Effect of SCN lesions on sleep in squirrel monkeys: evidence for opponent processes in sleep-wake regulation

Sleep and wakefulness are governed by both the suprachiasmatic nuclei of the hypothalamus (SCN), and a sleep homeostatic process; however, the interaction of these control systems is not well understood. From rodent studies it has been assumed that the SCN promote neither wake nor sleep but gate the...

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Published in:The Journal of neuroscience Vol. 13; no. 3; pp. 1065 - 1079
Main Authors: Edgar, DM, Dement, WC, Fuller, CA
Format: Journal Article
Language:English
Published: Washington, DC Soc Neuroscience 01-03-1993
Society for Neuroscience
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Abstract Sleep and wakefulness are governed by both the suprachiasmatic nuclei of the hypothalamus (SCN), and a sleep homeostatic process; however, the interaction of these control systems is not well understood. From rodent studies it has been assumed that the SCN promote neither wake nor sleep but gate the homeostatic sleep-promoting process. Yet in humans sleep tendency is lowest during the later waking hours of the day, and sleep duration can be predicted because of the precise circadian timing of waking. Thus in primates, the SCN could assure sleep-wake cycle consolidation by actively promoting or facilitating wakefulness. To evaluate this hypothesis, we examined the sleep-wake and sleep-stage patterns of intact and SCN-lesioned (SCNx) squirrel monkeys maintained in constant light. This diurnal primate has consolidated sleep and wake patterns more similar to man than rodents. Sleep-wake, sleep stages, brain temperature, and drinking circadian rhythms were eliminated, and total sleep time was significantly increased (4.0 hr, P < 0.01) in SCNx monkeys. However, total times in deeper stages of non-rapid eye movement (non-REM; e.g., delta sleep) and REM sleep were not significantly affected by SCN lesions. Increased total sleep time was associated with a reduction in subjective day wake consolidation, as evidenced by substantially shorter wake bout lengths in SCNx monkeys (15 +/- 6 min) as compared to intact monkeys (223 +/- 10 min; P < 0.0001, ANOVA). These findings show that the SCN influence the regulation of daily total wake and sleep times, and implicate an alternative sleep-wake regulatory model in which an SCN-dependent process actively facilitates the initiation and maintenance of wakefulness and opposes homeostatic sleep tendency during the subjective day in diurnal primates.
AbstractList Sleep and wakefulness are governed by both the suprachiasmatic nuclei of the hypothalamus (SCN), and a sleep homeostatic process; however, the interaction of these control systems is not well understood. From rodent studies it has been assumed that the SCN promote neither wake nor sleep but gate the homeostatic sleep-promoting process. Yet in humans sleep tendency is lowest during the later waking hours of the day, and sleep duration can be predicted because of the precise circadian timing of waking. Thus in primates, the SCN could assure sleep-wake cycle consolidation by actively promoting or facilitating wakefulness. To evaluate this hypothesis, we examined the sleep-wake and sleep-stage patterns of intact and SCN-lesioned (SCNx) squirrel monkeys maintained in constant light. This diurnal primate has consolidated sleep and wake patterns more similar to man than rodents. Sleep-wake, sleep stages, brain temperature, and drinking circadian rhythms were eliminated, and total sleep time was significantly increased (4.0 hr, P < 0.01) in SCNx monkeys. However, total times in deeper stages of non-rapid eye movement (non-REM; e.g., delta sleep) and REM sleep were not significantly affected by SCN lesions. Increased total sleep time was associated with a reduction in subjective day wake consolidation, as evidenced by substantially shorter wake bout lengths in SCNx monkeys (15 +/- 6 min) as compared to intact monkeys (223 +/- 10 min; P < 0.0001, ANOVA). These findings show that the SCN influence the regulation of daily total wake and sleep times, and implicate an alternative sleep-wake regulatory model in which an SCN-dependent process actively facilitates the initiation and maintenance of wakefulness and opposes homeostatic sleep tendency during the subjective day in diurnal primates.
Sleep and wakefulness are governed by both the suprachiasmatic nuclei of the hypothalamus (SCN), and a sleep homeostatic process; however, the interaction of these control systems is not well understood. We examined the sleep-wake and sleep-stage patterns of intact and SCN-lesioned (SCNx) squirrel monkeys maintained in constant light. Sleep-wake, sleep stages, brain temperature, and drinking circadian rhythms were eliminated, and total sleep time was significantly increased in SCNx monkeys. These findings show that the SCN influence the regulation of daily total wake and sleep times, and implicate an alternative sleep-wake regulatory model in which an SCN-dependent process actively facilitates the initiation and maintenance of wakefulness and opposes homeostatic sleep tendency during the subjective day in diurnal primates.
Author Edgar, DM
Dement, WC
Fuller, CA
AuthorAffiliation Department of Animal Physiology, University of California, Davis 95616
AuthorAffiliation_xml – name: Department of Animal Physiology, University of California, Davis 95616
Author_xml – sequence: 1
  fullname: Edgar, DM
– sequence: 2
  fullname: Dement, WC
– sequence: 3
  fullname: Fuller, CA
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ContentType Journal Article
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1993 by Society for Neuroscience 1993
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Keywords Suprachiasmatic nucleus
Body temperature
Central nervous system
Monkey
Drinking
Biological rhythm
Hypothalamus
Circadian rhythm
Saimiri sciureus
Vertebrata
Mammalia
Primates
Simioidea
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Sleep wake cycle
Brain (vertebrata)
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Snippet Sleep and wakefulness are governed by both the suprachiasmatic nuclei of the hypothalamus (SCN), and a sleep homeostatic process; however, the interaction of...
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SubjectTerms Analysis of Variance
Animals
Arousal - physiology
Biological and medical sciences
Body Temperature
Circadian Rhythm
Electroencephalography
Fundamental and applied biological sciences. Psychology
Male
Reference Values
Saimiri
Saimiri sciureus
Sleep - physiology
Sleep. Vigilance
Space life sciences
Suprachiasmatic Nucleus - physiology
Vertebrates: nervous system and sense organs
Wakefulness - physiology
Title Effect of SCN lesions on sleep in squirrel monkeys: evidence for opponent processes in sleep-wake regulation
URI http://www.jneurosci.org/cgi/content/abstract/13/3/1065
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Volume 13
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