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      A pilot time-in-bed restriction intervention behaviorally enhances slow-wave activity in older adults

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          Abstract

          Introduction:

          Identifying intervention methods that target sleep characteristics involved in memory processing is a priority for the field of cognitive aging. Older adults with greater sleep efficiency and non-rapid eye movement slow-wave activity (SWA) (0.5–4 Hz electroencephalographic activity) tend to exhibit better memory and cognitive abilities. Paradoxically, long total sleep times are consistently associated with poorer cognition in older adults. Thus, maximizing sleep efficiency and SWA may be a priority relative to increasing mere total sleep time. As clinical behavioral sleep treatments do not consistently enhance SWA, and propensity for SWA increases with time spent awake, we examined with a proof-of concept pilot intervention whether a greater dose of time-in-bed (TiB) restriction (75% of habitual TiB) would increase both sleep efficiency and SWA in older adults with difficulties staying asleep without impairing memory performance.

          Methods:

          Participants were adults ages 55–80 with diary-reported sleep efficiency <90% and wake after sleep onset (WASO) >20 min. Sleep diary, actigraphy, polysomnography (PSG), and paired associate memory acquisition and retention were assessed before and after a week-long TiB restriction intervention ( n = 30). TiB was restricted to 75% of diary-reported habitual TiB. A comparison group of n = 5 participants repeated assessments while following their usual sleep schedule to obtain preliminary estimates of effect sizes associated with repeated testing.

          Results:

          Subjective and objective sleep measures robustly improved in the TiB restriction group for sleep quality, sleep depth, sleep efficiency and WASO, at the expense of TiB and time spent in N1 and N2 sleep. As hypothesized, SWA increased robustly with TiB restriction across the 0.5–4 Hz range, as well as subjective sleep depth, subjective and objective WASO. Despite increases in sleepiness ratings, no impairments were found in memory acquisition or retention.

          Conclusion:

          A TiB restriction dose equivalent to 75% of habitual TiB robustly increased sleep continuity and SWA in older adults with sleep maintenance difficulties, without impairing memory performance. These findings may inform long-term behavioral SWA enhancement interventions aimed at improving memory performance and risk for cognitive impairments.

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          Most cited references47

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          The two-process model of sleep regulation: a reappraisal.

          In the last three decades the two-process model of sleep regulation has served as a major conceptual framework in sleep research. It has been applied widely in studies on fatigue and performance and to dissect individual differences in sleep regulation. The model posits that a homeostatic process (Process S) interacts with a process controlled by the circadian pacemaker (Process C), with time-courses derived from physiological and behavioural variables. The model simulates successfully the timing and intensity of sleep in diverse experimental protocols. Electrophysiological recordings from the suprachiasmatic nuclei (SCN) suggest that S and C interact continuously. Oscillators outside the SCN that are linked to energy metabolism are evident in SCN-lesioned arrhythmic animals subjected to restricted feeding or methamphetamine administration, as well as in human subjects during internal desynchronization. In intact animals these peripheral oscillators may dissociate from the central pacemaker rhythm. A sleep/fast and wake/feed phase segregate antagonistic anabolic and catabolic metabolic processes in peripheral tissues. A deficiency of Process S was proposed to account for both depressive sleep disturbances and the antidepressant effect of sleep deprivation. The model supported the development of novel non-pharmacological treatment paradigms in psychiatry, based on manipulating circadian phase, sleep and light exposure. In conclusion, the model remains conceptually useful for promoting the integration of sleep and circadian rhythm research. Sleep appears to have not only a short-term, use-dependent function; it also serves to enforce rest and fasting, thereby supporting the optimization of metabolic processes at the appropriate phase of the 24-h cycle.
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            Sleep and Human Aging.

            Older adults do not sleep as well as younger adults. Why? What alterations in sleep quantity and quality occur as we age, and are there functional consequences? What are the underlying neural mechanisms that explain age-related sleep disruption? This review tackles these questions. First, we describe canonical changes in human sleep quantity and quality in cognitively normal older adults. Second, we explore the underlying neurobiological mechanisms that may account for these human sleep alterations. Third, we consider the functional consequences of age-related sleep disruption, focusing on memory impairment as an exemplar. We conclude with a discussion of a still-debated question: do older adults simply need less sleep, or rather, are they unable to generate the sleep that they still need?
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              Sleep-dependent memory triage: evolving generalization through selective processing.

              The brain does not retain all the information it encodes in a day. Much is forgotten, and of those memories retained, their subsequent evolution can follow any of a number of pathways. Emerging data makes clear that sleep is a compelling candidate for performing many of these operations. But how does the sleeping brain know which information to preserve and which to forget? What should sleep do with that information it chooses to keep? For information that is retained, sleep can integrate it into existing memory networks, look for common patterns and distill overarching rules, or simply stabilize and strengthen the memory exactly as it was learned. We suggest such 'memory triage' lies at the heart of a sleep-dependent memory processing system that selects new information, in a discriminatory manner, and assimilates it into the brain's vast armamentarium of evolving knowledge, helping guide each organism through its own, unique life.
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                Author and article information

                Journal
                9918451286706676
                51881
                Front Sleep
                Front Sleep
                Frontiers in sleep
                2813-2890
                20 June 2024
                2024
                02 January 2024
                27 June 2024
                : 2
                : 1265006
                Affiliations
                [1 ]School of Medicine, University of Pittsburgh, Pittsburgh, PA, United States
                [2 ]Department of Psychiatry, University of Pittsburgh Medical Center, Pittsburgh, PA, United States
                [3 ]School of Nursing, University of Pittsburgh, Pittsburgh, PA, United States
                Author notes

                Author contributions

                KW: Conceptualization, Formal analysis, Funding acquisition, Investigation, Methodology, Resources, Supervision, Validation, Writing—original draft. RH: Formal analysis, Investigation, Visualization, Writing—original draft. YD: Formal analysis, Visualization, Writing—original draft. MS: Formal analysis, Writing—review & editing. KD: Formal analysis, Writing—original draft. AW: Formal analysis, Writing—original draft. CP: Investigation, Methodology, Supervision, Writing—review & editing, Project administration. MF: Data curation, Methodology, Software, Writing—review & editing. DB: Conceptualization, Methodology, Resources, Supervision, Writing—review & editing.

                [* ]CORRESPONDENCE: Kristine A. Wilckens, wilckenska@ 123456upmc.edu
                Article
                NIHMS2003344
                10.3389/frsle.2023.1265006
                11210605
                38938690
                62883fd8-45a7-481b-a7ed-6d191846a698

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

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                Categories
                Article

                behavioral slow-wave sleep enhancement,slow-oscillation,sleep restriction,memory retention,cognitive aging

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