Differential roles of sleep spindles and sleep slow oscillations in memory consolidation.

Yina Wei,Maxim Bazhenov,Giri P Krishnan,Maxim Komarov,Francesco P Battaglia

doi:10.1371/journal.pcbi.1006322

Yina Wei, Maxim Bazhenov + Show 3 more

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https://doi.org/10.1371/journal.pcbi.1006322

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Abstract

Sleep plays an important role in the consolidation of recent memories. However, the cellular and synaptic mechanisms of consolidation during sleep remain poorly understood. In this study, using a realistic computational model of the thalamocortical network, we tested the role of Non-Rapid Eye Movement (NREM) sleep in memory consolidation. We found that sleep spindles (the hallmark of N2 stage sleep) and slow oscillations (the hallmark of N3 stage sleep) both promote replay of the spike sequences learned in the awake state and replay was localized at the trained network locations. Memory performance improved after a period of NREM sleep but not after the same time period in awake. When multiple memories were trained, the local nature of the spike sequence replay during spindles allowed replay of the distinct memory traces independently, while slow oscillations promoted competition that could prevent replay of the weak memories in a presence of the stronger memory traces. This could lead to extinction of the weak memories unless when sleep spindles (N2 sleep) preceded slow oscillations (N3 sleep), as observed during the natural sleep cycle. Our study presents a mechanistic explanation for the role of sleep rhythms in memory consolidation and proposes a testable hypothesis how the natural structure of sleep stages provides an optimal environment to consolidate memories.

Highlights

Sleep is believed to play an important role in consolidating of the recently learned knowledge [1,2,3,4]
We found that sleep spindles and slow oscillations both promote replay of the spike sequences learned in the awake state and replay was localized at the trained network locations
Two major sleep rhythms are observed during sleep–spindles and slow oscillations–and studies reported the importance of these rhythms in sleep-related memory consolidation

Summary

Introduction

Sleep is believed to play an important role in consolidating of the recently learned knowledge [1,2,3,4]. NREM sleep was shown to be important for consolidating declarative (hippocampus-dependent) memories [19, 20], human studies suggest that NREM sleep may be involved in the consolidation of the procedural (hippocampus-independent) memories, e.g. simple motor tasks [21], or finger-sequence tapping tasks [22, 23]. Together studies suggest that NREM sleep is involved in the consolidation of the simple motor tasks, while REM sleep may become critical for learning the more complex memory tasks (see, e.g., [28]). A recent animal study [9] of consolidation of the procedural (skilled upper-limb) memory reported that reactivation of the neural activity was closely linked to the bursts of spindle activity and the waves of slow oscillation during NREM sleep. It was hypothesized that NREM sleep contributes to the consolidation of memories through the replay within the neocortex of the spike sequences associated with recent learning, the mechanisms behind sequence replay are poorly understood

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