期刊名称：Proceedings of the National Academy of Sciences
印刷版ISSN：0027-8424
电子版ISSN：1091-6490
出版年度：2022
卷号：119
期号：26
DOI：10.1073/pnas.2122515119
语种：English
出版社：The National Academy of Sciences of the United States of America
摘要：Significance
This work introduces a noninvasive approach to understanding information processing during sleep. Our results demonstrate that slow oscillations (SOs) provide the temporal-topographical event framework whereby long-range information flow increases dramatically compared to the relatively local activity patterns of the rest of sleep. The findings represent a conceptual leap in understanding how SOs unlock memory consolidation in a broken-down network, which is by promoting long-range, effective communication. This research will promote further investigations of understanding how brain oscillations alone and in nested rhythms promote network communication, as well as investigate how these properties vary and predict patterns of deficits in clinical populations and aging humans.
A prominent and robust finding in cognitive neuroscience is the strengthening of memories during nonrapid eye movement (NREM) sleep, with slow oscillations (SOs;<1Hz) playing a critical role in systems-level consolidation. However, NREM generally shows a breakdown in connectivity and reduction of synaptic plasticity with increasing depth: a brain state seemingly unfavorable to memory consolidation. Here, we present an approach to address this apparent paradox that leverages an event-related causality measure to estimate directional information flow during NREM in epochs with and without SOs. Our results confirm that NREM is generally a state of dampened neural communication but reveals that SOs provide two windows of enhanced large-scale communication before and after the SO trough. These peaks in communication are significantly higher when SOs are coupled with sleep spindles compared with uncoupled SOs. To probe the functional relevance of these SO-selective peaks of information flow, we tested the temporal and topographic conditions that predict overnight episodic memory improvement. Our results show that global, long-range communication during SOs promotes sleep-dependent systems consolidation of episodic memories. A significant correlation between peaks of information flow and memory improvement lends predictive validity to our measurements of effective connectivity. In other words, we were able to predict memory improvement based on independent electrophysiological observations during sleep. This work introduces a noninvasive approach to understanding information processing during sleep and provides a mechanism for how systems-level brain communication can occur during an otherwise low connectivity sleep state. In short, SOs are a gating mechanism for large-scale neural communication, a necessary substrate for systems consolidation and long-term memory formation.
关键词：eneffective connectivityslow oscillationsmemory consolidationcausal information flowSO-spindle coupling
