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

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

Stella Guldner  1 , Anna S Sarvasmaa  2 , Hervé Lemaître  3 , Jessica Massicotte  4 , Hélène Vulser  4 , Ruben Miranda  4 , Pauline Bezivin-Frère  4 , Irina Filippi  4 , Jani Penttilä  5 , Tobias Banaschewski  6 , Gareth J Barker  7 , Arun Lw Bokde  8 , Uli Bromberg  9 , Christian Büchel  9 , Patricia J Conrod  10 , Sylvane Desrivières  11 , Herta Flor  12 , Vincent Frouin  13 , Jürgen Gallinat  14 , Hugh Garavan  15 , Penny Gowland  16 , Andreas Heinz  17 , Frauke Nees  18 , Dimitri Papadopoulos-Orfanos  13 , Michael N Smolka  19 , Gunter Schumann  20 , Eric Artiges  21 , Marie-Laure Paillère Martinot  22 , Jean-Luc Martinot  23
Affiliations

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

Stella Guldner et al. Dev Cogn Neurosci. 2023 Feb.

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.

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Conflict of interest statement

Declaration of Competing Interest The authors declare the following financial interests/personal relationships which may be considered as potential competing interests: Dr Banaschewski served in an advisory or consultancy role for ADHS digital, Infectopharm, Lundbeck, Medice, Neurim Pharmaceuticals, Oberberg GmbH, Roche, and Takeda. He received conference support or speaker’s fee by Medice and Takeda. He has been involved in clinical trials conducted by Shire & Viforpharma. He received royalties from Hogrefe, Kohlhammer, CIP Medien, Oxford University Press. He has been involved in clinical trials conducted by Shire & Viforpharma. Dr Barker has received honoraria from General Electric Healthcare for teaching on scanner programming courses. Dr Barker has received honoraria from General Electric Healthcare for teaching on scanner programming courses. Dr Gowland has received a research grant from Lyndra and an honorarium paid to her employer from GlaxoSmithKline. The present work is unrelated to the above grants and relationships. Competing Interests Dr Banaschewski served in an advisory or consultancy role for ADHS digital, Infectopharm, Lundbeck, Medice, Neurim Pharmaceuticals, Oberberg GmbH, Roche, and Takeda. He received conference support or speaker’s fee by Medice and Takeda. He has been involved in clinical trials conducted by Shire & Viforpharma. He received royalties from Hogrefe, Kohlhammer, CIP Medien, Oxford University Press. He has been involved in clinical trials conducted by Shire & Viforpharma. Dr Barker has received honoraria from General Electric Healthcare for teaching on scanner programming courses. Dr Barker has received honoraria from General Electric Healthcare for teaching on scanner programming courses. Dr Gowland has received a research grant from Lyndra and an honorarium paid to her employer from GlaxoSmithKline. The present work is unrelated to the above grants and relationships.

Figures

Fig. 1
Fig. 1
Illustration of regions showing significant correlations (in blue) between ∆TIB-variability between weekends and weekdays (in minutes) and ∆ FA. The longitudinal ∆TIB-variability shown in this figure is calculated by subtracting TIB-variability at baseline from TIB-variability at follow-up. Thus, a positive value of Δ TIB-variability indicates greater TIB-variability (more catch-up sleep) at Follow-up compared to Baseline, i.e. an increase in TIB-variability. Scatterplots showing visual depiction of this relationship in left superior longitudinal fasciculus (l-SLF; sagittal view), body of the corpus callosum (CC; sagittal view) and left inferior fronto-occipital fasciculus (l-IFOF; coronal view). Note. * p < .05; * * p < .01; * ** p < .001. Significant results are displayed at p < 0.05 FEW corrected on study specific FA skeleton and mean FA mask (in green) using tbss_fill. Images are presented in radiological convention. MNI coordinates.
Fig. 2
Fig. 2
Regions of FA and illustration of significant correlations (in blue) between ∆ TIB on weekends (in minutes) and ∆ FA. The longitudinal ∆TIB on weekends shown in this figure is calculated by subtracting TIB on weekends at baseline from TIB on weekends at follow-up. Negative values indicate less time in bed on weekends from baseline to follow-up, whereas positive numbers indicate increased time in bed on weekends from baseline to follow-up. Scatterplots showing visual depiction of this relation in forceps major (FMaj), left inferior fronto-occipital fasciculus (l-IFOF) and left inferior longitudinal fasciculus (l-ILF). Note. *p < .05; * *p < .01; * ** p < .001. Significant results are displayed at p < 0.05 FWE corrected on study specific FA skeleton and mean FA mask (in green) using tbss_fill. Images are presented in radiological convention. MNI coordinates.
Fig. 3
Fig. 3
Results of mediation analysis. The association between ∆TIB-weekends and ∆internalizing problems was mediated by the effects of 5-year changes in sleep behaviour on white matter development in left Superior Longitudinal Fasciculus (l-SLF). * p < .05; * *p < .01, * **p < .001; ns, not significant; ∆, longitudinal difference (Follow-Up measurement – Baseline measurement).
See this image and copyright information in PMC

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