Irregular sleep habits, regional grey matter volumes, and psychological functioning in adolescents

the IMAGEN consortium; Winok Lapidaire; Anna S. Urrila; Eric Artiges; Ruben Miranda; Helene Vulser; Pauline Bezivin-Frere; Herve Lemaitre; Jani Penttilä; Tobias Banaschewski; Arun L.W. Bokde; Uli Bromberg; Christian Buchel; Patricia J. Conrod; Sylvane Desrivières; Vincent Frouin; Jurgen Gallinat; Hugh Garavan; Penny Gowland; Andreas Heinz; Bernd Ittermann; Dimitri Papadopoulos-Orfanos; Tomas Paus; Michael N. Smolka; Gunter Schumann; Marie Laure Paillere Martinot; Jean Luc Martinot; M. Fauth-Buhler; L. Poutska; F. Nees; Y. Grimmer; M. Struve; A. Strohle; V. Kappel; B. M. Van Noort; N. Bordas; Z. Bricaud; I. Filippi; A. Galinowski; F. Gollier-Briant; Vincent Menard; A. Cattrell; R. Goodman; A. Stringaris; C. Nymberg; L. Reed; B. Ittermann; R. Bruhl R; T. Hubner; K. Muller; U. Bromberg

doi:10.1371/journal.pone.0243720

Irregular sleep habits, regional grey matter volumes, and psychological functioning in adolescents

the IMAGEN consortium, Winok Lapidaire, Anna S. Urrila, Eric Artiges, Ruben Miranda, Helene Vulser, Pauline Bezivin-Frere, Herve Lemaitre, Jani Penttilä, Tobias Banaschewski, Arun L.W. Bokde, Uli Bromberg, Christian Buchel, Patricia J. Conrod, Sylvane Desrivières, Vincent Frouin, Jurgen Gallinat, Hugh Garavan, Penny Gowland, Andreas HeinzBernd Ittermann, Dimitri Papadopoulos-Orfanos, Tomas Paus, Michael N. Smolka, Gunter Schumann, Marie Laure Paillere Martinot, Jean Luc Martinot, M. Fauth-Buhler, L. Poutska, F. Nees, Y. Grimmer, M. Struve, A. Strohle, V. Kappel, B. M. Van Noort, N. Bordas, Z. Bricaud, I. Filippi, A. Galinowski, F. Gollier-Briant, Vincent Menard, A. Cattrell, R. Goodman, A. Stringaris, C. Nymberg, L. Reed, B. Ittermann, R. Bruhl R, T. Hubner, K. Muller, U. Bromberg

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Abstract

Changing sleep rhythms in adolescents often lead to sleep deficits and a delay in sleep timing between weekdays and weekends. The adolescent brain, and in particular the rapidly developing structures involved in emotional control, are vulnerable to external and internal factors. In our previous study in adolescents at age 14, we observed a strong relationship between weekend sleep schedules and regional medial prefrontal cortex grey matter volumes. Here, we aimed to assess whether this relationship remained in this group of adolescents of the general population at the age of 16 (n = 101; mean age 16.8 years; 55% girls). We further examined grey matter volumes in the hippocampi and the amygdalae, calculated with voxel-based morphometry. In addition, we investigated the relationships between sleep habits, assessed with self-reports, and regional grey matter volumes, and psychological functioning, assessed with the Strengths and Difficulties Questionnaire and tests on working memory and impulsivity. Later weekend wake-up times were associated with smaller grey matter volumes in the medial prefrontal cortex and the amygdalae, and greater weekend delays in wake-up time were associated with smaller grey matter volumes in the right hippocampus and amygdala. The medial prefrontal cortex region mediated the correlation between weekend wake up time and externalising symptoms. Paying attention to regular sleep habits during adolescence could act as a protective factor against the emergence of psychopathology via enabling favourable brain development.

