Thermosensitivity of anterior hypothalamic-preoptic neurons during the waking-sleeping cycle: a study in brain functional states

Parmeggiani, Pier Luigi; Cevolani, Daniela; Azzaroni, A; Ferrari, G.

doi:10.1016/0006-8993(87)90270-8

Cited by 56 publications

(17 citation statements)

References 13 publications

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“…During REMS, the relationship between hypothalamic temperature and metabolic heat production is weak [4] and shivering and panting are absent [5]. These phenomena likely result from changes in the thermal sensitivity of hypothalamic preoptic neurons [4], [6]. On the other hand, blood pressure increases at cold T a [7], [8], and this may explain at least part of the excess cardiovascular mortality in cold winter months [9], [10].…”

Section: Introductionmentioning

confidence: 99%

Effects of Ambient Temperature on Sleep and Cardiovascular Regulation in Mice: The Role of Hypocretin/Orexin Neurons

et al. 2012

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The central neural pathways underlying the physiological coordination between thermoregulation and the controls of the wake-sleep behavior and cardiovascular function remain insufficiently understood. Growing evidence supports the involvement of hypocretin (orexin) peptides in behavioral, cardiovascular, and thermoregulatory functions. We investigated whether the effects of ambient temperature on wake-sleep behavior and cardiovascular control depend on the hypothalamic neurons that release hypocretin peptides. Orexin-ataxin3 transgenic mice with genetic ablation of hypocretin neurons (n = 11) and wild-type controls (n = 12) were instrumented with electrodes for sleep scoring and a telemetric blood pressure transducer. Simultaneous sleep and blood pressure recordings were performed on freely-behaving mice at ambient temperatures ranging between mild cold (20°C) and the thermoneutral zone (30°C). In both mouse groups, the time spent awake and blood pressure were higher at 20°C than at 30°C. The cold-related increase in blood pressure was significantly smaller in rapid-eye-movement sleep (REMS) than either in non-rapid-eye-movement sleep (NREMS) or wakefulness. Blood pressure was higher in wakefulness than either in NREMS or REMS at both ambient temperatures. This effect was significantly blunted in orexin-ataxin3 mice irrespective of ambient temperature and particularly during REMS. These data demonstrate that hypocretin neurons are not a necessary part of the central pathways that coordinate thermoregulation with wake-sleep behavior and cardiovascular control. Data also support the hypothesis that hypocretin neurons modulate changes in blood pressure between wakefulness and the sleep states. These concepts may have clinical implications in patients with narcolepsy with cataplexy, who lack hypocretin neurons.

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Section: Introductionmentioning

confidence: 99%

Effects of Ambient Temperature on Sleep and Cardiovascular Regulation in Mice: The Role of Hypocretin/Orexin Neurons

et al. 2012

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“…, the neuron was termed a CSN (Parmeggiani et al, 1987). In the other method, if the Q 10 was Ͼ2 it was termed as WSN and if Q 10 was Ͻ0.5 it was termed as CSN (Curras et al, 1991).…”

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confidence: 99%

GABA exerts opposite influence on warm and cold sensitive neurons in medial preoptic area in rats

Jha¹,

Islam²,

Mallick³

2001

J. Neurobiol.

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The preoptic area regulates body temperature. GABA-ergic terminals and receptors are present in this area. Local microinjection studies have shown that GABA, its agonist, and its antagonist in this area may modulate body temperature. However, there are warm and cold sensitive neurons, and they are known to be affected by local and peripheral temperatures. In order to understand the mechanism of action of GABA in temperature regulation at the cellular level it was necessary to study the effect of GABA on individual thermosensitive neurons in in vivo preparations. Hence, in this study the responses of preoptic area thermosensitive and insensitive neurons to microiontophoretic application of picrotoxin, a GABA-A antagonist, were studied in anaesthetized rats. It was observed that a majority of both the thermosensitive and insensitive neurons were affected by microiontophoretic application of picrotoxin. Although almost an equal number of cold and warm sensitive neurons were affected, a majority of the cold sensitive neurons were excited, while a majority of the warm sensitive neurons were inhibited by picrotoxin. The results suggested that in normal conditions GABA acts through GABA-A receptor in modulating the spontaneous activity of thermosensitive neurons in the preoptic area. Furthermore, the results of the present study taken together with other reports suggest that normally GABA exerts a direct inhibitory action on the cold sensitive neurons, while it acts on presynaptic heteroreceptors, possibly on norepinephrinergic afferent input terminals on the warm sensitive neurons, for mediating its action.

