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      Caudate Volume Mediates the Interaction between Total Sleep Time and Executive Function after Acute Exercise in Healthy Older Adults

      research-article
      a , b , a , c , b , b , d , e , a , c , a , c , *
      ,
      Brain Plasticity
      IOS Press
      Sleep, acute exercise, caudate, basal ganglia, mediation, older adults , the Stroop task, executive function

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          Abstract

          Although both exercise and sleep are significant lifestyle factors in cognitive aging, the interaction of these two factors with respect to cognition remains to be determined. Also, little is known regarding the role of the basal ganglia (BG) in cognitive aging despite its involvement in both sleep and executive function. The primary objective of this study was to investigate the interaction between sleep and acute exercise on executive function performance, and secondarily, to assess if BG volume mediates this interaction. Thirty healthy older adults (65.8±7.3 years) completed 30 minutes of seated rest or moderate-intensity cycling exercise on different days. Structural MRI was used to assess the volumes of BG components including caudate, putamen, and globus pallidus shortly after the experimental conditions. Approximately 90 minutes after each condition, the Stroop task was administered to measure executive function. To examine sleep, participants wore a wrist actigraph for 8.0±3.6 days prior to the first experimental session. Results revealed that while longer total sleep time (TST) was associated with shorter Stroop response time (RT), shorter TST was associated with longer RT after exercise, compared to rest, for both congruent ( p = 0.029) and incongruent ( p = 0.022) trials. Longer TST was correlated with greater caudate volume, and greater caudate volume was associated with exercise-related improvement in Stroop incongruent RT. Ultimately, we found that the association between longer sleep duration and faster processing speed after acute exercise was mediated by greater caudate volume. These findings suggest that TST is an important factor for acute exercise-induced cognitive improvements in older adults, and that our study is a first step in understanding the interactive effects of these important lifestyle factors in cognitive aging that might simultaneously be addressed to promote healthy cognitive aging. Future studies should examine the interactive effects of sleep and chronic exercise on cognitive function, and whether BG volume might also mediate this interaction.

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          Most cited references47

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          Automatic sleep/wake identification from wrist activity.

          The purpose of this study was to develop and validate automatic scoring methods to distinguish sleep from wakefulness based on wrist activity. Forty-one subjects (18 normals and 23 with sleep or psychiatric disorders) wore a wrist actigraph during overnight polysomnography. In a randomly selected subsample of 20 subjects, candidate sleep/wake prediction algorithms were iteratively optimized against standard sleep/wake scores. The optimal algorithms obtained for various data collection epoch lengths were then prospectively tested on the remaining 21 subjects. The final algorithms correctly distinguished sleep from wakefulness approximately 88% of the time. Actigraphic sleep percentage and sleep latency estimates correlated 0.82 and 0.90, respectively, with corresponding parameters scored from the polysomnogram (p < 0.0001). Automatic scoring of wrist activity provides valuable information about sleep and wakefulness that could be useful in both clinical and research applications.
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            Sleep disturbances and chronic disease in older adults: results of the 2003 National Sleep Foundation Sleep in America Survey.

            To assess the association between sleep problems and chronic disease in older adults. Self-reported standardized questionnaire data from 1506 community-dwelling men and women aged 55-84 years in the continental United States who completed a 20-min telephone interview when contacted from lists of randomly selected telephone numbers. A majority of the participants (83%) reported one or more of 11 medical conditions and nearly one in four elderly respondents (age 65-84 years) had major comorbidity (i.e. four or more conditions). Depression, heart disease, bodily pain and memory problems were associated with more prevalent symptoms of insomnia. Other conditions such as obesity, arthritis, diabetes, lung diseases, stroke and osteoporosis were associated with other sleep-related problems such as breathing pauses, snoring, daytime sleepiness, restless legs or insufficient sleep (<6 h nightly). Poll findings are consistent with epidemiological studies of sleep, aging and chronic disease. These results suggest that the sleep complaints common in older adults are often secondary to their comorbidities and not to aging per se. These types of studies may be useful in promoting sleep awareness among health professionals and among older adults, especially those with heart disease, depression, chronic bodily pain or major comorbidity.
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              The effect of acute exercise on serum brain-derived neurotrophic factor levels and cognitive function.

              Brain-derived neurotrophic factor (BDNF) is one of a family of neurotrophic factors that participates in neuronal transmission, modulation and plasticity. Previous studies using animals have demonstrated that acute and chronic exercise leads to increases in BDNF in various brain regions. To determine the effects of acute exercise on serum BDNF levels in humans, and to determine the relationship between exercise intensity and BDNF responses. Additionally, the relationship between changes in BDNF and cognitive function was examined. Fifteen subjects (25.4 +/- 1.01 yr; 11 male, 4 female) performed a graded exercise test (GXT) for the determination of VO2max and ventilatory threshold (VTh) on a cycle ergometer. On separate days, two subsequent 30-min endurance rides were performed at 20% below the VTh (VTh - 20) and at 10% above the VTh (VTh + 10). Serum BDNF and cognitive function were determined before and after the GXT and endurance rides with an enzyme-linked immunosorbent assay (ELISA) and the Stroop tests, respectively. The mean VO2max was 2805.8 +/- 164.3 mL x min(-1) (104.2 +/- 7.0% pred). BDNF values (pg x mL(-1)) increased from baseline (P<0.05) after exercise at the VTh + 10 (13%) and the GXT (30%). There was no significant change in BDNF from baseline after the VTh - 20. Changes in BDNF did not correlate with VO2max during the GXT, but they did correlate with changes in lactate (r=0.57; P<0.05). Cognitive function scores improved after all exercise conditions, but they did not correlate with BDNF changes. BDNF levels in humans are significantly elevated in response to exercise, and the magnitude of increase is exercise intensity dependent. Given that BDNF can transit the blood-brain barrier in both directions, the intensity-dependent findings may aid in designing exercise prescriptions for maintaining or improving neurological health.
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                Author and article information

                Journal
                Brain Plast
                Brain Plast
                BPL
                Brain Plasticity
                IOS Press (Nieuwe Hemweg 6B, 1013 BG Amsterdam, The Netherlands )
                2213-6304
                2213-6312
                27 November 2019
                26 December 2019
                2019
                : 5
                : 1 , Exercise Effects on Cognitive Function in Humans
                : 69-82
                Affiliations
                [a ]Department of Kinesiology, University of Maryland , College Park, MD, USA
                [b ]Department of Mental Health, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD
                [c ]Program in Neuroscience and Cognitive Science, University of Maryland , College Park , MD, USA
                [d ]Department of Psychiatry and Behavioral Sciences, Johns Hopkins School of Medicine, Baltimore, MD, USA
                [e ]Center on Aging and Health, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, USA
                Author notes
                [* ]Correspondence to: J. Carson Smith, PhD, Department of Kinesiology, University of Maryland, College Park, MD, 20742, USA. phone: +1 301 405 0344; fax: + 1 301 405 5578; E-mail: carson@ 123456umd.edu .
                Article
                BPL190087
                10.3233/BPL-190087
                6971824
                31970061
                cd71bdde-6730-447f-849f-9665e37dd905
                © 2019 – IOS Press and the authors. All rights reserved

                This is an open access article distributed under the terms of the Creative Commons Attribution Non-Commercial (CC BY-NC 4.0) License, which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

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                Research Report

                sleep,acute exercise,caudate,basal ganglia,mediation,older adults,the stroop task,executive function

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