Original language	English
Article number	e0243720
Journal	PLoS ONE
Volume	16
Issue number	2 February
DOIs	https://doi.org/10.1371/journal.pone.0243720
Publication status	Published - Feb 2021
Publication type	A1 Journal article-refereed

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journal.pone.0243720Final published version, 834 KBLicence: CC BY

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the IMAGEN consortium, Lapidaire, W., Urrila, A. S., Artiges, E., Miranda, R., Vulser, H., Bezivin-Frere, P., Lemaitre, H., Penttilä, J., Banaschewski, T., Bokde, A. L. W., Bromberg, U., Buchel, C., Conrod, P. J., Desrivières, S., Frouin, V., Gallinat, J., Garavan, H., Gowland, P., ... Bromberg, U. (2021). Irregular sleep habits, regional grey matter volumes, and psychological functioning in adolescents. PLoS ONE, 16(2 February), Article e0243720. https://doi.org/10.1371/journal.pone.0243720

@article{d6791c6948bc4a9d8f4ff0c5ccde0061,

title = "Irregular sleep habits, regional grey matter volumes, and psychological functioning in adolescents",

abstract = "Changing sleep rhythms in adolescents often lead to sleep deficits and a delay in sleep timing between weekdays and weekends. The adolescent brain, and in particular the rapidly developing structures involved in emotional control, are vulnerable to external and internal factors. In our previous study in adolescents at age 14, we observed a strong relationship between weekend sleep schedules and regional medial prefrontal cortex grey matter volumes. Here, we aimed to assess whether this relationship remained in this group of adolescents of the general population at the age of 16 (n = 101; mean age 16.8 years; 55% girls). We further examined grey matter volumes in the hippocampi and the amygdalae, calculated with voxel-based morphometry. In addition, we investigated the relationships between sleep habits, assessed with self-reports, and regional grey matter volumes, and psychological functioning, assessed with the Strengths and Difficulties Questionnaire and tests on working memory and impulsivity. Later weekend wake-up times were associated with smaller grey matter volumes in the medial prefrontal cortex and the amygdalae, and greater weekend delays in wake-up time were associated with smaller grey matter volumes in the right hippocampus and amygdala. The medial prefrontal cortex region mediated the correlation between weekend wake up time and externalising symptoms. Paying attention to regular sleep habits during adolescence could act as a protective factor against the emergence of psychopathology via enabling favourable brain development. ",

author = "{the IMAGEN consortium} and Winok Lapidaire and Urrila, {Anna S.} and Eric Artiges and Ruben Miranda and Helene Vulser and Pauline Bezivin-Frere and Herve Lemaitre and Jani Penttil{\"a} and Tobias Banaschewski and Bokde, {Arun L.W.} and Uli Bromberg and Christian Buchel and Conrod, {Patricia J.} and Sylvane Desrivi{\`e}res and Vincent Frouin and Jurgen Gallinat and Hugh Garavan and Penny Gowland and Andreas Heinz and Bernd Ittermann and Dimitri Papadopoulos-Orfanos and Tomas Paus and Smolka, {Michael N.} and Gunter Schumann and Martinot, {Marie Laure Paillere} and Martinot, {Jean Luc} and M. Fauth-Buhler and L. Poutska and F. Nees and Y. Grimmer and M. Struve and A. Strohle and V. Kappel and {Van Noort}, {B. M.} and N. Bordas and Z. Bricaud and I. Filippi and A. Galinowski and F. Gollier-Briant and Vincent Menard and A. Cattrell and R. Goodman and A. Stringaris and C. Nymberg and L. Reed and B. Ittermann and {Bruhl R}, R. and T. Hubner and K. Muller and U. Bromberg",