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“…In addition, the medial POA also has an important role in the regulation of body temperature, and damage to cells in this region results in dysfunction of the control ofboth sleep-wakefulness and body temperature in cats (McGinty and Sterman, 1968;Szymusiak et al, 199 1). Furthermore, the thermosensitive neurons in the POA are known to change their sensitivities to the brain temperature in association with changes in the sleep-wakefulness alteration (Glotzbach and Heller, 1984;Parmeggiani et al, 1987). These findings indicate that the regulation of body temperature in the POA is closely related to the sleep-wakefulness control mechanism.…”

Section: Discussionmentioning

confidence: 90%

Prostaglandin E2 exerts an awaking effect in the posterior hypothalamus at a site distinct from that mediating its febrile action in the anterior hypothalamus

Onoe¹,

Watanabe²,

Ono³

et al. 1992

J. Neurosci.

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The precise sites for prostaglandin E2 (PGE2)-related activity responsible for the promotion of wakefulness and elevation of brain temperature were determined in several regions of the monkey brain. PGE2 was administered through a microdialysis probe into 11 brain loci mainly in the preoptic area/anterior hypothalamic region (POA/AH) and the tuberomammillary region in the posterior hypothalamus (TuM-PH). Administration of PGE2 into the POA/AH resulted in a marked and dose- dependent febrile response. When a low dose (15 pmol/min) of PGE2 was administered into the POA/AH, brain temperature increased significantly up to a 0.6 degrees C rise, but sleep behavior and amounts of time in wakefulness, slow wave sleep (SWS), and REM sleep during the administration period were not significantly different from those of the control monkeys. Dose of PGE2 above 150 pmol/min elevated the brain temperature and heart rate more markedly and suppressed sleep. The degree of inhibition of sleep by PGE2 was closely correlated with the changes in these autonomic responses. On the other hand, when a low dose of PGE2 was administered into the TuM-PH, the time spent awake during the administration period increased up to 3.5-fold and the amount of time spent in SWS decreased to 50% of that of the control level, with negligible changes in brain temperature and heart rate. The awaking response of PGE2 in the TuM-PH was also dose dependent, but was not correlated with the change in brain temperature. Among 11 brain regions tested, the hyperthermic effect of PGE2 was most potent in the POA, while its awaking effect was most pronounced in the TuM-PH close to the mammillary complex. These findings demonstrate that the site of action of PGE2 for the regulation of sleep-wakefulness is clearly distinct from that for the temperature regulation. PGE2 may be involved in the neurochemical mechanism of wakefulness mediated in a specific site in the PH.

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Thermosensitivity of anterior hypothalamic-preoptic neurons during the waking-sleeping cycle: a study in brain functional states

Cited by 56 publications

References 13 publications

Effects of Ambient Temperature on Sleep and Cardiovascular Regulation in Mice: The Role of Hypocretin/Orexin Neurons

Effects of Ambient Temperature on Sleep and Cardiovascular Regulation in Mice: The Role of Hypocretin/Orexin Neurons

GABA exerts opposite influence on warm and cold sensitive neurons in medial preoptic area in rats

Prostaglandin E2 exerts an awaking effect in the posterior hypothalamus at a site distinct from that mediating its febrile action in the anterior hypothalamus

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