Precise Slow Oscillation–Spindle Coupling Promotes Memory Consolidation in Younger and Older Adults
Memory consolidation during sleep relies on the precisely timed interaction of rhythmic neural events. Here, we investigate differences in slow oscillations (SO; 0.5–1 Hz), sleep spindles (SP), and their coupling across the adult human lifespan and ask whether observed alterations relate to the abil...
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          | Published in | Scientific reports Vol. 9; no. 1; p. 1940 | 
|---|---|
| Main Authors | , , , , , , | 
| Format | Journal Article | 
| Language | English | 
| Published | 
        London
          Nature Publishing Group UK
    
        13.02.2019
     Nature Publishing Group  | 
| Subjects | |
| Online Access | Get full text | 
| ISSN | 2045-2322 2045-2322  | 
| DOI | 10.1038/s41598-018-36557-z | 
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| Abstract | Memory consolidation during sleep relies on the precisely timed interaction of rhythmic neural events. Here, we investigate differences in slow oscillations (SO; 0.5–1 Hz), sleep spindles (SP), and their coupling across the adult human lifespan and ask whether observed alterations relate to the ability to retain associative memories across sleep. We demonstrate that older adults do not show the fine-tuned coupling of fast SPs (12.5–16 Hz) to the SO peak present in younger adults but, instead, are characterized most by a slow SP power increase (9–12.5 Hz) at the end of the SO up-state. This slow SP power increase, typical for older adults, coincides with worse memory consolidation in young age already, whereas the tight precision of SO–fast SP coupling promotes memory consolidation across younger and older adults. Crucially, brain integrity in source regions of SO and SP generation, including the medial prefrontal cortex, thalamus, hippocampus and entorhinal cortex, reinforces this beneficial SO–SP coupling in old age. Our results reveal that cognitive functioning is not only determined by maintaining structural brain integrity across the adult lifespan, but also by the preservation of precisely timed neural interactions during sleep that enable the consolidation of declarative memories. | 
    
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| AbstractList | Memory consolidation during sleep relies on the precisely timed interaction of rhythmic neural events. Here, we investigate differences in slow oscillations (SO; 0.5-1 Hz), sleep spindles (SP), and their coupling across the adult human lifespan and ask whether observed alterations relate to the ability to retain associative memories across sleep. We demonstrate that older adults do not show the fine-tuned coupling of fast SPs (12.5-16 Hz) to the SO peak present in younger adults but, instead, are characterized most by a slow SP power increase (9-12.5 Hz) at the end of the SO up-state. This slow SP power increase, typical for older adults, coincides with worse memory consolidation in young age already, whereas the tight precision of SO-fast SP coupling promotes memory consolidation across younger and older adults. Crucially, brain integrity in source regions of SO and SP generation, including the medial prefrontal cortex, thalamus, hippocampus and entorhinal cortex, reinforces this beneficial SO-SP coupling in old age. Our results reveal that cognitive functioning is not only determined by maintaining structural brain integrity across the adult lifespan, but also by the preservation of precisely timed neural interactions during sleep that enable the consolidation of declarative memories.Memory consolidation during sleep relies on the precisely timed interaction of rhythmic neural events. Here, we investigate differences in slow oscillations (SO; 0.5-1 Hz), sleep spindles (SP), and their coupling across the adult human lifespan and ask whether observed alterations relate to the ability to retain associative memories across sleep. We demonstrate that older adults do not show the fine-tuned coupling of fast SPs (12.5-16 Hz) to the SO peak present in younger adults but, instead, are characterized most by a slow SP power increase (9-12.5 Hz) at the end of the SO up-state. This slow SP power increase, typical for older adults, coincides with worse memory consolidation in young age already, whereas the tight precision of SO-fast SP coupling promotes memory consolidation across younger and older adults. Crucially, brain integrity in source regions of SO and SP generation, including the medial prefrontal cortex, thalamus, hippocampus and entorhinal cortex, reinforces this beneficial SO-SP coupling in old age. Our results reveal that cognitive functioning is not only determined by maintaining structural brain integrity across the adult lifespan, but also by the preservation of precisely timed neural interactions during sleep that enable the consolidation of declarative memories. Memory consolidation during sleep relies on the precisely timed interaction of rhythmic neural events. Here, we investigate differences in slow oscillations (SO; 0.5–1 Hz), sleep spindles (SP), and their coupling across the adult human lifespan and ask whether observed alterations relate to the ability to retain associative memories across sleep. We demonstrate that older adults do not show the fine-tuned coupling of fast SPs (12.5–16 Hz) to the SO peak present in younger adults but, instead, are characterized most by a slow SP power increase (9–12.5 Hz) at the end of the SO up-state. This slow SP power increase, typical for older adults, coincides with worse memory consolidation in young age already, whereas the tight precision of SO–fast SP coupling promotes memory consolidation across younger and older adults. Crucially, brain integrity in source regions of SO and SP generation, including the medial prefrontal cortex, thalamus, hippocampus and entorhinal cortex, reinforces this beneficial SO–SP coupling in old age. Our results reveal that cognitive functioning is not only determined by maintaining structural brain integrity across the adult lifespan, but also by the preservation of precisely timed neural interactions during sleep that enable the consolidation of declarative memories.  | 
    
