Aging disrupts the temporal organization of slow oscillations beyond density reduction

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 supported 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.