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

Hélène Vulser; Hervé S Lemaître; Stella Guldner; Pauline Bezivin-Frère; Martin Löffler; Anna S Sarvasmaa; Jessica Massicotte-Marquez; Eric Artiges; Marie-Laure Paillère Martinot; Irina Filippi; Ruben Miranda; Argyris Stringaris; Betteke Maria van Noort; Jani Penttilä; Yvonne Grimmer; Andreas Becker; Tobias Banaschewski; Arun L W Bokde; Sylvane Desrivières; Juliane H Fröhner; Hugh Garavan; Antoine Grigis; Penny A Gowland; Andreas Heinz; Dimitri Papadopoulos Orfanos; Luise Poustka; Michael N Smolka; Philip A Spechler; Henrik Walter; Robert Whelan; Gunter Schumann; Herta Flor; Jean-Luc Martinot; Frauke Nees; IMAGEN Consortium

doi:10.1016/j.jaac.2022.06.003

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

J Am Acad Child Adolesc Psychiatry. 2023 Jan;62(1):48-58. doi: 10.1016/j.jaac.2022.06.003. Epub 2022 Jun 15.

Authors

Hélène Vulser¹, Hervé S Lemaître², Stella Guldner³, Pauline Bezivin-Frère⁴, Martin Löffler³, Anna S Sarvasmaa⁵, Jessica Massicotte-Marquez⁴, Eric Artiges⁶, Marie-Laure Paillère Martinot⁷, Irina Filippi⁴, Ruben Miranda⁸, Argyris Stringaris⁹, Betteke Maria van Noort¹⁰, Jani Penttilä¹¹, Yvonne Grimmer¹², Andreas Becker¹³, Tobias Banaschewski¹², Arun L W Bokde¹⁴, Sylvane Desrivières¹⁵, Juliane H Fröhner¹⁶, Hugh Garavan¹⁷, Antoine Grigis¹⁸, Penny A Gowland¹⁹, Andreas Heinz²⁰, Dimitri Papadopoulos Orfanos¹⁸, Luise Poustka²¹, Michael N Smolka¹⁶, Philip A Spechler¹⁷, Henrik Walter²⁰, Robert Whelan²², Gunter Schumann²³, Herta Flor²⁴, Jean-Luc Martinot⁴, Frauke Nees²⁵; IMAGEN Consortium

Affiliations

¹ Institute of Cognitive and Clinical Neuroscience, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Germany; AP-HP Sorbonne Université, Pitié-Salpêtrière Hospital, France. Electronic address: helene.vulser@aphp.fr.
² Institut des Maladies Neurodégénératives, UMR 5293, CNRS, CEA, Université de Bordeaux, Bordeaux, France.
³ Institute of Cognitive and Clinical Neuroscience, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Germany.
⁴ 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.
⁵ National Institute for Health and Welfare, Mental Health Unit, Helsinki, Finland, and the University of Helsinki and Helsinki University Hospital, Helsinki, Finland.
⁶ 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; EPS Barthélémy Durand, Etampes, France.
⁷ AP-HP Sorbonne Université, Pitié-Salpêtrière Hospital, France; 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.
⁸ AP-HP Sorbonne Université, Pitié-Salpêtrière Hospital, France.
⁹ National Institute of Mental Health, Bethesda, Maryland.
¹⁰ MSB Medical School Berlin, Hochschule für Gesundheit und Medizin, Siemens Villa, Berlin.
¹¹ Psychosocial Services Adolescent Outpatient Clinic, Lahti, Finland.
¹² Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.
¹³ University Medical Center, Göttingen.
¹⁴ School of Medicine and Trinity College Institute of Neuroscience, Trinity College Dublin, Dublin, Ireland.
¹⁵ Centre for Population Neuroscience and Precision Medicine (PONS), Institute of Psychiatry, Psychology & Neuroscience, SGDP Centre, King's College London, London, United Kingdom.
¹⁶ Technische Universität Dresden, Dresden, Germany.
¹⁷ University of Vermont, Burlington.
¹⁸ NeuroSpin, Commissariat à l'Energie Atomique, Université Paris-Saclay, Gif-sur-Yvette, France.
¹⁹ Sir Peter Mansfield Imaging Centre School of Physics and Astronomy, University of Nottingham, University Park, Nottingham, United Kingdom.
²⁰ Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany.
²¹ University Medical Centre Göttingen, Göttingen, Germany.
²² School of Psychology and Global Brain Health Institute, Trinity College Dublin, Ireland.
²³ 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.
²⁴ Institute of Cognitive and Clinical Neuroscience, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Germany; School of Social Sciences, University of Mannheim, Germany.
²⁵ Institute of Cognitive and Clinical Neuroscience, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Germany; 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.

PMID: 35714839
DOI: 10.1016/j.jaac.2022.06.003

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.

Keywords: MRI; adolescent; chronotype; gray matter; longitudinal.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Adolescent
Brain / diagnostic imaging
Catechol O-Methyltransferase* / genetics
Chronotype
Depression* / diagnostic imaging
Female
Humans
Male
Sleep
Surveys and Questionnaires
Young Adult

Substances

Catechol O-Methyltransferase

Abstract

Publication types

MeSH terms

Substances

Grants and funding