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

Abstract

Sleep plays an important role in consolidation of recent memories. However, the mechanisms of consolidation remain poorly understood. In this study, using a realistic computational model of the thalamocortical network, we demonstrated that sleep spindles (the hallmark of N2 stage sleep) and slow oscillations (the hallmark of N3 stage sleep) both facilitate spike sequence replay as necessary for consolidation. When multiple memories were trained, the local nature of spike sequence replay during spindles allowed replay of the memories independently, while during slow oscillations replay of the weak memory was competing to the strong memory replay. This led to the weak memory extinction unless when sleep spindles (N2 sleep) preceded slow oscillations (N3 sleep), as observed during natural sleep. 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.peer-reviewed) is the author/funder. All rights reserved. No reuse allowed without permission.The copyright holder for this preprint (which was not . http://dx.doi.org/10.1101/153007 doi: bioRxiv preprint first posted online 3 Significant StatementNumerous studies suggest importance of NREM sleep rhythms -spindles and slow oscillations -in sleep related memory consolidation. However, synaptic mechanisms behind the role of these rhythms in memory and learning are still unknown. Our new study predicts that sleep replay -the neuronal substrate of memory consolidation -is organized within the sleep spindles and coordinated by the Down to Up state transitions of the slow oscillation. For multiple competing memories, slow oscillations facilitated only strongest memory replay, while sleep spindles allowed a consolidation of the multiple competing memories independently. Our study predicts how the basic structure of the natural sleep stages provides an optimal environment for consolidation of multiple memories.peer-reviewed)

Can sleep protect memories from catastrophic forgetting?

“…Network architecture. The thalamocortical network model used in this study has been previously described in detail Wei et al, 2016;Wei et al, 2018). Briefly, our network was comprised of a thalamus which contained 100 thalamocortical relay neurons (TC) and 100 reticular neurons (RE), and a cortex containing 500 pyramidal neurons (PY) and Intrinsic currents.…”

“…A detailed description of the individual currents can be found in our previous studies Wei et al, 2018).…”

“…Sleep has been suggested to play an important role in memory consolidation (Paller and Voss, 2004;Walker and Stickgold, 2004;Rasch and Born, 2013;Stickgold, 2013;Wei et al, 2016;Wei et al, 2018). Specifically, the role of stage 2 (N2) and stage 3 (N3) Non Rapid Eye Movement (NREM) sleep has been shown to help with the consolidation of newly encoded memories (Paller and Voss, 2004;Walker and Stickgold, 2004;Rasch and Born, 2013;Stickgold, 2013).…”

“…Sleep may enhance memory consolidation through repeated memory reactivation or replay during characteristic sleep rhythms such as spindles and slow oscillations (Paller and Voss, 2004;Clemens et al, 2005;Marshall et al, 2006;Rasch and Born, 2013;Wei et al, 2016;Ladenbauer et al, 2017;Wei et al, 2018). Memory replay during deep N3 sleep could help strengthen previously stored memories and prevent future interference.…”

Shaping memory consolidation via targeted memory reactivation during sleep

“…During NREM sleep, SOs synchronize neuronal activity both in the neocortex and in other regions relevant to memory consolidation, such as the thalamus and the hippocampus, where thalamocortical spindles and SWR originate, respectively . Thus, SOs may provide a global temporal frame whereby the depolarizing up‐phases repeatedly drive the reactivation of memories in hippocampal circuits in parallel with thalamocortical spindles, enabling these signals to reach the neocortical networks while still in the depolarizing up‐state . The memory traces are also locally potentiated by sleep spindles, which seem to induce local plasticity in selected neuronal circuits that were previously reactivated .…”