Homeostatic Regulation of Sleep: A Role for Preoptic Area Neurons

Gvilia, Irma; Xu, Feng; McGinty, Dennis; Szymusiak, Ronald

doi:10.1523/jneurosci.2012-06.2006

Cited by 119 publications

(109 citation statements)

References 27 publications

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“…These cells increase discharge before sleep onset and during both NREM and REM sleep (Suntsova et al, 2002). Activation of MnPN sleepactive neurons reflects a homeostatic sleep drive (Suntsova et al, 2002;Gvilia et al, 2006). Here, we show that MnPN inactivation results in sustained wakefulness.…”

Section: Effects Of the Mnpn On Pf/lh Neuronsmentioning

confidence: 55%

The Median Preoptic Nucleus Reciprocally Modulates Activity of Arousal-Related and Sleep-Related Neurons in the Perifornical Lateral Hypothalamus

Suntsova¹,

Guzmán-Marı́n²,

Kumar³

et al. 2007

J. Neurosci.

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Section: Effects Of the Mnpn On Pf/lh Neuronsmentioning

confidence: 55%

The Median Preoptic Nucleus Reciprocally Modulates Activity of Arousal-Related and Sleep-Related Neurons in the Perifornical Lateral Hypothalamus

Suntsova¹,

Guzmán-Marı́n²,

Kumar³

et al. 2007

J. Neurosci.

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“…All cell counts were calculated for constant rectangular grids corresponding to four areas of interest. Grid sizes for infant rats were scaled based on the grids used in our previous studies in adult rats (19,23,25). (1) The rostral MnPN (rMnPN) grid was a 510 ϫ 510-m square centered on the apex of the third ventricle rostral to the decussation of the anterior commissure and to bregma (anterior, 0.1 mm) (2).…”

Section: Discussionmentioning

confidence: 99%

“…Based on patterns of c-Fos protein expression, MnPN neurons are activated during periods of SD, suggesting involvement of MnPN neurons in mediating sleepiness and promoting sleep onset in response to SD (25). Maximal activation in VLPO neurons occurs during recovery sleep following SD, suggesting a role for VLPO neurons in regulating sleep continuity and sleep depth during recovery sleep (25). This hypothesized dichotomy of function (24,46) is supported by electrophysiological (44,45) and anatomical studies in adult animals (49,48,8).…”

mentioning

confidence: 93%

“…Some evidence suggests that VLPO and MnPN have different functions in the homeostatic response to SD. Based on patterns of c-Fos protein expression, MnPN neurons are activated during periods of SD, suggesting involvement of MnPN neurons in mediating sleepiness and promoting sleep onset in response to SD (25). Maximal activation in VLPO neurons occurs during recovery sleep following SD, suggesting a role for VLPO neurons in regulating sleep continuity and sleep depth during recovery sleep (25).…”

mentioning

confidence: 99%

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Maturation of sleep homeostasis in developing rats: a role for preoptic area neurons

Gvilia

Suntsova

Angara

et al. 2011

American Journal of Physiology-Regulatory, Integrative and Comp

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Gvilia I, Suntsova N, Angara B, McGinty D, Szymusiak R. Maturation of sleep homeostasis in developing rats: a role for preoptic area neurons. Am J Physiol Regul Integr Comp Physiol 300: R885-R894, 2011. First published February 16, 2011 doi:10.1152/ajpregu.00727.2010.-The present study evaluated the hypothesis that developmental changes in hypothalamic sleepregulatory neuronal circuits contribute to the maturation of sleep homeostasis in rats during the fourth postnatal week. In a longitudinal study, we quantified electrographic measures of sleep during baseline and in response to sleep deprivation (SD) on postnatal days 21/29 (P21/29) and P22/30 (experiment 1). During 24-h baseline recordings on P21, total sleep time (TST) during the light and dark phases did not differ significantly. On P29, TST during the light phase was significantly higher than during the dark phase. Mean duration of non-rapideye-movement (NREM) sleep bouts was significantly longer on P29 vs. P21, indicating improved sleep consolidation. On both P22 and P30, rats exhibited increased NREM sleep amounts and NREM electroencephalogram delta power during recovery sleep (RS) compared with baseline. Increased NREM sleep bout length during RS was observed only on P30. In experiment 2, we quantified activity of GABAergic neurons in median preoptic nucleus (MnPN) and ventrolateral preoptic area (VLPO) during SD and RS in separate groups of P22 and P30 rats using c-Fos and glutamic acid decarboxylase (GAD) immunohistochemistry. In P22 rats, numbers of Fos ϩ GAD ϩ neurons in VLPO did not differ among experimental conditions. In P30 rats, Fos ϩ GAD ϩ counts in VLPO were elevated during RS. MnPN neuronal activity was state-dependent in P22 rats, but Fos ϩ GAD ϩ cell counts were higher in P30 rats. These findings support the hypothesis that functional emergence of preoptic sleep-regulatory neurons contributes to the maturation of sleep homeostasis in the developing rat brain. postnatal development; sleep-promoting systems; sleep homeostasis; preoptic hypothalamus SLEEP IN ADULT MAMMALS is homeostatically regulated. Rats exhibit a gradual emergence of different components of sleep homeostasis during postnatal development (5,14,40,47). Some aspects of sleep homeostasis are present in rats on postnatal day (P) 2, when sleep deprivation (SD) increases sleep time during postdeprivation recovery sleep (47). Postdeprivation increases in non-rapid-eye-movement (NREM) sleep delta (␦) power, a measure of the intensity of homeostatic response in adults (7), are observed in P24 rats but not in P20 rats (14). In developing rats, electroencephalogram (EEG) spectral power in the ␦ frequency (0.5-4.0 Hz) in NREM sleep progressively increases across P10 -P20 (13,22). However, the normal decline in NREM sleep ␦-wave activity during the rest phase, typical of adult rats and reflective of adult sleep homeostasis, is absent in rats younger than P24 (13). The above findings suggest that sleep homeostasis in rats undergoes significant maturation between the third and fourth po...

