Preoptic/anterior hypothalamic neurons: thermosensitivity in wakefulness and non rapid eye movement sleep

doi:10.1016/0006-8993(96)00035-2

Brain Research

Volume 718, Issues 1–2, 29 April 1996, Pages 76-82

https://doi.org/10.1016/0006-8993(96)00035-2 Get rights and content

Abstract

Thermosensitive neurons of the preoptic/anterior hypothalamic area (POAH) have been implicated in the regulation of both body temperature and non rapid eye movement (NREM) sleep. During NREM sleep, a majority of POAH warm-sensitive neurons (WSN) exhibit increased discharge compared to wakefulness. Cold-sensitive neurons (CSN) exhibit reduced discharge in NREM sleep compared to wakefulness. To further study the mechanism underlying these processes, the present study compared discharge rate and thermosensitivity (discharge rate change/°C) of WSNs and CSNs in NREM sleep and wakefulness in freely moving adult cats. The thermosensitivity of 24 WSNs and 31 CSNs from the medial POAH was determined from responses to local POAH warming and cooling. WSNs with increased discharge in NREM sleep exhibited increased thermosensitivity during NREM sleep compared to wakefulness. CSNs with decreased discharge during NREM sleep exhibited decreased thermosensitivity in NREM sleep. The change in thermosensitivity from wakefulness to NREM sleep was correlated with the change in discharge rate in WSNs but not in CSNs. In addition, 9 of 47 neurons that were thermo-insensitive during wakefulness became warm-sensitive during NREM sleep. Changes in POAH neuronal thermosensitivity could be a component of the mechanism for stabilization of state after state transition.

