Slow oscillations promote long range effective communication: the key for memory consolidation in a broken down network

Abstract

One of the most prominent and robust findings in cognitive neuroscience is the strengthening of memories during non-rapid eye movement (NREM) sleep, with slow oscillations (SOs, < 1Hz) playing a critical role in systems-level consolidation. However, NREM is a sleep period generally showing a breakdown in connectivity and reduction of synaptic plasticity with increasing depth: a brain state seemingly unfavorable to memory consolidation. Here, we present a novel approach to address this apparent paradox that leverages an event-related causality measure to estimate directional information flow during NREM sleep 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 promote sleep-dependent systems consolidation of episodic memories. A significant correlation between peaks of information flow and memory improvement lends a predictive validity to our measurements of effective connectivity. In other words, we were able to predict memory improvement on the basis of independent electrophysiological observations during sleep. This work introduces a non-invasive approach to understanding information processing during sleep, a behavioral stage whose function, until now, has been understood only after synaptic reorganization after waking from sleep. Our findings provide a mechanism for how systems-level brain communication can occur during an otherwise low connectivity sleep state, indicating that SOs are a gating mechanism for large-scale neural communication, which is the necessary substrate for systems consolidation and long-term memory formation.