Abstract

Eye movement is not only for adjusting the visual field and maintaining the stability of visual information on the retina, but also provides an external manifestation of the cognitive status of the brain. Recent studies showed similarity in eye movement patterns between wakefulness and rapid eye movement (REM) sleep, indicating that the brain status of REM sleep likely resembles that of awake status. REM sleep in humans could be divided into phasic REM and tonic REM sleep according to the difference in eye movement frequencies. Mice are the most commonly used animal model for studying neuronal and molecular mechanisms underlying sleep. However, there was a lack of details for eye movement patterns during REM sleep, hence it remains unknown whether REM sleep can be further divided into different stages in mice. Here we developed a device combining electroencephalogram (EEG), electromyogram (EMG) as well as eye movements recording in mice to study the eye movement patterns during sleep. We implanted a magnet beneath the conjunctiva of eye and tracked eye movements using a magnetic sensor. The magnetic signals showed strong correlation with video-oculography in head-fixed mice, indicating that the magnetic signals reflect the direction and magnitude of eye movement. We also found that the magnet implanted beneath the conjunctiva exhibited good biocompatibility. Finally, we examined eye movement in sleep–wake cycle, and discriminated tonic REM and phasic REM according to the frequency of eye movements, finding that compared to tonic REM, phasic REM exhibited higher oscillation power at 0.50 Hz, and lower oscillation power at 1.50–7.25 Hz and 9.50–12.00 Hz. Our device allowed to simultaneously record EEG, EMG, and eye movements during sleep and wakefulness, providing a convenient and high temporal-spatial resolution tool for studying eye movements in sleep and other researches in mice.

Highlights

  • Eye movements help human to align fovea to the target with attention and stabilize the vision on retina and is precisely regulated by visual, somatosensory, vestibular, and other systems (Sweeney et al, 2007; Kheradmand et al, 2016; Shemesh and Zee, 2019; Billington et al, 2020)

  • We developed a device for conducting eye movements and simultaneous EEG/EMG recording during sleep–wake cycle in mice

  • Previous studies reported that during wake, rapid eye movement (REM) and NREM sleep, the average frequency of eye movements in mice was about 0.90, 0.25, and 0.05 Hz, respectively, which was recorded by EOG (Fulda et al, 2011; Gutierrez Herrera et al, 2019)

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Summary

Introduction

Eye movements help human to align fovea to the target with attention and stabilize the vision on retina and is precisely regulated by visual, somatosensory, vestibular, and other systems (Sweeney et al, 2007; Kheradmand et al, 2016; Shemesh and Zee, 2019; Billington et al, 2020). In Rodents, REM sleep was identified as theta band (6–10 Hz) dominant EEG, elevated theta/delta (0.65–4 Hz) power ratio, and high eye movement frequency. Non-REM sleep was identified as delta band (0.65–4 Hz) dominant EEG, low theta/delta power ratio, and low eye movement frequency (Jouvet, 1965; Mann and Roschke, 1997; Weber and Dan, 2016). The phasic REM sleep is characterized by bursts of eye movements, while tonic REM sleep had less eye movements These two microstates had different arousal thresholds and spontaneous oscillation activity. Tonic REM sleep showed elevated high alpha and beta band, while phasic REM sleep showed the predominance of slow delta, theta, and higher gamma band (Ermis et al, 2010; Simor et al, 2020). Developing a device to track eye movements with eyelid closed would be useful to unveil the role of eye movements in sleep depth and cortical processing during sleep

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