Longitudinal associations between adolescent catch-up sleep, white-matter maturation and internalizing problems

Stella Guldner; Anna S Sarvasmaa; Hervé Lemaître; Jessica Massicotte; Hélène Vulser; Ruben Miranda; Pauline Bezivin-Frère; Irina Filippi; Jani Penttilä; Tobias Banaschewski; Gareth J Barker; Arun Lw Bokde; Uli Bromberg; Christian Büchel; Patricia J Conrod; Sylvane Desrivières; Herta Flor; Vincent Frouin; Jürgen Gallinat; Hugh Garavan; Penny Gowland; Andreas Heinz; Frauke Nees; Dimitri Papadopoulos-Orfanos; Michael N Smolka; Gunter Schumann; Eric Artiges; Marie-Laure Paillère Martinot; Jean-Luc Martinot

doi:10.1016/j.dcn.2022.101193

Longitudinal associations between adolescent catch-up sleep, white-matter maturation and internalizing problems

Dev Cogn Neurosci. 2023 Feb:59:101193. doi: 10.1016/j.dcn.2022.101193. Epub 2022 Dec 29.

Authors

Stella Guldner¹, Anna S Sarvasmaa², Hervé Lemaître³, Jessica Massicotte⁴, Hélène Vulser⁴, Ruben Miranda⁴, Pauline Bezivin-Frère⁴, Irina Filippi⁴, Jani Penttilä⁵, Tobias Banaschewski⁶, Gareth J Barker⁷, Arun Lw Bokde⁸, Uli Bromberg⁹, Christian Büchel⁹, Patricia J Conrod¹⁰, Sylvane Desrivières¹¹, Herta Flor¹², Vincent Frouin¹³, Jürgen Gallinat¹⁴, Hugh Garavan¹⁵, Penny Gowland¹⁶, Andreas Heinz¹⁷, Frauke Nees¹⁸, Dimitri Papadopoulos-Orfanos¹³, Michael N Smolka¹⁹, Gunter Schumann²⁰, Eric Artiges²¹, Marie-Laure Paillère Martinot²², Jean-Luc Martinot²³

