A quantitative study of electroencephalography, eye movements and neck electromyography characterizing the sleep-wake cycle of the guinea-pig.

Abstract

The qualitative and quantitative characteristics of cerebral cortex electrical activity, ocular motility and muscular activity were studied in six head-restrained guinea-pigs during wakefulness, slow-wave and paradoxical sleep. Animals were chronically implanted with bipolar electrodes in the obliquus capitis muscle for electromyographic recordings and epidurally through the parietal bones for electroencephalographic (EEG) recordings. Eye movements were recorded using the scleral search-coil technique. After postoperative recovery and a short period of habituation to immobilization, head-restrained animals exhibited a polyphasic sleep-wake cycle similar to what has already been described in the unrestrained guinea-pig. Paradoxical sleep periods of mean duration 110 +/- 42 s occurred at a mean interval of 32.2 +/- 7.2 min. Amplitude and frequency components of EEG activity were different for each state of vigilance. EEG amplitude was highest and frequency range lowest-with two well-defined peaks at 4 and 10 Hz-during slow-wave sleep. During paradoxical sleep, frequencies were higher and amplitudes lower than during wakefulness. Three types of eye movement intermingled with periods of ocular fixation were recorded: saccadic movements during wakefulness and paradoxical sleep, slow drifts during slow-wave sleep and paradoxical sleep, and a new type of eye movement-bursts of high-velocity eye oscillations during paradoxical sleep. Saccadic eye movements during paradoxical sleep were more frequent and showed higher velocities and amplitudes than during wakefulness. During paradoxical sleep the episodes of eye oscillation (8-14 Hz) occurred quite regularly every 1.6 s and had a mean duration of 1.4 s. During wakefulness, the obliquus muscle activity displayed a burst-tonic pattern. Bursting components were closely related to saccadic eye movements directed to the side of the recorded muscle. The muscle activity was predominantly tonic during slow-wave sleep and was completely absent during paradoxical sleep except for small bursts or twitches. These twitches were tightly synchronized with the occurrence of the rapid eye movements oriented towards the side of the recorded obliquus muscle, as during wakefulness. These results strongly suggest that paradoxical sleep is characterized by the oscillatory discharge of at least two neuronal populations: the brainstem saccadic generators and the tecto-reticular spinal network which underlies gaze-orienting behaviour during wakefulness. The occurrence of rhythmic discharges at approximately 11 Hz may explain the spinal motoneurons' inhibition during paradoxical sleep in order to avoid anarchic motor behavior. Whether these neuronal oscillations are simply an epiphenomenon or have functional implications remains to be determined.