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

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.

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

“…5). Consistent with the role of REM sleep in emotional memory processing [36][37][38][39][40][41][42][43] , a recall test 24 h after FC showed a reduced freezing response in mice subjected to SD or REMD (Fig. 3g).…”

“…Moreover, REMD impairs the consolidation of fear extinction memory in rats 41,42 and the attenuation of REM sleep theta rhythm in mice impairs fear contextual memory consolidation 43 . Together, these findings suggest that REM sleep has a general function in emotional memory consolidation in many species, including humans and rodents [36][37][38][39][40][41][42][43] , potentially involving experience-dependent synapse elimination as demonstrated here. Interestingly, in contrast to the rapid effect on FC-induced spine elimination, REM sleep has no significant effect on spine elimination within the first It has been shown that dendritic Ca 2+ spikes increase in the motor cortex during REM sleep and are involved in the pruning and strengthening of newly formed spines induced after motor training 19 .…”

Hippocampal Network Oscillations Rescue Memory Consolidation Deficits Caused by Sleep Loss

“…( Vecsey et al 2009 ; Aton et al 2009a ; Seibt et al 2012 ; Dumoulin et al 2015 ; Havekes et al 2016 ; Tudor et al 2016 )Recent findings have shown that coherent rhythms of activity between brain areas (e.g., between hippocampus and cortex) are associated with memory storage across a period of sleep ( Rothschild et al 2017 ; Totty et al 2017 ; Xia et al 2017 ). An unanswered question is how these oscillations are coordinated between thalamocortical circuits and the hippocampus.…”

The role of sleep in emotional processing: insights and unknowns from rodent research

“…Similarly, post-training pharmacological blockade of gapjunctions, which impairs theta oscillations, prevents the consolidation of contextual, but not cued, fear conditioning (Bissiere et al 2011), although the manipulation here wasn't restricted to REM sleep. Theta oscillations during REM sleep are therefore a good candidate for offline coordinated activity related to emotional processing (Genzel et al 2015;Totty et al 2017). REM sleep is modified after both appetitive and aversive training (Genzel et al 2015;Datta 2000), while total and selective REM sleep deprivations after training impairs emotional memory consolidation and prevents the related network reorganization (Rosier et al 2018;Graves et al 2003;Ravassard et al 2016;Ognjanovski et al 2018).…”