National Library of Medicine - National Center for Biotechnology Information

2018 Jan 3;97(1):221-230.e4. doi: 10.1016/j.neuron.2017.11.020. Epub 2017 Dec 14.

Old Brains Come Uncoupled in Sleep: Slow Wave-Spindle Synchrony, Brain Atrophy, and Forgetting

Randolph F Helfrich 1, Bryce A Mander 2, William J Jagust 3, Robert T Knight 3, Matthew P Walker 3

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Abstract

The coupled interaction between slow-wave oscillations and sleep spindles during non-rapid-eye-movement (NREM) sleep has been proposed to support memory consolidation. However, little evidence in humans supports this theory. Moreover, whether such dynamic coupling is impaired as a consequence of brain aging in later life, contributing to cognitive and memory decline, is unknown. Combining electroencephalography (EEG), structural MRI, and sleep-dependent memory assessment, we addressed these questions in cognitively normal young and older adults. Directional cross-frequency coupling analyses demonstrated that the slow wave governs a precise temporal coordination of sleep spindles, the quality of which predicts overnight memory retention. Moreover, selective atrophy within the medial frontal cortex in older adults predicted a temporal dispersion of this slow wave-spindle coupling, impairing overnight memory consolidation and leading to forgetting. Prefrontal-dependent deficits in the spatiotemporal coordination of NREM sleep oscillations therefore represent one pathway explaining age-related memory decline.

Keywords: age-related memory decline; aging; atrophy; directional cross-frequency coupling; hierarchical nesting; hippocampus-dependent memory consolidation; overnight forgetting; prefrontal cortex; sleep spindles; slow oscillation.

Copyright © 2017 Elsevier Inc. All rights reserved.

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Figures

Figure 1

Figure 1. Memory task and oscillatory signatures…

 

Figure 2

Figure 2. SO-Spindle interactions in old and…

 

Figure 3

Figure 3. Timing of SO-spindle interactions predicts…

 

Figure 4

Figure 4. Directional SO-spindle coupling depends on…

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Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

    MeSH terms

    • Aged
    • Aging / pathology*
    • Aging / physiology
    • Atrophy
    • Brain / pathology*
    • Brain / physiopathology*
    • Female
    • Humans
    • Male
    • Memory Consolidation / physiology*
    • Sleep / physiology*
    • Young Adult

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