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Sleep spindle characteristics and sleep architecture are associated with learning of executive functions in school-age children

  • Marije C.M. Vermeulen
  • , Kristiaan B. Van der Heijden
  • , Hanna Swaab
  • , Eus J.W. Van Someren*
  • *Corresponding author for this work

Research output: Contribution to JournalArticleAcademicpeer-review

Abstract

The macro- and microstructural characteristics of sleep electroencephalography have been associated with several aspects of executive functioning. However, only a few studies have addressed the association of sleep characteristics with the learning involved in the acquisition of executive functions, and no study has investigated this for planning and problem-solving skills in the developing brain of children. The present study examined whether children's sleep stages and microstructural sleep characteristics are associated with performance improvement over repeated assessments of the Tower of Hanoi task, which requires integrated planning and problem-solving skills. Thirty children (11 boys, mean age 10.7 years, SD = 0.8) performed computerized parallel versions of the Tower of Hanoi three times across 2 days, including a night with polysomnographically assessed sleep. Pearson correlations were used to evaluate the associations of Tower of Hanoi solution time improvements across repeated assessments with sleep stages (% of total sleep time), slow-wave activity, and fast and slow spindle features. The results indicated a stronger performance improvement across wake in children with more Stage N2 sleep and less slow-wave sleep. Stronger improvements across sleep were present in children in whom slow spindles were more dense, and in children in whom fast spindles were less dense, of shorter duration and had less power. The findings indicate that specific sleep electroencephalography signatures reflect the ability of the developing brain to acquire and improve on integrated planning and problem-solving skills.

Original languageEnglish
Article numbere12779
Pages (from-to)1-10
Number of pages10
JournalJournal of Sleep Research
Volume28
Issue number1
Early online date18 Oct 2018
DOIs
Publication statusPublished - Feb 2019

Funding

This work was supported by the Netherlands Organization of Scientific Research (NWO), The Hague: National Initiative Brain & Cognition Research Program “Innovative Learning Materials and Methods” under Grant 056‐32‐013; and VICI Innovation Grant 453‐07‐001. Data were obtained during “The Great Sleep Experiment” event, organized and sponsored by Netherlands Organization for Scientific Research (NWO) and the Netherlands Institute for Neuroscience. The event was also sponsored by Beter Bed, Medcare, IBM, Amstel Botel, Cambridge Neurotechnology, J&J Pharmaceutical Research and Development, Nederlandse Vereniging voor Slaap‐Waak Onder-zoek, Onderzoeksschool Neurowetenschappen Amsterdam, Philips, SEIN Zwolle, Gelre ziekenhuizen Zutphen, OLVG Amsterdam, Sint Lucas Andreas Ziekenhuis Amsterdam, Spaarne Ziekenhuis Hoofd-dorp, and Zaans Medisch Centrum Zaandam. The authors want to thank all participating children and their teachers, and all 22 volunteering lab technicians and the research staff who made “The Great Sleep Experiment” possible. Finally, the authors would like to thank Prof. R. Huber for his kind permission to use and adapt his automated spindle detection scripts, Prof. M. Massimini for the slow‐ wave script, and Dr R.G. Astill, Dr G. Piantoni and F. van Schalkwijk MSc for their assistance in preparing the data. This work was supported by the Netherlands Organization of Scientific Research (NWO), The Hague: National Initiative Brain & Cognition Research Program ?Innovative Learning Materials and Methods? under Grant 056-32-013; and VICI Innovation Grant 453-07-001. Data were obtained during ?The Great Sleep Experiment? event, organized and sponsored by Netherlands Organization for Scientific Research (NWO) and the Netherlands Institute for Neuroscience. The event was also sponsored by Beter Bed, Medcare, IBM, Amstel Botel, Cambridge Neurotechnology, J&J Pharmaceutical Research and Development, Nederlandse Vereniging voor Slaap-Waak Onderzoek, Onderzoeksschool Neurowetenschappen Amsterdam, Philips, SEIN Zwolle, Gelre ziekenhuizen Zutphen, OLVG Amsterdam, Sint Lucas Andreas Ziekenhuis Amsterdam, Spaarne Ziekenhuis Hoofddorp, and Zaans Medisch Centrum Zaandam. The authors want to thank all participating children and their teachers, and all 22 volunteering lab technicians and the research staff who made ?The Great Sleep Experiment? possible. Finally, the authors would like to thank Prof. R. Huber for his kind permission to use and adapt his automated spindle detection scripts, Prof. M. Massimini for the slow-wave script, and Dr R.G. Astill, Dr G. Piantoni and F. van Schalkwijk MSc for their assistance in preparing the data.

FundersFunder number
Amstel Botel
J&J Pharmaceutical Research and Development
National Initiative Brain & Cognition Research Program056‐32‐013, 453‐07‐001
National Initiative Brain & Cognition Research Program ?
Nederlandse Vereniging voor Slaap-Waak Onderzoek
Netherlands Institute for Neuroscience
Netherlands Organization for Scientific Research
Netherlands Organization of Scientific Research
Onderzoeksschool Neurowetenschappen Amsterdam
Zaans Medisch Centrum Zaandam
International Business Machines Corporation
Nederlandse Organisatie voor Wetenschappelijk Onderzoek

    Keywords

    • children
    • executive functioning
    • slow-wave sleep
    • spindles
    • Tower of Hanoi

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