Slow oscillation–spindle coupling strength predicts real-life gross-motor learning in adolescents and adults
Previously, we demonstrated that precise temporal coordination between slow oscillations (SOs) and sleep spindles indexes declarative memory network development (Hahn et al., 2020). However, it is unclear whether these findings in the declarative memory domain also apply in the motor memory domain....
| Main Authors: | , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
eLife Sciences Publications Ltd
2022-02-01
|
| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/66761 |
| _version_ | 1811227501792329728 |
|---|---|
| author | Michael A Hahn Kathrin Bothe Dominik Heib Manuel Schabus Randolph F Helfrich Kerstin Hoedlmoser |
| author_facet | Michael A Hahn Kathrin Bothe Dominik Heib Manuel Schabus Randolph F Helfrich Kerstin Hoedlmoser |
| author_sort | Michael A Hahn |
| collection | DOAJ |
| description | Previously, we demonstrated that precise temporal coordination between slow oscillations (SOs) and sleep spindles indexes declarative memory network development (Hahn et al., 2020). However, it is unclear whether these findings in the declarative memory domain also apply in the motor memory domain. Here, we compared adolescents and adults learning juggling, a real-life gross-motor task. Juggling performance was impacted by sleep and time of day effects. Critically, we found that improved task proficiency after sleep lead to an attenuation of the learning curve, suggesting a dynamic juggling learning process. We employed individualized cross-frequency coupling analyses to reduce inter- and intragroup variability of oscillatory features. Advancing our previous findings, we identified a more precise SO–spindle coupling in adults compared to adolescents. Importantly, coupling precision over motor areas predicted overnight changes in task proficiency and learning curve, indicating that SO–spindle coupling relates to the dynamic motor learning process. Our results provide first evidence that regionally specific, precisely coupled sleep oscillations support gross-motor learning. |
| first_indexed | 2024-04-12T09:42:33Z |
| format | Article |
| id | doaj.art-a1161ce83a284f6cbd7da11938983c4e |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-12T09:42:33Z |
| publishDate | 2022-02-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-a1161ce83a284f6cbd7da11938983c4e2022-12-22T03:38:02ZengeLife Sciences Publications LtdeLife2050-084X2022-02-011110.7554/eLife.66761Slow oscillation–spindle coupling strength predicts real-life gross-motor learning in adolescents and adultsMichael A Hahn0https://orcid.org/0000-0002-3022-0552Kathrin Bothe1Dominik Heib2Manuel Schabus3https://orcid.org/0000-0001-5899-8772Randolph F Helfrich4https://orcid.org/0000-0001-8045-3111Kerstin Hoedlmoser5https://orcid.org/0000-0001-5177-4389Department 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 Tübingen, Tübingen, 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, 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, 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, AustriaHertie-Institute for Clinical Brain Research, University Medical Center Tübingen, Tübingen, 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, AustriaPreviously, we demonstrated that precise temporal coordination between slow oscillations (SOs) and sleep spindles indexes declarative memory network development (Hahn et al., 2020). However, it is unclear whether these findings in the declarative memory domain also apply in the motor memory domain. Here, we compared adolescents and adults learning juggling, a real-life gross-motor task. Juggling performance was impacted by sleep and time of day effects. Critically, we found that improved task proficiency after sleep lead to an attenuation of the learning curve, suggesting a dynamic juggling learning process. We employed individualized cross-frequency coupling analyses to reduce inter- and intragroup variability of oscillatory features. Advancing our previous findings, we identified a more precise SO–spindle coupling in adults compared to adolescents. Importantly, coupling precision over motor areas predicted overnight changes in task proficiency and learning curve, indicating that SO–spindle coupling relates to the dynamic motor learning process. Our results provide first evidence that regionally specific, precisely coupled sleep oscillations support gross-motor learning.https://elifesciences.org/articles/66761sleepmemory consolidationcross-frequency couplingmotor memorysleep spindlesdevelopment |
| spellingShingle | Michael A Hahn Kathrin Bothe Dominik Heib Manuel Schabus Randolph F Helfrich Kerstin Hoedlmoser Slow oscillation–spindle coupling strength predicts real-life gross-motor learning in adolescents and adults eLife sleep memory consolidation cross-frequency coupling motor memory sleep spindles development |
| title | Slow oscillation–spindle coupling strength predicts real-life gross-motor learning in adolescents and adults |
| title_full | Slow oscillation–spindle coupling strength predicts real-life gross-motor learning in adolescents and adults |
| title_fullStr | Slow oscillation–spindle coupling strength predicts real-life gross-motor learning in adolescents and adults |
| title_full_unstemmed | Slow oscillation–spindle coupling strength predicts real-life gross-motor learning in adolescents and adults |
| title_short | Slow oscillation–spindle coupling strength predicts real-life gross-motor learning in adolescents and adults |
| title_sort | slow oscillation spindle coupling strength predicts real life gross motor learning in adolescents and adults |
| topic | sleep memory consolidation cross-frequency coupling motor memory sleep spindles development |
| url | https://elifesciences.org/articles/66761 |
| work_keys_str_mv | AT michaelahahn slowoscillationspindlecouplingstrengthpredictsreallifegrossmotorlearninginadolescentsandadults AT kathrinbothe slowoscillationspindlecouplingstrengthpredictsreallifegrossmotorlearninginadolescentsandadults AT dominikheib slowoscillationspindlecouplingstrengthpredictsreallifegrossmotorlearninginadolescentsandadults AT manuelschabus slowoscillationspindlecouplingstrengthpredictsreallifegrossmotorlearninginadolescentsandadults AT randolphfhelfrich slowoscillationspindlecouplingstrengthpredictsreallifegrossmotorlearninginadolescentsandadults AT kerstinhoedlmoser slowoscillationspindlecouplingstrengthpredictsreallifegrossmotorlearninginadolescentsandadults |