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Sleep spindle maturity promotes slow oscillation-spindle coupling across child and adolescent development

The synchronization of canonical fast sleep spindle activity (12.5–16 Hz, adult-like) precisely during the slow oscillation (0.5–1 Hz) up peak is considered an essential feature of adult non-rapid eye movement sleep. However, there is little knowledge on how this well-known coalescence between slow...

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Autores principales: Joechner, Ann-Kathrin, Hahn, Michael A, Gruber, Georg, Hoedlmoser, Kerstin, Werkle-Bergner, Markus
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10672804/
https://www.ncbi.nlm.nih.gov/pubmed/37999945
http://dx.doi.org/10.7554/eLife.83565
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author Joechner, Ann-Kathrin
Hahn, Michael A
Gruber, Georg
Hoedlmoser, Kerstin
Werkle-Bergner, Markus
author_facet Joechner, Ann-Kathrin
Hahn, Michael A
Gruber, Georg
Hoedlmoser, Kerstin
Werkle-Bergner, Markus
author_sort Joechner, Ann-Kathrin
collection PubMed
description The synchronization of canonical fast sleep spindle activity (12.5–16 Hz, adult-like) precisely during the slow oscillation (0.5–1 Hz) up peak is considered an essential feature of adult non-rapid eye movement sleep. However, there is little knowledge on how this well-known coalescence between slow oscillations and sleep spindles develops. Leveraging individualized detection of single events, we first provide a detailed cross-sectional characterization of age-specific patterns of slow and fast sleep spindles, slow oscillations, and their coupling in children and adolescents aged 5–6, 8–11, and 14–18 years, and an adult sample of 20- to 26-year-olds. Critically, based on this, we then investigated how spindle and slow oscillation maturity substantiate age-related differences in their precise orchestration. While the predominant type of fast spindles was development-specific in that it was still nested in a frequency range below the canonical fast spindle range for the majority of children, the well-known slow oscillation-spindle coupling pattern was evident for sleep spindles in the adult-like canonical fast spindle range in all four age groups—but notably less precise in children. To corroborate these findings, we linked personalized measures of fast spindle maturity, which indicate the similarity between the prevailing development-specific and adult-like canonical fast spindles, and slow oscillation maturity, which reflects the extent to which slow oscillations show frontal dominance, with individual slow oscillation-spindle coupling patterns. Importantly, we found that fast spindle maturity was uniquely associated with enhanced slow oscillation-spindle coupling strength and temporal precision across the four age groups. Taken together, our results suggest that the increasing ability to generate adult-like canonical fast sleep spindles actuates precise slow oscillation-spindle coupling patterns from childhood through adolescence and into young adulthood.
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spelling pubmed-106728042023-11-24 Sleep spindle maturity promotes slow oscillation-spindle coupling across child and adolescent development Joechner, Ann-Kathrin Hahn, Michael A Gruber, Georg Hoedlmoser, Kerstin Werkle-Bergner, Markus eLife Neuroscience The synchronization of canonical fast sleep spindle activity (12.5–16 Hz, adult-like) precisely during the slow oscillation (0.5–1 Hz) up peak is considered an essential feature of adult non-rapid eye movement sleep. However, there is little knowledge on how this well-known coalescence between slow oscillations and sleep spindles develops. Leveraging individualized detection of single events, we first provide a detailed cross-sectional characterization of age-specific patterns of slow and fast sleep spindles, slow oscillations, and their coupling in children and adolescents aged 5–6, 8–11, and 14–18 years, and an adult sample of 20- to 26-year-olds. Critically, based on this, we then investigated how spindle and slow oscillation maturity substantiate age-related differences in their precise orchestration. While the predominant type of fast spindles was development-specific in that it was still nested in a frequency range below the canonical fast spindle range for the majority of children, the well-known slow oscillation-spindle coupling pattern was evident for sleep spindles in the adult-like canonical fast spindle range in all four age groups—but notably less precise in children. To corroborate these findings, we linked personalized measures of fast spindle maturity, which indicate the similarity between the prevailing development-specific and adult-like canonical fast spindles, and slow oscillation maturity, which reflects the extent to which slow oscillations show frontal dominance, with individual slow oscillation-spindle coupling patterns. Importantly, we found that fast spindle maturity was uniquely associated with enhanced slow oscillation-spindle coupling strength and temporal precision across the four age groups. Taken together, our results suggest that the increasing ability to generate adult-like canonical fast sleep spindles actuates precise slow oscillation-spindle coupling patterns from childhood through adolescence and into young adulthood. eLife Sciences Publications, Ltd 2023-11-24 /pmc/articles/PMC10672804/ /pubmed/37999945 http://dx.doi.org/10.7554/eLife.83565 Text en © 2023, Joechner et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Neuroscience
Joechner, Ann-Kathrin
Hahn, Michael A
Gruber, Georg
Hoedlmoser, Kerstin
Werkle-Bergner, Markus
Sleep spindle maturity promotes slow oscillation-spindle coupling across child and adolescent development
title Sleep spindle maturity promotes slow oscillation-spindle coupling across child and adolescent development
title_full Sleep spindle maturity promotes slow oscillation-spindle coupling across child and adolescent development
title_fullStr Sleep spindle maturity promotes slow oscillation-spindle coupling across child and adolescent development
title_full_unstemmed Sleep spindle maturity promotes slow oscillation-spindle coupling across child and adolescent development
title_short Sleep spindle maturity promotes slow oscillation-spindle coupling across child and adolescent development
title_sort sleep spindle maturity promotes slow oscillation-spindle coupling across child and adolescent development
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10672804/
https://www.ncbi.nlm.nih.gov/pubmed/37999945
http://dx.doi.org/10.7554/eLife.83565
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