Human REM sleep controls neural excitability in support of memory formation

Abstract

Sleep oscillations provide a key substrate to facilitate memory processing, the underlying mechanism of which may involve the overnight homeostatic regulation of plasticity at a synaptic and whole-network level. However, there remains a lack of human data demonstrating if and how sleep enhances memory consolidation and associated neural homeostasis. We combined intracranial recordings and scalp electroencephalography (EEG) in humans to reveal a new role for rapid eye movement (REM) sleep in promoting the homeostatic recalibration of optimal excitation/inhibition-balance. Moreover, the extent of this REM-sleep homeostatic recalibration predicted the success of overnight memory consolidation, expressly the modulation of hippocampal— neocortical excitability favoring remembering rather than forgetting. The findings describe a novel, fundamental role of human REM sleep in maintaining neural homeostasis, thereby enhancing long-term memory.

Spectral slope and Lempel-Ziv complexity as robust markers of brain states during sleep and wakefulness

“…In contrast, the narrowband complexity was not positively correlated with memory performance and even expressed a negative relationship on some electrodes. Since we observed a positive relationship between overnight decreases in resting state slopes and memory performance in another study (Lendner et al, 2022), we further assessed whether the overnight change in slope during the retrieval task is also correlated with sleep-dependent memory consolidation. However, we did not obtain a significant relationship, indicating that while flatter slopes during the retrieval were associated with slightly better memory performance in the according session, overnight changes in the slope or complexity were not related to performance changes in our study.…”

Resting-state aperiodic neural activity as a novel objective marker of daytime somnolence

“…The slope of the aperiodic component has been recently described as a marker of homeostatic sleep need 50 , based on theoretical accounts of neural activity leading to sleep need 51,52 and experimental results in animals and humans which have delineated processes of synaptic regulation as a function of sleep [53][54][55] . Broadly, as the individual progresses through wakefulness, incidental information processing necessarily occurs, and this leads to saturation of synaptic connections in cortex.…”

Considerations towards a neurobiologically-informed EEG measurement of sleepiness

“…Experimental support has been found for a role of all canonical frequency bands of brain activity as modulated by, or markers of, sleepiness [32][33][34][35][36][37][38] . There have also been findings in support of other elements of the EEG in relation to sleepiness, such as event-related potential (ERP) component amplitude changes [39] , microstates and phase locking values between various regions/frequencies [40] , informational complexity markers [41,42] and aperiodic indices [43,44] . That is, sleepiness may be represented in a diffuse manner in the brain, at least in terms of objective measurement via the EEG.…”

“…Importantly, recent experimental work in sleep disordered patients has demonstrated that the aperiodic component of the EEG can be used to classify insomnia patients from noninsomniac controls [41] and to differentiate both patients diagnosed with excessive daytime somnolence and sub-clinical cases of the same from non-sleepy controls [53] . These can be seen as applied extensions of the work of Lendner et al [43,44] , who found that aperiodic measures could be used to differentiate between wakeful and sleep states, as well as between different sleep stages within the individual. Further, in line with predictions made in the Synaptic Homeostasis Hypothesis [23] and experimental data supporting the theory [47,54] , neuronal excitability was shown to reduce across a night of sleep.…”