Neural Dynamics of Mental Imagery, Visual Perception, and Rapid Eye Movement Sleep

Abstract

In order to better understand the functional role of rapid eye movement (REM) sleep, we sought to gain a deeper understanding of the differences between neural activity during REM sleep and during the awake state. We set out to investigate the temporal directionality of communication and coupling in neural activity between different areas of the brain during REM sleep and awake activities. One theory suggests that dreaming, which occurs predominantly during REM sleep, may be a mechanism for humans to incorporate information learned during the day, reflecting the memory consolidation function of sleep. Both mental imagery and dreaming are internally generated percepts while sensory processing is more externally generated, though similar neural regions are utilized. The difference in information flow between REM sleep, mental imagery, and stimulus perception may help us understand which regions of the brain and neural processes are key for the functional role REM sleep may serve. We conducted three studies comparing the oscillatory and topographical characteristics of REM sleep, visual perception, and mental imagery in an effort to help illuminate how REM sleep processes memories. Participants with no history of neurological disorders provided electroencephalography (EEG) data, while other participants provided intracranial data with electrodes surgically implanted as part of their epilepsy treatment plan. Both sets of human participants were monitored during visual stimulus processing, imagery, and REM sleep. The visual stimuli involved clock angles. The imagery task involved imagining two clock times and comparing their angles after an auditory stimulus. Brain activity during sleep was recorded during an overnight stay. Additionally, subjects performed a video imagery task where visual and auditory perception and imagery were tested by watching a video, then being asked to imagine the visuals or audio of that video. Intracranial participants provided access to data from internal structures of the brain and localized results, such as low frequency activity observed in the hippocampus during REM sleep. Conventional EEG participants provided access to data giving a better distributed image of the entire brain. Results from 20 EEG participants showed clear differences in the spectral content of certain regions of the brain when comparing the average power and coherence across the three conditions (visual stimuli, imagery, and REM sleep). Consistent for both imagery task paradigms, more power was observed frontally and centrally in the delta and theta frequency bands in REM sleep compared to perception and imagery, while both visual perception and imagery had higher power than REM sleep in most channels apart from the central midline channels in the beta and gamma frequency ranges, and more coherence occipitally and parietally in the gamma frequency band compared to REM sleep. Beyond a better understanding of the neural dynamics underlying mental imagery, visual perception, and REM sleep, these results may help in the construction of better brain machine interface algorithms and provide insight into diseases associated with REM sleep problems, such as Parkinson's disease, narcolepsy, and depression. In addition, we used sleep as a window into neurological disorders. In particular, we utilized high-density EEG polysomnography in Parkinson's disease (PD) patients to help reveal not only atypical REM sleep, but also disrupted Non-REM (NREM) sleep architecture, including reduced slow wave and spindle power and abnormal spindle-slow wave coupling. While this study was preliminary, findings suggest that these sleep abnormalities may underlie the motor memory deficits observed in PD. Collectively, this work highlights the importance of REM and NREM sleep in memory consolidation across visual perception, imagery, and motor learning tasks. These findings could potentially lead to insights into diseases involving REM sleep abnormalities.