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POA warming suppresses waking-related activity of arousal-promoting neurons in the tuberomammillary nucleus and PFLH, the midbrain reticular formation, and the dorsal raphe nucleus (Krilowicz et al., 1994; Guzman-Marin et al., 2000; Methippara et al., 2003). Single-unit recordings in cats and rats during natural sleep and wakefulness combined with local manipulation of hypothalamic temperature reveal that a subset of warm-sensing neurons in the POAH, including those in the MnPO, exhibit elevation of spontaneous discharge rate during sleep onset and NREM sleep, compared to waking (Alam et al., 1995, 1996, 1997). A subset of cold-sensing neurons in these nuclei are maximally activated during waking and exhibit reduced discharge during sleep onset and NREM sleep.
Sleep in mammals is accompanied by a decrease in core body temperature (CBT). The circadian clock in the hypothalamic suprachiasmatic nucleus regulates daily rhythms in both CBT and arousal states, and these rhythms are normally coupled. Reductions in metabolic heat production resulting from behavioral quiescence and reduced muscle tone along with changes in autonomic nervous system activity and thermoeffector activity contribute to the sleep-related fall in CBT. Reductions in sympathetic tone to the peripheral vasculature resulting in heat loss through the skin are reflected in a sleep-related increase in distal skin temperature that is a prominent feature of sleep onset in humans. Within a sleep episode, patterns of autonomic nervous system and thermoeffector activity and the ability to defend against heat and cold exposure differ during nonrapid eye movement (NREM) and rapid eye movement sleep. Anatomic and functional integration of the control of arousal states and thermoregulation occur in the preoptic/anterior hypothalamus. Subsets or warm-sensing neurons in the preoptic/anterior hypothalamus implicated in CBT regulation are spontaneously activated during sleep onset and NREM sleep compared to waking and may underlie sleep-related changes in autonomic nervous system and thermoeffector activity.
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Glutamate when microinjected at the medial preoptic area (mPOA) influences brain temperature (T_br) and body temperature (T_b) in rats. Glutamate and its various receptors are present at the mPOA. The aim of this study was to identify the contribution of each of the ionotropic glutamatergic receptors at the mPOA on changes in T_br and T_b in freely moving rats. Adult male Wistar rats (n=40) were implanted with bilateral guide cannula with indwelling styli above the mPOA. A telemetric transmitter was implanted at the peritoneum to record T_b and locomotor activity (LMA). A precalibrated thermocouple wire implanted near the hypothalamus was used to assess T_br. Specific agonist for each ionotropic glutamate receptor was microinjected into the mPOA and its effects on temperature and LMA were measured in the rats. The rats were also microinjected with the respective ionotropic receptor antagonists, 15 min prior to the microinjection of each agonist. Amongst amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA), N-methyl-d-aspartate (NMDA) and kainic acid, AMPA increased T_b and LMA when injected at the mPOA. Specific antagonists for AMPA receptors was able to attenuate this increase (p<0.005). Pharmacological blockade of NMDA was able to lower T_br only. Microinjection of kainic acid and its antagonist had no effect on the variables. The finding of the study suggests that activation of the AMPA receptors at the mPOA, leads to the rise in body temperature.
GABA<inf>B</inf> receptors as a common target for hypothermia and spike and wave seizures: Intersecting mechanisms of thermoregulation and absence epilepsy
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Citation Excerpt :
Since the lesion of the preoptic hypothalamic zone induces suppression of both NREM sleep and active thermoregulation, it can be concluded that the temperature controlling regions of the preoptic hypothalamus also controls the initiation of NREM sleep (McGinty and Szymusiak, 1990, 2000; Szymusiak and McGinty, 2008). For illustration, a 2 °C local warming of the PO/AH region during wakefulness will readily facilitate sleep due to the functional dichotomy of WS neurons: the initiation of NREM sleep and thermoregulation (Alam et al., 1995, 1996). Thus, the thermoregulation and NREM sleep appear to be very closely related.
In the current study the link among the γ-hydroxybutyrate (GHB)/pentylenetetrazole (PTZ)-induced absence-like seizures and concomitant decreases in the core temperature, as well as electroencephalographic (EEG) activity during rewarming from deep hypothermia produced by a drug-free protocol were investigated. During the rewarming period after deep cooling, most Wistar rats suffered from bilaterally synchronous spike and waves with no or mild behavioral correlates. Spike and wave seizures were temperature-dependent and were initially registered when body temperature (T_b) reached 25–27 °C, but mostly during the mild hypothermia of 0.3–1.3 °C (T_b of 36.3–37.3 °C). In chemical absence models, spike and wave discharges were also closely accompanied by mild systemic hypothermia, as both PTZ- and GHB-induced temperature decreases ranged from about 1–1.4 °C respectively, together with EEG markers of absence activity. Thus, throughout the different experimental designs, the occurrence of spike and wave discharges was always related to a mild (0.3–1.4 °C) decrease of T_b. Benzodiazepine diazepam as the GABA_A-positive allosteric modulator and CGP 62349 as the selective antagonist of GABA_B receptors were used to determine if their well-known anticonvulsant properties also affect hypothermia elicited by these drugs. Finally, during the course of spontaneous rewarming