REM sleep prefrontal high-frequency oscillation chains mediate distinct cortical – hippocampal reactivation patterns compared to NREM sleep

REM sleep and non-REM sleep play crucial roles in memory consolidation within hippocampal-cortical circuits. However, the mechanisms behind REM memory processes are not as well understood compared to NREM memory reactivation. In this study, researchers discovered prefrontal cortical (PFC) high-frequency oscillation (HFO) chains during REM sleep in rodents while studying the consolidation of spatial memory.

Through high-density tetrode recordings, they observed that REM cortical HFOs form distinctive chains, which are phase-modulated by theta oscillations. This modulation leads to increased CA1-PFC theta coherence, creating periods of heightened hippocampal-cortical communication. REM HFO chains sequentially activate specific PFC ensembles during local suppression, which sets them apart from the widespread reactivation bursts seen during NREM ripple oscillations.

Moreover, REM HFO chains preferentially involve CA1 neuronal populations that adjust their preferred theta-phase from behavior to REM sleep. The activation of CA1 neurons during REM HFO chains is correlated with suppression of CA1 activity during NREM PFC ripples, and is linked to the differential changes in CA1 firing rates between sleep stages.

By incorporating the effects of acetylcholine, a cortical network model can recreate the distinct REM and NREM activity patterns, offering a mechanistic explanation for the widespread coactivity during REM HFO chains, as opposed to the sparse, temporally extended reactivation occurring on a background of local suppression during NREM cortical ripples.

These findings highlight the role of PFC HFOs in regulating distinct reactivation patterns during sleep stages.