Low-frequency stimulation of the hippocampus following fear extinction impairs both restoration of rapid eye movement sleep and retrieval of extinction memory

Abstract

Post-learning rapid eye movement (REM) sleep deprivation has often been shown to impair hippocampal functioning, which results in deficit in retrieval of some types of memory. However, it remains to be determined whether post-learning alteration of hippocampal functioning affects, in turn, REM sleep. Recent studies have shown that both post-extinction REM sleep deprivation and post-extinction application of hippocampal low-frequency stimulation (LFS) impair memory of fear extinction, indicating possible bidirectional interactions between hippocampal functioning and REM sleep. To analyze the potential effect of post-extinction alteration of hippocampal functioning on REM sleep, rats were implanted with stimulating electrodes in the dorsal hippocampus for post-extinction LFS. Sleep was recorded before (two sessions, 1 day apart) and after conditioning (five tone and eyelid-shock pairings), and following extinction training (25 tone-alone presentations) for 6 h per session. Fear conditioning reduced time spent in REM sleep, which was restored with fear extinction. Hippocampal LFS, applied immediately following extinction training, abolished the restorative effect of fear extinction on REM sleep and impaired extinction retrieval. These data extend previous findings and suggest bidirectional interactions between hippocampal functioning and REM sleep for successful extinction retrieval.