Memory corticalization triggered by REM sleep: mechanisms of cellular and systems consolidation

Abstract

Once viewed as a passive physiological state, sleep is a heterogeneous and complex sequence of brain states with essential effects on synaptic plasticity and neuronal functioning. Rapid-eye-movement (REM) sleep has been shown to promote calcium-dependent plasticity in principal neurons of the cerebral cortex, both during memory consolidation in adults and during post-natal development. This article reviews the plasticity mechanisms triggered by REM sleep, with a focus on the emerging role of kinases and immediate-early genes for the progressive corticalization of hippocampus-dependent memories. The body of evidence suggests that memory corticalization triggered by REM sleep is a systemic phenomenon with cellular and molecular causes.

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

“…REM sleep network activity (e.g., theta oscillations, PGO waves) likely participates for the stimulation of widespread translation activation. Transcription of translation factors and some IEGs (e.g., Egr1/Zif268) during NREM and REM sleep may also help sustained synaptic remodeling (i.e., structural plasticity) via replenishment of PRPs across NREM-REM cycles (Almeida-Filho et al, 2018).…”

“…We add to the proposed function of NREM sleep oscillations in that we suggest PRP capture at selected synapses in reactivated circuits (regardless of brain structures). In contrast to other ideas positing different roles for REM and NREM sleep in plasticity (Crick and Mitchison, 1983; Giuditta et al, 1995; Rasch and Born, 2013; Giuditta, 2014; Almeida-Filho et al, 2018; Navarro-Lobato and Genzel, 2018), our ideas are based on current ideas about metaplasticity, rather than uniform processes that drive plasticity in one (net) direction, or transcriptional events only. Our model also differs in the description of priming mechanisms that link plastic changes in waking with subsequent changes in sleep.…”

“…For example, synaptic potentiation, which has been proposed to occur during either wake (Tononi and Cirelli, 2014) or sleep (Rasch and Born, 2013), is a dynamic process that is initially labile and relies on specific molecular mechanisms for its long lasting expression. There is also an abundant literature showing that both wake and sleep promote molecular mechanisms of synaptic plasticity (for recent reviews, see da Costa Souza and Ribeiro, 2015; Puentes-Mestril and Aton, 2017; Almeida-Filho et al, 2018; Navarro-Lobato and Genzel, 2018). What is less clear is how the mechanisms of plasticity induction and consolidation are divided across brain states.…”

REM sleep promotes experience-dependent dendritic spine elimination in the mouse cortex

“…Mammalian sleep cycles compose of non-rapid eye movement (NREM) sleep and rapid eye movement (REM) sleep 1,2 . Many lines of evidence suggest that sleep is important for regulating neuronal plasticity during brain development and after learning [3][4][5][6][7][8][9] . For example, NREM sleep has been shown to promote synaptic potentiation 10 , synapse formation 11 , and synaptic weakening after wakefulness [12][13][14] .…”

Sleeping through brain excitation and inhibition

“…REM sleep's function has remained elusive since its discovery in 1952 by Eugene Aserinsky, with proposals ranging from emotional processing to problem-solving and memory corticalization 14,15 . Tamaki and colleagues' new approach enables us to take a fresh look at this old problem by taking into consideration the balance between excitatory and inhibitory neurotransmission and its effects on consolidation.…”