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“…However, inactivation of the septohippocampal system potentiates general anesthesia (Ma et al, 2002), and the sedative action of general anesthetics may involve endogenous sleep-promoting pathways (Nelson et al, 2002). It is conceivable that selective loss of septal cholinergic neurons might promote recovery sleep, perhaps by disinhibiting adjacent preoptic neurons known to be involved in sleep homeostasis (Gvilia et al, 2006). This possible role of septal cholinergic neurons antagonistic to the caudal cholinergic neurons remains to be investigated.…”

mentioning

confidence: 99%

Effects of Ibotenate and 192IgG-Saporin Lesions of the Nucleus Basalis Magnocellularis/Substantia Innominata on Spontaneous Sleep and Wake States and on Recovery Sleep after Sleep Deprivation in Rats

Kaur¹,

Junek²,

Black³

et al. 2008

J. Neurosci.

115

110

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The basal forebrain (BF) is known for its role in cortical and behavioral activation, and has been postulated to have a role in compensatory mechanisms after sleep loss. However, specific neuronal phenotypes responsible for these roles are unclear. We investigated the effects of ibotenate (IBO) and 192IgG-saporin (SAP) lesions of the caudal BF on spontaneous sleep-waking and electroencephalogram (EEG), and recovery sleep and EEG after 6 h of sleep deprivation (SD). Relative to artificial CSF (ACSF) controls, IBO injections decreased parvalbumin and cholinergic neurons in the caudal BF by 43 and 21%, respectively, and cortical acetylcholinesterase staining by 41%. SAP injections nonsignificantly decreased parvalbumin neurons by 11%, but significantly decreased cholinergic neurons by 69% and cortical acetylcholinesterase by 84%. IBO lesions had no effect on sleep-wake states but increased baseline delta power in all states [up to 62% increase during non-rapid eye movement (NREM) sleep]. SAP lesions transiently increased NREM sleep by 13%, predominantly during the dark phase, with no effect on EEG. During the first 12 h after SD, animals with IBO and SAP lesions showed lesser rebound NREM sleep (32 and 77% less, respectively) and delta power (78 and 53% less) relative to ACSF controls. These results suggest that noncholinergic BF neurons promote cortical activation by inhibiting delta waves, whereas cholinergic BF neurons play a nonexclusive role in promoting wake. Intriguingly, these results also suggest that both types of BF neurons play important roles, probably through different mechanisms, in increased NREM sleep and EEG delta power after sleep loss.

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Homeostatic Regulation of Sleep: A Role for Preoptic Area Neurons

Cited by 119 publications

References 27 publications

The Median Preoptic Nucleus Reciprocally Modulates Activity of Arousal-Related and Sleep-Related Neurons in the Perifornical Lateral Hypothalamus

The Median Preoptic Nucleus Reciprocally Modulates Activity of Arousal-Related and Sleep-Related Neurons in the Perifornical Lateral Hypothalamus

Maturation of sleep homeostasis in developing rats: a role for preoptic area neurons

Effects of Ibotenate and 192IgG-Saporin Lesions of the Nucleus Basalis Magnocellularis/Substantia Innominata on Spontaneous Sleep and Wake States and on Recovery Sleep after Sleep Deprivation in Rats

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