Abstract
Study Objectives: To examine the association between sleep duration trajectories over 28 years and measures of cognition, gray matter volume, and white matter microstructure. We hypothesize that consistently meeting sleep guidelines that recommend at least 7 hours of sleep per night will be associated with better cognition, greater gray matter volumes, higher fractional anisotropy, and lower radial diffusivity values.
Methods: We studied 613 participants (age 42.3 ± 5.03 years at baseline) who self-reported sleep duration at five time points between 1985 and 2013, and who had cognitive testing and magnetic resonance imaging administered at a single timepoint between 2012 and 2016. We applied latent class growth analysis to estimate membership into trajectory groups based on self-reported sleep duration over time. Analysis of gray matter volumes was carried out using FSL Voxel-Based-Morphometry and white matter microstructure using Tract Based Spatial Statistics. We assessed group differences in cognitive and MRI outcomes using nonparametric permutation testing.
Results: Latent class growth analysis identified four trajectory groups, with an average sleep duration of 5.4 ± 0.2 hours (5%, N = 29), 6.2 ± 0.3 hours (37%, N = 228), 7.0 ± 0.2 hours (45%, N = 278), and 7.9 ± 0.3 hours (13%, N = 78). No differences in cognition, gray matter, and white matter measures were detected between groups.
Conclusions: Our null findings suggest that current sleep guidelines that recommend at least 7 hours of sleep per night may not be supported in relation to an association between sleep patterns and cognitive function or brain structure.
Keywords: aging, cognition, gray matter, sleep, white matter
Statement of Significance: Up to a third of adults report between 6 and 7 hours of sleep per night, and thus fail to meet sleep guidelines which recommend at least 7 hours of sleep per night. Although extreme short sleep (e.g. ≤5 hours per night) has repeatedly been associated with poor cognitive health, it is currently unclear if such relationships subsist for more moderate short-sleep durations. We found no differences in cognitive or structural MRI measures between groups that reported, on average, 5.4 hours, 6.2 hours, 7.0 hours, and 7.9 hours sleep per night over 5 timepoints spanning 28 years. If replicated with longitudinal markers of cognitive health, such null results could challenge the suitability of current sleep guidelines on cognitive outcomes.
Discussion
The aim of this study was to examine sleep duration trajectories over a 28-year period and their relationship with measures of cognition, gray matter volume, and white matter microstructure. We hypothesized that consistently meeting recommendations for sleep duration (i.e. self-reporting a minimum of 7 hours sleep per night) would be favorably associated with cognition, gray matter volume and white matter microstructure, compared with consistently not meeting the guidelines or transitioning in and out of the guidelines over time. In contrast to our hypotheses, our results did not show any differences in cognitive measures, gray matter volume, or white matter microstructure between different sleep trajectory groups.To the best of our knowledge, only one study has previously applied latent class growth modeling to examine trajectories of self-reported sleep duration over time within an adult population. In a study of 8,673 Canadian adults, Gilmour et al. identified four sleep trajectory groups with intercepts of 5.57 hours (11% of participants), 6.68 hours (49%), 7.65 hours (37%), and 8.34 hours (2%) [36]. We also identified four trajectory groups, with intercepts of 5.54 hours (5% of participants), 6.57 hours (37%), 6.95 hours (45%), and 7.85 (13%) hours. With regard to shape, the trajectories identified in both studies displayed limited meaningful change over time. For example, average sleep duration differed by less than an hour between timepoints in all groups—indicating that extreme increases or decreases in sleep duration over time are limited in prevalence. Given that our studies differ both in terms of demographics and methods (e.g. sleep duration was assessed over an 8-year time period in Gilmour et al. [36], compared with over 28-years in our study), it is encouraging that our results are broadly complimentary.
Of particular note within our study is that 37% of participants were included in a group with an average sleep duration of 6.2 hours. Guidelines published by the American Society for Sleep Medicine and the Sleep Research Society state that “adults should sleep 7 or more hours per night on a regular basis to promote optimal health” [4]. In addition, the National Sleep Foundation’s guidelines posit that 7–9 hours sleep per night is “recommended” for health and well-being, with less than 6 hours sleep “not recommended” [3]. In these guidelines, 6 hours sleep per night falls in a somewhat gray area between these two groups, and is classified as “may be appropriate.” Relevant to the revision of such guidelines, our study found no evidence to suggest that consistently reporting approximately 6 hours sleep per night is associated with adverse cognitive and MRI outcomes.