Affiliations

¹ Université Paris-Saclay; Institut National de la Santé et de la Recherche Médicale, INSERM U1299 "Trajectoires développementales Psychiatrie", Ecole Normale Supérieure Paris-Saclay, CNRS UMR 9010, Université Paris Cité, Centre Borelli, Gif sur Yvette, France; Department of Cognitive and Clinical Neuroscience, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany; Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.
² Université Paris-Saclay; Institut National de la Santé et de la Recherche Médicale, INSERM U1299 "Trajectoires développementales Psychiatrie", Ecole Normale Supérieure Paris-Saclay, CNRS UMR 9010, Université Paris Cité, Centre Borelli, Gif sur Yvette, France; National Institute for Health and Welfare, Department of Public Health Solutions, Mental Health Unit, Helsinki, Finland; Finnish Student Health Service, Helsinki, Finland.
³ Université Paris-Saclay; Institut National de la Santé et de la Recherche Médicale, INSERM U1299 "Trajectoires développementales Psychiatrie", Ecole Normale Supérieure Paris-Saclay, CNRS UMR 9010, Université Paris Cité, Centre Borelli, Gif sur Yvette, France; Institut des Maladies Neurodégénératives, UMR 5293, CNRS, CEA, Université de Bordeaux, 33076 Bordeaux, France.
⁴ Université Paris-Saclay; Institut National de la Santé et de la Recherche Médicale, INSERM U1299 "Trajectoires développementales Psychiatrie", Ecole Normale Supérieure Paris-Saclay, CNRS UMR 9010, Université Paris Cité, Centre Borelli, Gif sur Yvette, France.
⁵ Université Paris-Saclay; Institut National de la Santé et de la Recherche Médicale, INSERM U1299 "Trajectoires développementales Psychiatrie", Ecole Normale Supérieure Paris-Saclay, CNRS UMR 9010, Université Paris Cité, Centre Borelli, Gif sur Yvette, France; Department of Social and Health Care, Psychosocial Services Adolescent Outpatient Clinic, Lahti, Finland.
⁶ Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.
⁷ Department of Neuroimaging, Institute of Psychiatry, Psychology & Neuroscience, King's College London, United Kingdom.
⁸ Department of Neuroimaging, Institute of Psychiatry, Psychology & Neuroscience, King's College London, United Kingdom; Discipline of Psychiatry, School of Medicine and Trinity College Institute of Neuroscience, Trinity College, Dublin, Ireland.
⁹ Department of Systems Neuroscience, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.
¹⁰ Department of Psychiatry, CHU Sainte-Justine Research Center, University of Montreal, Montreal, QC, Canada.
¹¹ Institute of Psychiatry, Psychology & Neuroscience, King's College London, London, United Kingdom.
¹² Department of Cognitive and Clinical Neuroscience, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.
¹³ Neurospin, Commissariat à l'Energie Atomique et aux Energies Alternatives, Saclay, France.
¹⁴ University Medical Centre Hamburg-Eppendorf, Clinic and Policlinic for Psychiatry and Psychotherapy; Hamburg, Germany.
¹⁵ Departments of Psychiatry and Psychology, University of Vermont, 05405 Burlington, Vermont, USA.
¹⁶ Sir Peter Mansfield Imaging Centre, University of Nottingham, United Kingdom.
¹⁷ Department of Psychiatry and Psychotherapy CCM, Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany.
¹⁸ Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany; Institute of Medical Psychology and Medical Sociology, University Medical Center Schleswig Holstein, Kiel University, Kiel, Germany.
¹⁹ Department of Psychiatry and Neuroimaging Center, Technische Universität Dresden, Dresden, Germany.
²⁰ Centre for Population Neuroscience and Stratified Medicine (PONS), ISTBI, Fudan University Shanghai; and Dept. of Psychiatry and Neuroscience, Charité University Medicine, Berlin, Germany.
²¹ Université Paris-Saclay; Institut National de la Santé et de la Recherche Médicale, INSERM U1299 "Trajectoires développementales Psychiatrie", Ecole Normale Supérieure Paris-Saclay, CNRS UMR 9010, Université Paris Cité, Centre Borelli, Gif sur Yvette, France; EPS Barthelemy Durand, Etampes, France.
²² Université Paris-Saclay; Institut National de la Santé et de la Recherche Médicale, INSERM U1299 "Trajectoires développementales Psychiatrie", Ecole Normale Supérieure Paris-Saclay, CNRS UMR 9010, Université Paris Cité, Centre Borelli, Gif sur Yvette, France; AP-HP. Sorbonne Université, Department of Child and Adolescent Psychiatry, Pitié-Salpêtrière Hospital, Paris, France.
²³ Université Paris-Saclay; Institut National de la Santé et de la Recherche Médicale, INSERM U1299 "Trajectoires développementales Psychiatrie", Ecole Normale Supérieure Paris-Saclay, CNRS UMR 9010, Université Paris Cité, Centre Borelli, Gif sur Yvette, France. Electronic address: [email protected].

Abstract

Sleep is an important contributor for neural maturation and emotion regulation during adolescence, with long-term effects on a range of white matter tracts implicated in affective processing in at-risk populations. We investigated the effects of adolescent sleep patterns on longitudinal changes in white matter development and whether this is related to the emergence of emotional (internalizing) problems. Sleep patterns and internalizing problems were assessed using self-report questionnaires in adolescents recruited in the general population followed up from age 14-19 years (N = 111 White matter structure was measured using diffusion tensor imaging (DTI) and estimated using fractional anisotropy (FA). We found that longitudinal increases in time in bed (TIB) on weekends and increases in TIB-variability between weekdays to weekend, were associated with an increase in FA in various interhemispheric and cortico-striatal tracts. Extracted FA values from left superior longitudinal fasciculus mediated the relationship between increases in TIB on weekends and a decrease in internalizing problems. These results imply that while insufficient sleep might have potentially harmful effects on long-term white matter development and internalizing problems, longer sleep duration on weekends (catch-up sleep) might be a natural counteractive and protective strategy.

Keywords: Adolescence; Adolescents; Anxiety; Brain Development; Cohort; DTI; Depression; Internalized symptoms; Internalizing; Longitudinal; MRI; Prevention; Sleep; White Matter.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't

MeSH terms

Adolescent
Adult
Anisotropy
Brain
Diffusion Tensor Imaging / methods
Emotions
Humans
Sleep
Sleep Deprivation
White Matter* / physiology
Young Adult

Abstract

Publication types

MeSH terms

Grants and funding