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...
| Main Authors: | , , , , |
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| Format: | Article |
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eLife Sciences Publications Ltd
2023-11-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/83565 |
| _version_ | 1797456874131423232 |
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| author | Ann-Kathrin Joechner Michael A Hahn Georg Gruber Kerstin Hoedlmoser Markus Werkle-Bergner |
| author_facet | Ann-Kathrin Joechner Michael A Hahn Georg Gruber Kerstin Hoedlmoser Markus Werkle-Bergner |
| author_sort | Ann-Kathrin Joechner |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-03-09T16:14:03Z |
| format | Article |
| id | doaj.art-93a5c021808f40f488695ae0349d180f |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-03-09T16:14:03Z |
| publishDate | 2023-11-01 |
| publisher | eLife Sciences Publications Ltd |
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| series | eLife |
| spelling | doaj.art-93a5c021808f40f488695ae0349d180f2023-11-24T15:57:17ZengeLife Sciences Publications LtdeLife2050-084X2023-11-011210.7554/eLife.83565Sleep spindle maturity promotes slow oscillation-spindle coupling across child and adolescent developmentAnn-Kathrin Joechner0https://orcid.org/0000-0003-4962-1089Michael A Hahn1https://orcid.org/0000-0002-3022-0552Georg Gruber2Kerstin Hoedlmoser3https://orcid.org/0000-0001-5177-4389Markus Werkle-Bergner4https://orcid.org/0000-0002-6399-9996Center for Lifespan Psychology, Max Planck Institute for Human Development, Berlin, GermanyDepartment of Psychology, Laboratory for Sleep, Cognition and Consciousness Research, University of Salzburg, Salzburg, Austria; Centre for Cognitive Neuroscience Salzburg (CCNS), University of Salzburg, Salzburg, Austria; Hertie-Institute for Clinical Brain Research, University Medical Center Tuebingen, Tuebingen, GermanyDepartment of Psychiatry and Psychotherapy, Medical University of Vienna, Vienna, Austria; The Siesta Group, Vienna, AustriaDepartment of Psychology, Laboratory for Sleep, Cognition and Consciousness Research, University of Salzburg, Salzburg, Austria; Centre for Cognitive Neuroscience Salzburg (CCNS), University of Salzburg, Salzburg, AustriaCenter for Lifespan Psychology, Max Planck Institute for Human Development, Berlin, GermanyThe 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.https://elifesciences.org/articles/83565sleepmemoryrhythmic neural activity |
| spellingShingle | Ann-Kathrin Joechner Michael A Hahn Georg Gruber Kerstin Hoedlmoser Markus Werkle-Bergner Sleep spindle maturity promotes slow oscillation-spindle coupling across child and adolescent development eLife sleep memory rhythmic neural activity |
| 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 | sleep memory rhythmic neural activity |
| url | https://elifesciences.org/articles/83565 |
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