Age-Related Influences of Prior Sleep on Brain Activation during Verbal Encoding

Michelle B Jonelis,Sonia Ancoli-Israel,Jennifer S Salamat,Benjamin S Mckenna,Mark W Bondi,Sean P A Drummond

doi:10.3389/fneur.2012.00049

Abstract

Disrupted sleep is more common in older adults (OLD) than younger adults (YOUNG), often co-morbid with other conditions. How these sleep disturbances affect cognitive performance is an area of active study. We examined whether brain activation during verbal encoding correlates with sleep quantity and quality the night before testing in a group of healthy OLD and YOUNG. Twenty-seven OLD (ages 59–82) and 27 YOUNG (ages 19–36) underwent one night of standard polysomnography. Twelve hours post-awakening, subjects performed a verbal encoding task while undergoing functional magnetic resonance imaging. Analyses examined the group (OLD vs. YOUNG) by prior sleep quantity (total sleep time, TST) or quality (sleep efficiency, SE) interaction on cerebral activation, controlling for performance. Longer TST promoted higher levels of activation in the bilateral anterior parahippocampal in OLD and lower activation levels in the left anterior parahippocampus in YOUNG. Greater SE promoted higher activation levels in the left posterior parahippocampus and right inferior frontal gyrus in YOUNG, but not in OLD. The roles of these brain regions in verbal encoding suggest, in OLD, longer sleep duration may be linked to the ability to engage in functional compensation during cognitive challenges. By contrast, in YOUNG, shorter sleep duration may necessitate functional compensation to maintain cognitive performance, similar to what is seen following acute sleep deprivation. Additionally, in YOUNG, better sleep quality may improve semantic retrieval processes, thereby aiding encoding.

Highlights

Disrupted sleep is more common in older adults (OLD) than younger adults (YOUNG), often co-morbid with other conditions
We hypothesized lower quantity and quality of sleep would result in greater cerebral responses in brain regions involved in verbal encoding for OLD but not for YOUNG
In summary, our study used a verbal encoding task to examine whether the quantity and quality of sleep during the night immediately preceding testing affected the cerebral response to this cognitive challenge differently for OLD and YOUNG

Summary

Introduction

Disrupted sleep is more common in older adults (OLD) than younger adults (YOUNG), often co-morbid with other conditions. The general trend is toward a decline with age, OLD show greater variability than YOUNG in both sleep and cognition, with some OLD showing little or no decline relative to YOUNG (Middleton and Strick, 2002; Ohayon et al, 2004). While both sleep and cognitive performance measures tend to decrease with age, if and how sleep changes in aging might affect cognitive function is not well known. Since experimental sleep deprivation studies show sleep loss is associated with performance decline in most cognitive domains in YOUNG, there has been speculation about whether the decline in cognitive performance with age could be explained by the corresponding decline in sleep with age

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