous) was associated with all the sleep characteristics except time in bed during weekdays (Table 1; Table S1, available online). Furthermore, MESC score (continuous) correlated with bedtime during weekdays in boys, but not in girls. Lower MESC score (continuous, ie, higher eveningness) also correlated with lower NEO Five-Factor Inventory (NEO-FFI) conscientiousness dimension score,

Discussion

In the present study, we investigated for the first time the association between regional GMV at age 14 and 19 and chronotype at age 14, explored the specificity of these changes compared with changes associated with chronotype sleep-related characteristics, and determined the association of such changes with later depressive symptoms. We observed that eveningness (both continuous and categorical) was associated with larger GMV in the right mPFC at age 14 and 5 years later at age 19. GMV in the

CRediT authorship contribution statement

Hélène Vulser: Writing – review & editing, Writing – original draft, Software, Methodology, Investigation, Funding acquisition, Formal analysis, Data curation, Conceptualization. Hervé S. Lemaître: Writing – review & editing, Writing – original draft, Validation, Supervision, Software, Methodology, Formal analysis, Conceptualization. Stella Guldner: Writing – review & editing, Writing – original draft, Methodology, Investigation, Conceptualization. Pauline Bezivin-Frère: Writing – review &

References (48)

  • A.D. Boes et al.

    Rostral anterior cingulate cortex volume correlates with depressed mood in normal healthy children

    Biol Psychiatry

    (2008)
  • G. Salvadore et al.

    Prefrontal cortical abnormalities in currently depressed versus currently remitted patients with major depressive disorder

    Neuroimage

    (2011)
  • K. Yucel et al.

    Increased subgenual prefrontal cortex size in remitted patients with major depressive disorder

    Psychiatry Res

    (2009)
  • Y. Dauvilliers et al.

    Catechol-O-methyltransferase, dopamine, and sleep-wake regulation

    Sleep Med Rev

    (2015)
  • R. Honea et al.

    Impact of interacting functional variants in COMT on regional gray matter volume in human brain

    Neuroimage

    (2009)
  • R.K. Lenroot et al.

    Sexual dimorphism of brain developmental trajectories during childhood and adolescence

    Neuroimage

    (2007)
  • M.A. Carskadon et al.

    Association between puberty and delayed phase preference

    Sleep

    (1993)
  • A. Sadeh et al.

    Sleep and the transition to adolescence: A longitudinal study

    Sleep

    (2009)
  • M. Gulec et al.

    Chronotype effects on general well-being and psychopathology levels in healthy young adults

    Biol Rhythm Res

    (2013)
  • D.A. Haraden et al.

    The relationship between depression and chronotype: A longitudinal assessment during childhood and adolescence

    Depress Anxiety

    (2017)
  • J.F. Van den Berg et al.

    Chronotype and depressive symptoms in students: An investigation of possible mechanisms

    Chronobiol Int

    (2018)
  • J. Rosenberg et al.

    Chronotype differences in cortical thickness: Grey matter reflects when you go to bed

    Brain Struct Funct

    (2018)
  • A.S. Urrila et al.

    Sleep habits, academic performance, and the adolescent brain structure

    Sci Rep

    (2017)
  • S. Whittle et al.

    Structural brain development and depression onset during adolescence: A prospective longitudinal study

    Am J Psychiatry

    (2014)

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    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: https://imagen-project.org/.

    The radiographer staff at Centre de NeuroImagerie de Recherche de l’Institut du Cerveau et de la Moelle épinière (http://www.cenir.org/mri.html?lang=en) is acknowledged for support in magnetic resonance imaging datasets acquisition.

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