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Serotonin neurons and sleep. I. Long term recordings of dorsal raphe discharge frequency and PGO waves.

R. Lydic, R. W. McCarley, J. A. Hobson


Brain stem transection studies suggest that pontine neurons play a key role in regulating the mammalian sleep cycle. The serotonin (5-HT) hypothesis originally postulated that pontine 5-HT containing neurons directly initiated and maintained synchronized or NREM sleep and "primed" rapid eye movement (REM) sleep. Contrary to the predictions of this hypothesis, single unit recordings from the serotonergic dorsal raphe nucleus (DRN) have uniformly shown that DRN discharge rate is positively correlated with behavioral arousal but negatively correlated with both the NREM and REM phases of sleep. These findings required revision of the original 5-HT hypothesis and suggested instead that DRN discharge may influence the maintenance of behavioral arousal and, by ceasing to discharge, may contribute to the generation of NREM and REM sleep. The purpose of this paper was to quantitatively assess the strength of the correlation between DRN discharge, REM sleep, and PGO waves following the experimental perturbations of the sleep cycle. Since forced locomotor activity is known to powerfully alter the timing of sleep and wakefulness, the present experiments used forced activity in an attempt to dissociate DRN discharge from the sleep cycle. It was hypothesized that such dissociations would suggest DRN discharge is not involved in sleep cycle regulation. Contrastingly, preserved correlations would support the hypothesis of a possible causal relationship between DRN discharge, PGO waves activity, and the timing of sleep and wakefulness. Extracellular recordings were obtained from single cells in the DRN of intact, undrugged cats across greater than 300 sleep cycles with durations ranging from about 8 to 80 mins. Forced activity significantly reduced the amount of time spent in wakefulness and increased the number but not the duration of REM sleep epochs. The results revealed that DRN discharge rate was altered as a function of sleep cycle duration. In no case, however, was forced activity able to completely dissociate the characteristic DRN discharge rates from PGO waves or the ultradian sleep cycle. The inability of forced activity to disrupt the faithful relationships between DRN discharge, PGO waves, and sleep cycle phase thus provides a new form of correlative evidence consistent with the hypothesis that the DRN is involved in sleep cycle regulation.

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