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      Voluntary exercise can strengthen the circadian system in aged mice

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          Abstract

          Consistent daily rhythms are important to healthy aging according to studies linking disrupted circadian rhythms with negative health impacts. We studied the effects of age and exercise on baseline circadian rhythms and on the circadian system's ability to respond to the perturbation induced by an 8 h advance of the light:dark (LD) cycle as a test of the system's robustness. Mice (male, mPer2 luc/C57BL/6) were studied at one of two ages: 3.5 months ( n = 39) and >18 months ( n = 72). We examined activity records of these mice under entrained and shifted conditions as well as mPER2::LUC measures ex vivo to assess circadian function in the suprachiasmatic nuclei (SCN) and important target organs. Age was associated with reduced running wheel use, fragmentation of activity, and slowed resetting in both behavioral and molecular measures. Furthermore, we observed that for aged mice, the presence of a running wheel altered the amplitude of the spontaneous firing rate rhythm in the SCN in vitro. Following a shift of the LD cycle, both young and aged mice showed a change in rhythmicity properties of the mPER2::LUC oscillation of the SCN in vitro, and aged mice exhibited longer lasting internal desynchrony. Access to a running wheel alleviated some age-related changes in the circadian system. In an additional experiment, we replicated the effect of the running wheel, comparing behavioral and in vitro results from aged mice housed with or without a running wheel (>21 months, n = 8 per group, all examined 4 days after the shift). The impact of voluntary exercise on circadian rhythm properties in an aged animal is a novel finding and has implications for the health of older people living with environmentally induced circadian disruption.

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          The online version of this article (doi:10.1007/s11357-012-9502-y) contains supplementary material, which is available to authorized users.

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          Most cited references59

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          Sleep complaints among elderly persons: an epidemiologic study of three communities.

          The frequencies of five common sleep complaints--trouble falling asleep, waking up, awaking too early, needing to nap and not feeling rested--were assessed in over 9,000 participants aged 65 years and older in the National Institute on Aging's multicentered study entitled "Established Populations for Epidemiologic Studies of the Elderly" (EPESE). Less than 20% of the participants in each community rarely or never had any complaints, whereas over half reported at least one of these complaints as occurring most of the time. Between 23% and 34% had symptoms of insomnia, and between 7% and 15% percent rarely or never felt rested after waking up in the morning. In multivariate analyses, sleep complaints were associated with an increasing number of respiratory symptoms, physical disabilities, nonprescription medications, depressive symptoms and poorer self-perceived health. Sleep disturbances, particularly among older persons, oftentimes may be secondary to coexisting diseases. Determining the prevalence of specific sleep disorders, independent of health status, will require the development of more sophisticated and objective measures of sleep disturbances.
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            Disruption of circadian clocks has ramifications for metabolism, brain, and behavior.

            Circadian (daily) rhythms are present in almost all plants and animals. In mammals, a brain clock located in the hypothalamic suprachiasmatic nucleus maintains synchrony between environmental light/dark cycles and physiology and behavior. Over the past 100 y, especially with the advent of electric lighting, modern society has resulted in a round-the-clock lifestyle, in which natural connections between rest/activity cycles and environmental light/dark cycles have been degraded or even broken. Instances in which rapid changes to sleep patterns are necessary, such as transmeridian air travel, demonstrate negative effects of acute circadian disruption on physiology and behavior. However, the ramifications of chronic disruption of the circadian clock for mental and physical health are not yet fully understood. By housing mice in 20-h light/dark cycles, incongruous with their endogenous ∼24-h circadian period, we were able to model the effects of chronic circadian disruption noninvasively. Housing in these conditions results in accelerated weight gain and obesity, as well as changes in metabolic hormones. In the brain, circadian-disrupted mice exhibit a loss of dendritic length and decreased complexity of neurons in the prelimbic prefrontal cortex, a brain region important in executive function and emotional control. Disrupted animals show decreases in cognitive flexibility and changes in emotionality consistent with the changes seen in neural architecture. How our findings translate to humans living and working in chronic circadian disruption is unknown, but we believe that this model can provide a foundation to understand how environmental disruption of circadian rhythms impacts the brain, behavior, and physiology.
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              Aerobic exercise improves self-reported sleep and quality of life in older adults with insomnia.

              To assess the efficacy of moderate aerobic physical activity with sleep hygiene education to improve sleep, mood and quality of life in older adults with chronic insomnia. Seventeen sedentary adults aged >or=55 years with insomnia (mean age 61.6 [SD±4.3] years; 16 female) participated in a randomized controlled trial comparing 16 weeks of aerobic physical activity plus sleep hygiene to non-physical activity plus sleep hygiene. Eligibility included primary insomnia for at least 3 months, habitual sleep duration 5. Outcomes included sleep quality, mood and quality of life questionnaires (PSQI, Epworth Sleepiness Scale [ESS], Short-form 36 [SF-36], Center for Epidemiological Studies Depression Scale [CES-D]). The physical activity group improved in sleep quality on the global PSQI (p<.0001), sleep latency (p=.049), sleep duration (p=.04), daytime dysfunction (p=.027), and sleep efficiency (p=.036) PSQI sub-scores compared to the control group. The physical activity group also had reductions in depressive symptoms (p=.044), daytime sleepiness (p=.02) and improvements in vitality (p=.017) compared to baseline scores. Aerobic physical activity with sleep hygiene education is an effective treatment approach to improve sleep quality, mood and quality of life in older adults with chronic insomnia.
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                Author and article information

                Contributors
                +1-413-2475261 , +1-413-5853786 , mharring@smith.edu
                Journal
                Age (Dordr)
                Age
                Springer Netherlands (Dordrecht )
                0161-9152
                1574-4647
                23 January 2013
                23 January 2013
                December 2013
                : 35
                : 6
                : 2137-2152
                Affiliations
                [ ]Neuroscience Program, Smith College, Northampton, MA 01063 USA
                [ ]Mathematics Department, Amherst College, Amherst, MA 01002 USA
                [ ]Medway School of Pharmacy, University of Kent, Central Avenue, Chatham, Kent, ME4 4TB UK
                [ ]School of Psychology, University of Glasgow, Glasgow, G12 8QB Scotland UK
                Article
                9502
                10.1007/s11357-012-9502-y
                3825002
                23340916
                24e62e06-fb81-48a9-b67c-94919d29dab2
                © The Author(s) 2013

                Open Access This article is distributed under the terms of the Creative Commons Attribution License which permits any use, distribution, and reproduction in any medium, provided the original author(s) and the source are credited.

                History
                : 2 July 2012
                : 5 December 2012
                Categories
                Article
                Custom metadata
                © American Aging Association 2013

                Geriatric medicine
                circadian,exercise,wheel,suprachiasmatic nucleus,thymus,esophagus,spleen
                Geriatric medicine
                circadian, exercise, wheel, suprachiasmatic nucleus, thymus, esophagus, spleen

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