Differential Brain and Eye Responses to External Auditory Information in Phasic and Tonic REM Sleep

Introduction: Rapid eye movement (REM) sleep, can be categorized into phasic and tonic episodes.
Phasic REM sleep, typically associated with dreaming, is conventionally considered a phase of brain isolation, detached from external influences. In contrast, tonic REM sleep phases are believed to foster a heightened connection with the environment and enhanced receptiveness to external stimuli. Despite this understanding, there is limited knowledge regarding processing external information during these distinct REM stages. The objective of this study is to elucidate the contrasting characteristics of phasic and tonic REM sleep stages by examining brain and eye responses to different auditory stimuli in these distinct REM episodes.
Materials and Methods:To this end, we analysed high-density electroencephalography (EEG) data from 17 healthy human subjects who underwent a full night of sleep (~8 hours). Throughout the night, participants were presented with auditory stimuli, including their own name (SON) and two unfamiliar names (UNs), spoken by either a familiar voice (FV) or an unfamiliar voice (UFV). We classified REM sleep into four-second phasic and tonic episodes based on the presence or absence of rapid eye movements. Our analysis included multivariate decoding, event-related and time-frequency analyses, as well as differences in aperiodic EEG activity.
Results: Our findings revealed notable differences between phasic and tonic REM sleep episodes. During tonic REM, we observed a higher number of microarousals and a shallower slope of the EEG signal as compared to phasic REM, with the former highlighting increased external processing and the latter indicating more excitatory cortical activity. In terms of auditory processing, we discovered distinct event-related potentials (ERPs) and time-frequency responses to voices during tonic REM sleep. Specifically, UFV stimuli elicited stronger responses compared to FVs. Conversely, no significant differences in brain responses were observed during phasic REM sleep, characterized by dream occurrence, for either voices or names. Notably, however, we found significantly stronger eye responses to SONs compared to UNs during phasic REM sleep.
Conclusions: Our results confirm prior evidence suggesting a preference for processing unfamiliar stimuli during sleep, particularly REM sleep. Additionally, we demonstrate that eye movements during phasic REM sleep differentiate between sounds, suggesting that the brain remains partially responsive to the environment during these dream episodes. These findings shed light on the intricate nature of REM sleep and provide insights into the neural activity occurring during this enigmatic sleep stage.