note = "Funding Information: This study was funded by the European Union-funded FP6 Integrated Project IMAGEN (LSHM-CT-2007-037286), agence nationale de la recherche (ANR-12-SAMA-0004 and ANR-19- CE37-0017-03), Eranet (ANR-18-NEUR00002-01- ADORe and AF12-NEUR0008-01 - WM2NA), Fondation pour la Recherche M?dicale (DPA20140629802), Mission Interminist?rielle de Lutte Contre les Drogues et les Conduites Addictives, and Fondation de France (00081242) in the form of grants awarded to JLM. This study was also funded by the F?d?ration pour la Recherche sur le Cerveau in the form of a grant awarded to MLP and JLM. This study was also funded by the Academy of Finland (276612), Emil Aaltosen S??ti? Foundation, and Jalmari ja Rauha Ahokkaan S??ti? Foundation in the form of grants awarded to ASU and in the form of grants from IDEX Paris Saclay and INSERM - APHP 2010 interface grant awarded to HV. Publisher Copyright: {\textcopyright} 2021 Lapidaire et al.",

year = "2021",

month = feb,

doi = "10.1371/journal.pone.0243720",

language = "English",

volume = "16",

number = "2 February",

}

the IMAGEN consortium, Lapidaire, W, Urrila, AS, Artiges, E, Miranda, R, Vulser, H, Bezivin-Frere, P, Lemaitre, H, Penttilä, J, Banaschewski, T, Bokde, ALW, Bromberg, U, Buchel, C, Conrod, PJ, Desrivières, S, Frouin, V, Gallinat, J, Garavan, H, Gowland, P, Heinz, A, Ittermann, B, Papadopoulos-Orfanos, D, Paus, T, Smolka, MN, Schumann, G, Martinot, MLP, Martinot, JL, Fauth-Buhler, M, Poutska, L, Nees, F, Grimmer, Y, Struve, M, Strohle, A, Kappel, V, Van Noort, BM, Bordas, N, Bricaud, Z, Filippi, I, Galinowski, A, Gollier-Briant, F, Menard, V, Cattrell, A, Goodman, R, Stringaris, A, Nymberg, C, Reed, L, Ittermann, B, Bruhl R, R, Hubner, T, Muller, K & Bromberg, U 2021, 'Irregular sleep habits, regional grey matter volumes, and psychological functioning in adolescents', PLoS ONE, vol. 16, no. 2 February, e0243720. https://doi.org/10.1371/journal.pone.0243720

TY - JOUR

T1 - Irregular sleep habits, regional grey matter volumes, and psychological functioning in adolescents

AU - the IMAGEN consortium

AU - Lapidaire, Winok

AU - Urrila, Anna S.

AU - Artiges, Eric

AU - Miranda, Ruben

AU - Vulser, Helene

AU - Bezivin-Frere, Pauline

AU - Lemaitre, Herve

AU - Penttilä, Jani

AU - Banaschewski, Tobias

AU - Bokde, Arun L.W.

AU - Bromberg, Uli

AU - Buchel, Christian

AU - Conrod, Patricia J.

AU - Desrivières, Sylvane

AU - Frouin, Vincent

AU - Gallinat, Jurgen

AU - Garavan, Hugh

AU - Gowland, Penny

AU - Heinz, Andreas

AU - Ittermann, Bernd

AU - Papadopoulos-Orfanos, Dimitri

AU - Paus, Tomas

AU - Smolka, Michael N.

AU - Schumann, Gunter

AU - Martinot, Marie Laure Paillere

AU - Martinot, Jean Luc

AU - Fauth-Buhler, M.

AU - Poutska, L.

AU - Nees, F.

AU - Grimmer, Y.

AU - Struve, M.

AU - Strohle, A.

AU - Kappel, V.

AU - Van Noort, B. M.

AU - Bordas, N.

AU - Bricaud, Z.

AU - Filippi, I.

AU - Galinowski, A.

AU - Gollier-Briant, F.

AU - Menard, Vincent

AU - Cattrell, A.

AU - Goodman, R.

AU - Stringaris, A.

AU - Nymberg, C.

AU - Reed, L.

AU - Ittermann, B.

AU - Bruhl R, R.

AU - Hubner, T.

AU - Muller, K.

AU - Bromberg, U.