Such null findings, however, do not necessarily indicate that sleep duration is not important to cognitive health. Rather, our null findings may reflect the limited number of participants reporting extremes in sleep duration within our sample. At each phase, between 92% and 96% of participants reported 6, 7, or 8 hours sleep per night (Supplementary Material Table S5). The group with the shortest sleep duration in our study contained just 5% of participants and had a mean sleep duration of 5.4 hours. The group with the longest sleep duration, which contained 13% of participants, had a mean sleep duration of 7.87 hours—a value that falls within guidelines for recommended sleep durations. Change in sleep duration was also limited within our sample—between 89% and 94% of participants reported change in sleep duration of 0–1 hour between the baseline and subsequent data waves (Supplementary Material Tables S6–S7), and sleep trajectories remained relatively stable over time overall. Significant group differences for cognitive and MRI measures may only become apparent with larger samples of more extreme sleep durations, groups that have often been the focus of cognitive studies to date. For example, in a meta-analysis that reported significant associations between sleep duration and cognitive outcomes, the most common category for short-sleep duration was 5 hours or less (ranging from <4 to ≤6.5 hours), and the most common category for long-sleep duration was 9 hours or more (ranging from ≥8 to ≥11 hours) [5]. Furthermore, although few studies have examined the change in sleep duration over time, Devore et al. reported that women whose sleep duration changed by 2 hours or more in any direction, had worse cognitive outcomes compared with women with no change in sleep duration [8]. In addition, previous studies based on the entire Whitehall II cohort found that adverse changes in sleep duration are associated with poorer cognitive function [6]. There are many reasons that our findings may diverge, despite overlapping samples. These include differences in sample size (5431 vs 631; thereby impacting on power to assess extremes in sleep duration and change), characteristics (see Supplementary Material Table S8 for comparison), number of assessments of sleep duration (2 vs 5 times), and cognitive test battery administered. Therefore, our study does not contradict the hypothesis that extreme short sleep, extreme long sleep, or extreme changes in sleep duration are associated with adverse outcomes; but instead indicates that such groups may not be well represented in small population-based samples.
An alternative explanation for our null results is that it is not sleep duration alone that is associated with cognitive health in aging, but rather a combination of sleep quality and quantity. Indeed, in an overlapping sample, we have previously published that poor sleep quality is associated with reduced FA and increased RD within fronto-subcortical regions [15]. In an exploratory post hoc analysis, we divided the 6-hour and 7-hour groups into poor and good sleep quality groups dependent upon their PSQI score at the time of the MRI scan (due to limited sample size, we did not include 5-hour and 8-hour groups in this analysis) (Supplementary Material: Text S2, Table S9). F tests showed significant group differences for global FA and voxel-wise RD. The 6-hour good sleep quality group displayed higher global FA and reduced RD in widespread tracts, compared with both the 6-hour poor sleep quality group and 7-hour poor sleep quality group (Figure S2). The 6-hour good sleep quality group also displayed reduced RD compared with the 7-hour good sleep quality group in the corpus callosum (Figure S2). These results indicate that the combination of sleep quality and quantity may be more sensitive to measures of cognitive health in aging. However, it is critical to stress that our measures of sleep quality and quantity are not directly comparable (e.g. quality was measured using a 17-item questionnaire at a single timepoint, duration was measured using a single-item questionnaire at five timepoints). Therefore, these post hoc results should be considered exploratory and require independent replication.
Our study has a number of strengths, including the availability of sleep duration data at five points spanning 28 years prior to cognitive and MRI assessment, which allowed us to examine sleep trajectories over time. A major limitation of our analysis was the reliance on a single-item self-report of sleep duration, in which participants could only report their sleep durations in discrete categories (i.e. “5 hours or less,” “6 hours,” “7 hours,” “8 hours,” or “9 hours or more”). Sleep duration may be more sensitively measured if sleep was measured in hours and minutes and if there were no lower or upper thresholds for sleep duration. A further limitation is that participants were asked to report their sleep duration only on an “average week night.” The discrepancy between weeknight and weekend sleep duration is common in working-age populations and there is debate regarding whether long weekend sleep can compensate for short weeknight sleep for health outcomes such as mortality [37], weight, and insulin sensitivity [38]. In the Whitehall II study, the agreement between self-reported and accelerometer-measured total sleep duration was slightly higher in weekdays (kappa = 0.37, 95% CI 0.34–0.40) than weekend days (kappa = 0.33, 95% CI 0.31–0.36) [39]. Further research is needed to examine the long-term effects of weekend recovery sleep on cognition. Sleep duration is also often overestimated in self-reported compared to objective studies [40–42]. For example, within the Sleep Heart Health Study of 2,113 adults at a mean age of 67 years, morning self-estimated sleep time and total sleep time measured by polysomnography were estimated as 379 and 363 minutes, respectively, with a weak correlation of r = 0.16 between the measures [41]. Self-reported total sleep duration and sleep duration assessed using a wrist-worn accelerometer were moderately related in the Whitehall II study of 4,094 adults aged 60–83 (kappa 0.39, 95% CI 0.36–0.42) [39]. Importantly, differences between measurements may impact upon observed relationships with cognitive outcomes. For example, the Sleep Study of the National Social Life, Health, and Aging Project (NSHAP), a nationally representative cohort of older US adults (2010–2015), found that actigraphic measures of sleep disruption were associated with worse cognition and higher odds of 5-year cognitive decline but there was no association for self-reported sleep [43]. As self-reported measures of sleep duration correlate well with daily sleep diaries [44], are the mainstay of population-based cohort studies, and are the focus of sleep guidelines, further studies using both objective and self-report measures of sleep duration to examine cognitive and MRI outcomes are needed. Furthermore, our findings have limited generalizability, given that the Whitehall participants have relatively high educational attainment which might contribute to increased cognitive reserve. As a result, we may have underestimated the long-term neurocognitive effects associated with unfavorable sleep patterns in subpopulations of low educational attainment, who may be more sensitive to the detrimental health effects of sleep disturbance. We were also unable to rule out potential selection bias; it is plausible that those with the greatest cognitive decline and/or most extreme sleep durations were less likely to return for a follow-up assessment.
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