Changes in Brain Oscillatory Dynamics in Elderly Adults as a Consequence of Natural Aging

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Abstract

Abstract The oscillatory nature of slow waves during non-rapid eye movement (NREM) sleep has recently been proposed as crucial for the glymphatic system, facilitating the clearance of metabolic waste from the brain. While aging-related reductions in slow wave quantity and amplitude are well-documented and linked to this cleansing function, we propose that the rhythmic dynamics in which slow waves occur may also play a critical role. Thus, we introduce a novel classification of slow waves based on their dynamics into isolated waves and oscillation trains. Using overnight EEG recordings from young and elderly adults, we compared the proportions of each wave type. Additionally, we analyzed train composition, including the proportion of slow waves that initiate a train (lead waves) and the lengths of the trains. Elderly adults exhibited a higher prevalence of isolated waves and a lower proportion of oscillation trains. Moreover, while elderly adults showed a higher proportion of lead waves, their oscillation trains were shorter. We propose that natural aging may result in a less oscillatory brain state, potentially impairing cerebrospinal fluid pulsation and reducing the brain’s efficiency in cleansing pathogenic substances during sleep.
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Aging disrupts the temporal organization of slow oscillations beyond density reduction | Research Square window.SnipcartSettings = { analytics: { enabled: false } }; (function() { var accessVector = localStorage.getItem('access_vector') || ''; window.dataLayer = window.dataLayer || []; if (accessVector) { window.dataLayer.push({ user: { profile: { profileInfo: { snid: accessVector } } } }); } })(); (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0],j=d.createElement(s),dl=l!='dataLayer'?'&l='+l:'';j.async=true;j.src='https://www.googletagmanager.com/gtm.js?id='+i+dl;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-K279D39R'); Browse Preprints In Review Journals COVID-19 Preprints AJE Video Bytes Research Tools Research Promotion AJE Professional Editing AJE Rubriq About Preprint Platform In Review Editorial Policies Our Team Advisory Board Help Center Sign In Submit a Preprint Cite Share Download PDF Research Article Aging disrupts the temporal organization of slow oscillations beyond density reduction Lucila Capurro, Michael Radloff, María Cecilia González, María Laura Gorosito, and 3 more This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-5655250/v2 This work is licensed under a CC BY 4.0 License Status: Posted Version 2 posted You are reading this latest preprint version Show more versions Abstract Macroscopic and rhythmic brain oscillations have recently been shown to play a crucial role in glymphatic function by promoting cerebrospinal fluid flow and facilitating the clearance of metabolic waste. While age-related reductions in the number and amplitude of slow oscillations (SOs; 0.5-1 Hz) are well documented and associated with impaired clearance, little is known about how aging affects the temporal structure of these oscillations. Here, we propose that the rhythmic dynamics with which SOs occur represent a critical, yet overlooked, feature supporting glymphatic function. We introduce a novel classification of SOs based on their temporal organization, distinguishing isolated SOs from trains of consecutive oscillations according to inter-SO intervals. Using overnight electroencephalographic recordings from 57 young and 51 elderly adults across three independent datasets, we compared the proportions of isolated and consecutive SOs as well as the distribution of train lengths. Elderly adults displayed a significantly higher proportion of isolated SOs and shorter oscillatory trains than young adults, even after controlling for SO density and stage composition. Temporal shuffling procedures and analyses of density-matched epochs further confirmed that these differences cannot be attributed solely to density, but instead reflect a genuine age-related loss of rhythmicity. These findings reveal that natural aging not only reduces the amount and amplitude of SOs but also disrupts their temporal regularity. This alteration may weaken the sustained ionic currents that drive cerebrospinal fluid flow, compromise the efficiency of metabolic clearance during sleep, and thereby contribute to increased vulnerability to age-related neurodegenerative processes. Biological sciences/Neuroscience Biological sciences/Physiology/Ageing sleep aging electrophysiological changes slow oscillations Full Text Additional Declarations The authors declare no competing interests. Supplementary Files SI.pdf Cite Share Download PDF Status: Posted Version 2 posted You are reading this latest preprint version Show more versions Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. As a division of Research Square Company, we’re committed to making research communication faster, fairer, and more useful. We do this by developing innovative software and high quality services for the global research community. Our growing team is made up of researchers and industry professionals working together to solve the most critical problems facing scientific publishing. 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