Sleep-Dependent Oscillatory Synchronization: A Role in Fear Memory Consolidation.

Subimal Datta,Michael S Totty,Logan A Chesney,Phillip A Geist

doi:10.3389/fncir.2017.00049

Subimal Datta, Michael S Totty + Show 2 more

Open Access

https://doi.org/10.3389/fncir.2017.00049

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Abstract

Sleep plays an important role in memory consolidation through the facilitation of neuronal plasticity; however, how sleep accomplishes this remains to be completely understood. It has previously been demonstrated that neural oscillations are an intrinsic mechanism by which the brain precisely controls neural ensembles. Inter-regional synchronization of these oscillations is also known to facilitate long-range communication and long-term potentiation (LTP). In the present study, we investigated how the characteristic rhythms found in local field potentials (LFPs) during non-REM and REM sleep play a role in emotional memory consolidation. Chronically implanted bipolar electrodes in the lateral amygdala (LA), dorsal and ventral hippocampus (DH, VH), and the infra-limbic (IL), and pre-limbic (PL) prefrontal cortex were used to record LFPs across sleep-wake activity following each day of a Pavlovian cued fear conditioning paradigm. This resulted in three principle findings: (1) theta rhythms during REM sleep are highly synchronized between regions; (2) the extent of inter-regional synchronization during REM and non-REM sleep is altered by FC and EX; (3) the mean phase difference of synchronization between the LA and VH during REM sleep predicts changes in freezing after cued fear extinction. These results both oppose a currently proposed model of sleep-dependent memory consolidation and provide a novel finding which suggests that the role of REM sleep theta rhythms in memory consolidation may rely more on the relative phase-shift between neural oscillations, rather than the extent of phase synchronization.

Highlights

It is well-established that sleep plays an important role in learning and memory (Stickgold, 2005; Datta, 2006; Maquet, 2007; Diekelmann and Born, 2010; Ravassard et al, 2016; Li et al, 2017)
The principal findings of this study are as follows: (1) theta rhythms during rapid-eye movement sleep (REM) sleep are highly synchronized between regions; (2) the extent of inter-regional synchronization during REM and nonREM sleep is altered by fear conditioning (FC) and EX; (3) the mean phase difference of synchronization between the lateral amygdala (LA) and ventral and dorsal hippocampus (VH) during REM sleep predicts changes in freezing after cued fear extinction
These results are discussed to highlight a novel mechanism through which REM sleep theta rhythms may facilitate neural plasticity

Summary

INTRODUCTION

It is well-established that sleep plays an important role in learning and memory (Stickgold, 2005; Datta, 2006; Maquet, 2007; Diekelmann and Born, 2010; Ravassard et al, 2016; Li et al, 2017). Phasic activity during REM sleep and spindle activity during non-REM sleep has been heavily implicated in successful memory consolidation (Datta, 2000; Datta et al, 2004; Girardeau et al, 2009; Fogel and Smith, 2011) These effects on memory have been largely attributed to changes in neuronal plasticity, such as long-term potentiation (LTP), long-term depression (LTD), and other cellular modifications (Bramham et al, 1994; Datta et al, 2008; Shaffery et al, 2012; Dumoulin Bridi et al, 2015; Frank, 2015; Hennies et al, 2016; Ravassard et al, 2016; Li et al, 2017). This suggests that the role of oscillatory synchronization in memory consolidation may rely more on the relative phase-shift between neural oscillations, rather than the extent of phase synchronization

MATERIALS AND METHODS

RESULTS

DISCUSSION