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J Neurosci. 2017 Nov 29;37(48):11675-11687. doi: 10.1523/JNEUROSCI.3033-16.2017. Epub 2017 Oct 30.

White Matter Structure in Older Adults Moderates the Benefit of Sleep Spindles on Motor Memory Consolidation.

Author information

1
Sleep and Neuroimaging Laboratory, Department of Psychology, University of California, Berkeley, bmander@uci.edu mpwalker@berkeley.edu.
2
Department of Psychiatry and Human Behavior, University of California, Irvine, Orange, California 92868.
3
Sleep and Neuroimaging Laboratory, Department of Psychology, University of California, Berkeley.
4
Department of Psychiatry, McGill University, Montreal, Quebec, Canada.
5
Division of Pulmonary and Critical Care Medicine, California Pacific Medical Center, San Francisco, California 94115.
6
Department of Psychiatry and Human Behavior, Alpert Medical School of Brown University, Providence, Rhode Island 02903, and.
7
Department of Psychiatry, University of California, San Diego, La Jolla, California 92093.
8
Helen Wills Neuroscience Institute, and.
9
Life Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, California 94720.

Abstract

Sleep spindles promote the consolidation of motor skill memory in young adults. Older adults, however, exhibit impoverished sleep-dependent motor memory consolidation. The underlying pathophysiological mechanism(s) explaining why motor memory consolidation in older adults fails to benefit from sleep remains unclear. Here, we demonstrate that male and female older adults show impoverished overnight motor skill memory consolidation relative to young adults, with the extent of impairment being associated with the degree of reduced frontal fast sleep spindle density. The magnitude of the loss of frontal fast sleep spindles in older adults was predicted by the degree of reduced white matter integrity throughout multiple white matter tracts known to connect subcortical and cortical brain regions. We further demonstrate that the structural integrity of selective white matter fiber tracts, specifically within right posterior corona radiata, right tapetum, and bilateral corpus callosum, statistically moderates whether sleep spindles promoted overnight consolidation of motor skill memory. Therefore, white matter integrity within tracts known to connect cortical sensorimotor control regions dictates the functional influence of sleep spindles on motor skill memory consolidation in the elderly. The deterioration of white matter fiber tracts associated with human brain aging thus appears to be one pathophysiological mechanism influencing subcortical-cortical propagation of sleep spindles and their related memory benefits.SIGNIFICANCE STATEMENT Numerous studies have shown that sleep spindle expression is reduced and sleep-dependent motor memory is impaired in older adults. However, the mechanisms underlying these alterations have remained unknown. The present study reveals that age-related degeneration of white matter within select fiber tracts is associated with reduced sleep spindles in older adults. We further demonstrate that, within these same fiber tracts, the degree of degeneration determines whether sleep spindles can promote motor memory consolidation. Therefore, white matter integrity in the human brain, more than age per se, determines the magnitude of decline in sleep spindles in later life and, with it, the success (or lack thereof) of sleep-dependent motor memory consolidation in older adults.

KEYWORDS:

DTI; WMH; aging; motor memory; sleep; sleep spindles

PMID:
29084867
PMCID:
PMC5707766
DOI:
10.1523/JNEUROSCI.3033-16.2017
[Indexed for MEDLINE]
Free PMC Article

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