Changes in sleep EEG with aging in humans and rodents

Abstract

Sleep is one of the most ubiquitous but also complex animal behaviors. It is regulated at the global, systems level scale by circadian and homeostatic processes. Across the 24-h day, distribution of sleep/wake activity differs between species, with global sleep states characterized by defined patterns of brain electric activity and electromyography. Sleep patterns have been most intensely investigated in mammalian species. The present review begins with a brief overview on current understandings on the regulation of sleep, and its interaction with aging. An overview on age-related variations in the sleep states and associated electrophysiology and oscillatory events in humans as well as in the most common laboratory rodents follows. We present findings observed in different studies and meta-analyses, indicating links to putative physiological changes in the aged brain. Concepts requiring a more integrative view on the role of circadian and homeostatic sleep regulatory mechanisms to explain aging in sleep are emerging.

Keywords: Aging; EEG; Electrophysiology; Human; Rodents; Sleep.

Fig. 1

Comparison of the normal sleep architecture during the inactive sleep period of the three species discussed in this review. Lights out was at 0 h for the human subject and sleep was recorded during 8 h. The rodent species were held on a 12:12 L:D regime, with lights on depicted at 0 h and sleep recorded through 12 h. Sleep architecture is determined from EEG and electromyography recordings. Note the typical difference in sleep cycle lengths across species. W wake, REM rapid eye movement sleep, stages N1–N3 in human sleep; W wake, R rapid eye movement sleep, N non-rapid eye movement sleep in the rodent species. Rat data were kindly provided by Gina R. Poe, University of California, Los Angeles (UCLA)

Fig. 2

Age-related modulations in slow wave activity and sleep spindle density in humans predominate over frontal cortical regions. a Representative head plots of slow wave activity (< 4.6 Hz, absolute power as measured in μV²; left) and density (number of SW/min; right); warmer colors indicate higher values. The middle topoplots reveal the topographical differences in EEG activity between young and older human adults in which the cooler colors indicate greater differences. b Differences in the aged EEG activity in the fast sleep spindle density (13.5–15 Hz; bottom left) and slow sleep spindle density (12–13.5 Hz; bottom right). Figure taken and modified with permission from Mander and colleagues, Neuron (2017) 94 (1):19–36 [61]

Fig. 3

Age-related differences of sleep states within a sleep-wake cycle of undisturbed sleep in C57BL/6J mice. Diagrams show the time course of wake (left), NREMS (central), and REMS (right) in percentage (mean ± SEM) across a 24-h recording period. White and gray top bars indicate the light (inactive) and dark (active) phases, correspondingly. Comparisons are made between early adults (EA, blue), late adulthood (LA, cyan), and old adults (OA, purple) with significant differences comparing EA vs LA (blue), LA vs OA (cyan), and EA vs OA (purple). Data indicate that old mice had a significantly decreased wake and increased NREMS time as compared to younger animals, an effect that is more evident during their active phase. Figure taken and modified with permission from McKillop and colleagues, J Neurosci (2018) 38(16):3911–3928 [65]