Abstract
Hippocampal (HPC) theta oscillation during post-training rapid eye movement (REM) sleep supports spatial learning. Theta also modulates neuronal and oscillatory activity in the retrosplenial cortex (RSC) during REM sleep. To investigate the relevance of theta-driven interaction between these two regions to memory consolidation, we computed the Granger causality within theta range on electrophysiological data recorded in freely behaving rats during REM sleep, both before and after contextual fear conditioning. We found a training-induced modulation of causality between HPC and RSC that was correlated with memory retrieval 24 h later. Retrieval was proportional to the change in the relative influence RSC exerted upon HPC theta oscillation. Importantly, causality peaked during theta acceleration, in synchrony with phasic REM sleep. Altogether, these results support a role for phasic REM sleep in hippocampo-cortical memory consolidation and suggest that causality modulation between RSC and HPC during REM sleep plays a functional role in that phenomenon.
Highlights
Hippocampal (HPC) theta oscillation during post-training rapid eye movement (REM) sleep supports spatial learning
Since it has been shown that theta acceleration and high frequency oscillations (40–120 Hz) boost occur during phasic REM sleep[14], we examined whether changes in directionality occur during phasic REM sleep (phREM)
During REM sleep that follows contextual fear conditioning (CFC) training, we observed a modulation of the relative influences the HPC and retrosplenial cortex (RSC) exert upon each other’s theta oscillation, in a manner that is significantly related to learning performance
Summary
Hippocampal (HPC) theta oscillation during post-training rapid eye movement (REM) sleep supports spatial learning. Two distinct electrophysiological patterns observed in the HPC of rodents during sleep have been consistently related to memory processing: the sharp-wave ripple (SWR) complex[6], and the sustained theta oscillation[7] While the former is mainly observed during slow-wave sleep (SWS), the latter is the hallmark of rapid eye movement (REM, a.k.a. paradoxical) sleep in r odents[7]. We have recently reported that HPC theta oscillation during REM sleep modulates oscillatory and neuronal activity within the R SC16 Both regions are related to contextual fear memory p rocessing[1], and their cross-talk has been related to memory performance[2,3,17,18]. PhREM events coincided with augmented exchanged influence in the HPC-RSC network These results point to a specific role of REM sleep theta oscillations in spatial memory processing, mainly conveyed by the HPC-RSC intercommunication during phREM events
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