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The mediating role of cortical thickness and gray matter volume on sleep slow-wave activity during adolescence

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Abstract

During the course of adolescence, reductions occur in cortical thickness and gray matter (GM) volume, along with a 65% reduction in slow-wave (delta) activity during sleep (SWA) but empirical data linking these structural brain and functional sleep differences, is lacking. Here, we investigated specifically whether age-related differences in cortical thickness and GM volume and cortical thickness accounted for the typical age-related difference in slow-wave (delta) activity (SWA) during sleep. 132 healthy participants (age 12–21 years) from the National Consortium on Alcohol and NeuroDevelopment in Adolescence study were included in this cross-sectional analysis of baseline polysomnographic, electroencephalographic, and magnetic resonance imaging data. By applying mediation models, we identified a large, direct effect of age on SWA in adolescents, which explained 45% of the variance in ultra-SWA (0.3–1 Hz) and 52% of the variance in delta-SWA (1 to <4 Hz), where SWA was lower in older adolescents, as has been reported previously. In addition, we provide evidence that the structure of several, predominantly frontal, and parietal brain regions, partially mediated this direct age effect, models including measures of brain structure explained an additional 3–9% of the variance in ultra-SWA and 4–5% of the variance in delta-SWA, with no differences between sexes. Replacing age with pubertal status in models produced similar results. As reductions in GM volume and cortical thickness likely indicate synaptic pruning and myelination, these results suggest that diminished SWA in older, more mature adolescents may largely be driven by such processes within a number of frontal and parietal brain regions.

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Acknowledgements

The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. We thank our lab manager, Stephanie Claudatos, and research assistants, David Dresser, David Sugarbaker, Justin Greco, Sarah Inkelis, Lena Kardos, Devika Nair, and Leonardo Rosas, for their effort in collecting data for this project, and all research participants.

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Authors and Affiliations

  1. Centre for Health Sciences, SRI International, 333 Ravenswood Avenue, Menlo Park, CA, 94025, USA

    Aimée Goldstone, Adrian R. Willoughby, Massimiliano de Zambotti, Dongjin Kwon, Kilian M. Pohl, Adolf Pfefferbaum, Eva M. Müller-Oehring, Devin E. Prouty, Ian M. Colrain & Fiona C. Baker

  2. University of Pittsburgh School of Medicine, Pittsburgh, PA, USA

    Peter L. Franzen, Brant P. Hasler & Duncan B. Clark

  3. Department of Psychiatry and Behavioral Sciences, Stanford University School of Medicine, Stanford, CA, USA

    Dongjin Kwon, Kilian M. Pohl, Adolf Pfefferbaum, Edith V. Sullivan & Eva M. Müller-Oehring

  4. Melbourne School of Psychological Sciences, University of Melbourne, Parkville, VIC, Australia

    Ian M. Colrain

  5. Brain Function Research Group, School of Physiology, University of Witwatersrand, Johannesburg, South Africa

    Fiona C. Baker

Authors
  1. Aimée Goldstone
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  2. Adrian R. Willoughby
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  3. Massimiliano de Zambotti
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  4. Peter L. Franzen
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  5. Dongjin Kwon
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  6. Kilian M. Pohl
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  7. Adolf Pfefferbaum
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  8. Edith V. Sullivan
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  9. Eva M. Müller-Oehring
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  10. Devin E. Prouty
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  11. Brant P. Hasler
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  12. Duncan B. Clark
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  13. Ian M. Colrain
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  14. Fiona C. Baker
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Corresponding author

Correspondence to Fiona C. Baker.

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Conflict of interest

FCB and MdZ have received research grants from Fitbit Inc., Ebb Inc., and International Flavors and Fragrances Inc.

Financial statement

This study was supported by the National Consortium on Alcohol and NeuroDevelopment in Adolescence (NCANDA); grants: AA021690 (DBC), AA021697 (AP + KMP), AA021697-04S1 (KMP), AA021696 (IMC + FCB) and AA021695 (NCANDA Admin).

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Goldstone, A., Willoughby, A.R., de Zambotti, M. et al. The mediating role of cortical thickness and gray matter volume on sleep slow-wave activity during adolescence. Brain Struct Funct 223, 669–685 (2018). https://doi.org/10.1007/s00429-017-1509-9

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  • DOI: https://doi.org/10.1007/s00429-017-1509-9

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