Preferential Neural and Ocular Responses to External Stimuli during REM Sleep

Introduction:
Sleep comprises rapid eye movement (REM) sleep and non-rapid eye movement (NREM) sleep. While the microstructure of NREM sleep and their functions have been extensively studied, REM sleep structure and functions have been comparatively overlooked. Research dating back to more than 60 years ago identified that REM sleep can be divided into "phasic" and "tonic" episodes based on the presence (phasic) or absence (tonic) of rapid eye movements. Here, we revisit the neurophysiological basis for this dichotomy and examine brain activity and their functions during REM sleep microstates.
Method:
We recorded overnight high-density electroencephalography (EEG) in 17 healthy humans. We presented sounds to the participants throughout the night. These sounds were either the subject’s own name or unfamiliar names spoken by either a familiar voice or an unfamiliar voice. Using automatic algorithms followed by visual inspections, we divided REM sleep into phasic and tonic epochs. Thereafter, we compared brain activity as well as brain and eye movement responses to the different stimuli during these microstates.
Results:
We found that brain arousability and responsiveness to external stimuli are significantly higher during tonic REM episodes compared to phasic ones. This is evidenced by the greater number of microarousals detected during tonic REM and the stronger evoked responses to stimuli. Furthermore, brain responses were stronger to unfamiliar stimuli indicating that the brain continues to process external stimuli during tonic REM, with a unfamiliarity being a strong predictor of whether a sitmulus will be processed. Notably, we also observed preferential ocular responses to external stimuli, as eye movements were faster in response to unfamiliar voices and the subject’s name even during phasic episodes, presenting a new perspective on the preferntial processing of relevant information presented during REM sleep.
Conclusion:
Our findings provide evidence for preferential processing of external stimuli during tonic REM, corroborating previous findings. Moreover, we extend previous results by identifying eye movements as a strong predictor for information processing in the brain during REM sleep. These results shed new light on brain activity during the enigmatic REM sleep.