| ArticleNumber | 1940 | 
    
| Author | Grandy, Thomas H. Muehlroth, Beate E. Werkle-Bergner, Markus Fandakova, Yana Shing, Yee Lee Sander, Myriam C. Rasch, Björn  | 
    
| Author_xml | – sequence: 1 givenname: Beate E. surname: Muehlroth fullname: Muehlroth, Beate E. email: muehlroth@mpib-berlin.mpg.de organization: Center for Lifespan Psychology, Max Planck Institute for Human Development – sequence: 2 givenname: Myriam C. surname: Sander fullname: Sander, Myriam C. organization: Center for Lifespan Psychology, Max Planck Institute for Human Development – sequence: 3 givenname: Yana surname: Fandakova fullname: Fandakova, Yana organization: Center for Lifespan Psychology, Max Planck Institute for Human Development – sequence: 4 givenname: Thomas H. surname: Grandy fullname: Grandy, Thomas H. organization: Center for Lifespan Psychology, Max Planck Institute for Human Development – sequence: 5 givenname: Björn surname: Rasch fullname: Rasch, Björn organization: Department of Psychology, University of Fribourg – sequence: 6 givenname: Yee Lee surname: Shing fullname: Shing, Yee Lee organization: Center for Lifespan Psychology, Max Planck Institute for Human Development, Department of Developmental Psychology, Goethe University Frankfurt – sequence: 7 givenname: Markus orcidid: 0000-0002-6399-9996 surname: Werkle-Bergner fullname: Werkle-Bergner, Markus email: werkle@mpib-berlin.mpg.de organization: Center for Lifespan Psychology, Max Planck Institute for Human Development  | 
    
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/30760741$$D View this record in MEDLINE/PubMed | 
    
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| Publisher_xml | – name: Nature Publishing Group UK – name: Nature Publishing Group  | 
    
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| Snippet | Memory consolidation during sleep relies on the precisely timed interaction of rhythmic neural events. Here, we investigate differences in slow oscillations... | 
    
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| SubjectTerms | 59/57 631/378/1595/2167 631/378/1595/2638 631/378/2612 631/378/2649 631/477/2811 Activity patterns Adults Animal memory Cognitive ability Cortex (entorhinal) Humanities and Social Sciences Life span Memory multidisciplinary Older people Oscillations Prefrontal cortex Preservation Rhythms Science Science (multidisciplinary) Sleep Thalamus  | 
    
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| Title | Precise Slow Oscillation–Spindle Coupling Promotes Memory Consolidation in Younger and Older Adults | 
    
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