N1 - Funding Information: This study was funded by the European Union-funded FP6 Integrated Project IMAGEN (LSHM-CT-2007-037286), agence nationale de la recherche (ANR-12-SAMA-0004 and ANR-19- CE37-0017-03), Eranet (ANR-18-NEUR00002-01- ADORe and AF12-NEUR0008-01 - WM2NA), Fondation pour la Recherche M?dicale (DPA20140629802), Mission Interminist?rielle de Lutte Contre les Drogues et les Conduites Addictives, and Fondation de France (00081242) in the form of grants awarded to JLM. This study was also funded by the F?d?ration pour la Recherche sur le Cerveau in the form of a grant awarded to MLP and JLM. This study was also funded by the Academy of Finland (276612), Emil Aaltosen S??ti? Foundation, and Jalmari ja Rauha Ahokkaan S??ti? Foundation in the form of grants awarded to ASU and in the form of grants from IDEX Paris Saclay and INSERM - APHP 2010 interface grant awarded to HV. Publisher Copyright: © 2021 Lapidaire et al.

PY - 2021/2

Y1 - 2021/2

N2 - Changing sleep rhythms in adolescents often lead to sleep deficits and a delay in sleep timing between weekdays and weekends. The adolescent brain, and in particular the rapidly developing structures involved in emotional control, are vulnerable to external and internal factors. In our previous study in adolescents at age 14, we observed a strong relationship between weekend sleep schedules and regional medial prefrontal cortex grey matter volumes. Here, we aimed to assess whether this relationship remained in this group of adolescents of the general population at the age of 16 (n = 101; mean age 16.8 years; 55% girls). We further examined grey matter volumes in the hippocampi and the amygdalae, calculated with voxel-based morphometry. In addition, we investigated the relationships between sleep habits, assessed with self-reports, and regional grey matter volumes, and psychological functioning, assessed with the Strengths and Difficulties Questionnaire and tests on working memory and impulsivity. Later weekend wake-up times were associated with smaller grey matter volumes in the medial prefrontal cortex and the amygdalae, and greater weekend delays in wake-up time were associated with smaller grey matter volumes in the right hippocampus and amygdala. The medial prefrontal cortex region mediated the correlation between weekend wake up time and externalising symptoms. Paying attention to regular sleep habits during adolescence could act as a protective factor against the emergence of psychopathology via enabling favourable brain development.

AB - Changing sleep rhythms in adolescents often lead to sleep deficits and a delay in sleep timing between weekdays and weekends. The adolescent brain, and in particular the rapidly developing structures involved in emotional control, are vulnerable to external and internal factors. In our previous study in adolescents at age 14, we observed a strong relationship between weekend sleep schedules and regional medial prefrontal cortex grey matter volumes. Here, we aimed to assess whether this relationship remained in this group of adolescents of the general population at the age of 16 (n = 101; mean age 16.8 years; 55% girls). We further examined grey matter volumes in the hippocampi and the amygdalae, calculated with voxel-based morphometry. In addition, we investigated the relationships between sleep habits, assessed with self-reports, and regional grey matter volumes, and psychological functioning, assessed with the Strengths and Difficulties Questionnaire and tests on working memory and impulsivity. Later weekend wake-up times were associated with smaller grey matter volumes in the medial prefrontal cortex and the amygdalae, and greater weekend delays in wake-up time were associated with smaller grey matter volumes in the right hippocampus and amygdala. The medial prefrontal cortex region mediated the correlation between weekend wake up time and externalising symptoms. Paying attention to regular sleep habits during adolescence could act as a protective factor against the emergence of psychopathology via enabling favourable brain development.

U2 - 10.1371/journal.pone.0243720

DO - 10.1371/journal.pone.0243720

M3 - Article

C2 - 33566829

AN - SCOPUS:85101418009

SN - 1932-6203

VL - 16

JO - PLoS ONE

JF - PLoS ONE

IS - 2 February

M1 - e0243720

ER -

Irregular sleep habits, regional grey matter volumes, and psychological functioning in adolescents

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