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      Sleep Architecture When Sleeping at an Unusual Circadian Time and Associations with Insulin Sensitivity

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          Abstract

          Circadian misalignment affects total sleep time, but it may also affect sleep architecture. The objectives of this study were to examine intra-individual effects of circadian misalignment on sleep architecture and inter-individual relationships between sleep stages, cortisol levels and insulin sensitivity. Thirteen subjects (7 men, 6 women, age: 24.3±2.5 y; BMI: 23.6±1.7 kg/m 2) stayed in a time blinded respiration chamber during three light-entrained circadian cycles (3x21h and 3x27h) resulting in a phase advance and a phase delay. Sleep was polysomnographically recorded. Blood and salivary samples were collected to determine glucose, insulin and cortisol concentrations. Intra-individually, a phase advance decreased rapid eye movement (REM) sleep and slow-wave sleep (SWS), increased time awake, decreased sleep and REM sleep latency compared to the 24h cycle. A phase delay increased REM sleep, decreased stage 2 sleep, increased time awake, decreased sleep and REM sleep latency compared to the 24h cycle. Moreover, circadian misalignment changed REM sleep distribution with a relatively shorter REM sleep during the second part of the night. Inter-individually, REM sleep was inversely associated with cortisol levels and HOMA-IR index. Circadian misalignment, both a phase advance and a phase delay, significantly changed sleep architecture and resulted in a shift in rem sleep. Inter-individually, shorter REM sleep during the second part of the night was associated with dysregulation of the HPA-axis and reduced insulin sensitivity.

          Trial Registration: International Clinical Trials Registry Platform NTR2926 http://apps.who.int/trialsearch/

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          Most cited references25

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          A Biometric Study of Human Basal Metabolism.

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            Sleep curtailment is accompanied by increased intake of calories from snacks.

            Short sleep is associated with obesity and may alter the endocrine regulation of hunger and appetite. We tested the hypothesis that the curtailment of human sleep could promote excessive energy intake. Eleven healthy volunteers [5 women, 6 men; mean +/- SD age: 39 +/- 5 y; mean +/- SD body mass index (in kg/m(2)): 26.5 +/- 1.5] completed in random order two 14-d stays in a sleep laboratory with ad libitum access to palatable food and 5.5-h or 8.5-h bedtimes. The primary endpoints were calories from meals and snacks consumed during each bedtime condition. Additional measures included total energy expenditure and 24-h profiles of serum leptin and ghrelin. Sleep was reduced by 122 +/- 25 min per night during the 5.5-h bedtime condition. Although meal intake remained similar (P = 0.51), sleep restriction was accompanied by increased consumption of calories from snacks (1087 +/- 541 compared with 866 +/- 365 kcal/d; P = 0.026), with higher carbohydrate content (65% compared with 61%; P = 0.04), particularly during the period from 1900 to 0700. These changes were not associated with a significant increase in energy expenditure (2526 +/- 537 and 2390 +/- 369 kcal/d during the 5.5-h and 8.5-h bedtime periods, respectively; P = 0.58), and we found no significant differences in serum leptin and ghrelin between the 2 sleep conditions. Recurrent bedtime restriction can modify the amount, composition, and distribution of human food intake, and sleeping short hours in an obesity-promoting environment may facilitate the excessive consumption of energy from snacks but not meals.
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              Paradoxical timing of the circadian rhythm of sleep propensity serves to consolidate sleep and wakefulness in humans.

              The contribution of the circadian pacemaker and the sleep homeostat to sleep tendency and consolidation was quantified by forced desynchrony of the sleep-wake cycle from the circadian pacemaker in eight men who lived in time-isolation for 33-36 days. Analysis of 175 polygraphically recorded sleep episodes revealed that the circadian pacemaker and the sleep homeostat contribute about equally to sleep consolidation, and that the phase relationship between these oscillatory processes during entrainment to the 24-h day is uniquely timed to facilitate the ability to maintain a consolidated bout of sleep at night and a consolidated bout of wakefulness throughout the day.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2013
                8 August 2013
                : 8
                : 8
                : e72877
                Affiliations
                [1]Department of Human Biology, Nutrition and Toxicology Research Institute Maastricht, Maastricht University, Maastricht, The Netherlands
                Paris Institute of Technology for Life, Food and Environmental Sciences, France
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: HKJG FR MSW-P. Performed the experiments: HKJG CM FR EAPM. Analyzed the data: HKJG CM. Wrote the manuscript: HKJG. Reviewed and edited the manuscript: TCA MSW-P. Supervised execution of the study: MSW-P.

                Article
                PONE-D-13-02523
                10.1371/journal.pone.0072877
                3738551
                23951335
                f0496624-1f29-4f53-8244-9c5764992507
                Copyright @ 2013

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 9 January 2013
                : 10 July 2013
                Funding
                The authors have no funding or support to report.
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                Research Article

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