Primed to Sleep: The Dynamics of Synaptic Plasticity Across Brain States.

Julie Seibt,Marcos G Frank

doi:10.3389/fnsys.2019.00002

Julie Seibt, Marcos G Frank

Open Access

https://doi.org/10.3389/fnsys.2019.00002

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Abstract

It is commonly accepted that brain plasticity occurs in wakefulness and sleep. However, how these different brain states work in concert to create long-lasting changes in brain circuitry is unclear. Considering that wakefulness and sleep are profoundly different brain states on multiple levels (e.g., cellular, molecular and network activation), it is unlikely that they operate exactly the same way. Rather it is probable that they engage different, but coordinated, mechanisms. In this article we discuss how plasticity may be divided across the sleep–wake cycle, and how synaptic changes in each brain state are linked. Our working model proposes that waking experience triggers short-lived synaptic events that are necessary for transient plastic changes and mark (i.e., ‘prime’) circuits and synapses for further processing in sleep. During sleep, synaptic protein synthesis at primed synapses leads to structural changes necessary for long-term information storage.

Highlights

We propose that waking experience promotes two parallel events that recruit shared mechanisms: transient plastic changes and the priming of neurons for further modification in sleep
We propose that periodic reactivation of task-specific circuits during NREM oscillations, combined with priming during wake, provides an efficient mechanism for Plasticity Related Products (PRPs) capture in a neuron- and synapse-specific manner
While experience-dependent PRPs transcription occurs predominantly during wake, the final translation of PRPs transcripts necessary for synapse-specific structural plasticity stabilization occurs during REM sleep (Figure 3B)

Summary

Introduction

We propose that waking experience promotes two parallel events that recruit shared mechanisms: transient plastic changes and the priming of neurons for further modification in sleep. Later reactivation (within hours) of the neuronal network surrounding tagged synapses promotes the capture and translation of Plasticity Related Products (PRPs) leading to a final stabilization of synaptic weight change while maintaining input-specificity (Redondo and Morris, 2011).

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