from deep hypothermia, another selective GABA_B-blocking agent, CGP 35348, was used to elucidate if GABA_B inhibitory system could be critically implicated in the generation of hypothermia-dependent spike and waves. Diazepam prevented both the PTZ-induced hypothermia and electrographic absence seizures, but these two beneficial effects did not occur in the GHB model. Even though diazepam delayed GHB-induced maximal temperature decrease, the GHB effects remained highly significant. The GABA_B antagonist CGP 62349 completely prevented hypothermia as well as absence seizures in both chemical models. Likewise, spike and wave discharges, registered during the spontaneous rewarming from deep hypothermia, were completely prevented by CGP 35348. These findings show that systemic hypothermia should definitely be regarded as a marker of GABA_B receptor activation. Moreover, the results of this study clearly show that initial mild temperature decrease should be considered as strong absence-provoking factor. Hypothermia-induced nonconvulsive seizures also highlight the importance of continuous EEG monitoring in children undergoing therapeutic hypothermia after cardiac arrest. Since every change in peripheral or systemic temperature ultimately must be perceived by preoptic region of the anterior hypothalamus as the primary thermoregulatory and sleep-inducing center, the preoptic thermosensitive neurons in general and warm-sensitive neurons in particular, simply have to be regarded as the most probable candidate for connected thermoregulatory and absence generating mechanisms. Therefore, additional studies are needed to confirm their potential role in the generation and propagation of absence seizures.
Energy Expenditure. Role of Orexin.
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Apart from the stimulating energy expenditure by promoting wake and activity, orexin modulates body temperature during sleep (Mochizuki et al., 2006). Orexin may have indirect effects on sleep and thermoregulation as OXA-induced physical activity during the day may increase body temperature and the accumulation of metabolic end products that promote sleep and heat loss in a circadian manner (Alam et al., 1996; McGinty and Szymusiak, 2001). At the neural level, orexin neurons reciprocally innervate the preoptic area, which promotes sleep and heat loss (Alam et al., 1995; Kumar, 2004) and thermal stimuli to the preoptic area strongly modulates sleep propensity and EEG delta activity (Kumar, 2004).
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This chapter discusses the neurobiology of waking and sleeping. Waking and sleeping are actively generated by neuronal systems distributed through the brainstem and forebrain with different projections, discharge patterns, neurotransmitters, and receptors. Specific ascending systems stimulate cortical activation, characterized by fast, particularly gamma activity that occurs during waking and rapid eye movement (REM) sleep. In addition to glutamatergic neurons of the reticular formation and thalamus, cholinergic pontomesencephalic and basal forebrain neurons are integral components of the ascending activating system. Sleeping is initiated by inhibition of the activating and arousal systems. This inhibition is effected at multiple levels through particular GABAergic neurons which become active during sleep. Neurons in the preoptic area and basal forebrain play a particularly important role in this process. Some become active during slow-wave sleep (SWS), promoting deactivation, and slow-wave activity in the cerebral cortex. Others discharge at progressively increasing rates during SWS and REM sleep, promoting behavioral quiescence, and diminishing muscle tone. Through their projections and inhibitory neurotransmitter, they have the capacity to inhibit the monoaminergic neurons and orexin (Orx)neurons in the brainstem and hypothalamus.
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Thus far, most hypotheses on the evolutionary origin of sleep only addressed the probable origin of its main states, REM and NREM. Our article presents the origin of the whole continuum of mammalian vigilance states including waking, sleep and hibernation and the causes of the alternation NREM-REM in a sleeping episode. We propose: (1) the active state of reptiles is a form of subcortical waking, without homology with the cortical waking of mammals; (2) reptilian waking gave origin to mammalian sleep; (3) reptilian basking behaviour evolved into NREM; (4) post-basking risk assessment behaviour, with motor suspension, head dipping movements, eye scanning and stretch attending postures, evolved into phasic REM; (5) post-basking, goal directed behaviour evolved into tonic REM and (6) nocturnal rest evolved to shallow torpor. A small number of changes from previous reptilian stages explain these transformations.

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Preoptic/anterior hypothalamic neurons: thermosensitivity in wakefulness and non rapid eye movement sleep

Abstract

Brain Res. Bull.

Brain Res.

Brain Res.

Trends Neurosci.

Brain Res.

Brain Res.

Exp. Neurol.

Brain Res.

Neurosci. Lett.

Biochem. Biophys. Res. Commun.

Neuronal discharge of preoptic/anterior hypothalamic thermosensitive neurons: relation to NREM sleep

Am. J. Physiol.

Hypothalamic control of thermoregulation: neurophysiological basis

Changes in thermosensitive characteristics of hypothalamic units over time

Am. J. Physiol.

Rapid decline in body temperature before sleep: fluffing the physiological pillow?

Chronobiol. Int.

Effects of ouabain on neuronal thermosensitivity in hypothalamic tissue slices

Am. J. Physiol.

Intracellular analysis of inherent and synaptic activity in hypothalamic thermosensitive neurons in the rat

J. Physiol.

In vitro localization of thermosensitive neurons in the rat diencephalon

Am. J. Physiol.