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Prostaglandin EP3 receptor-expressing preoptic neurons bidirectionally control body temperature via tonic GABAergic signaling.

ABSTRACT: The bidirectional controller of the thermoregulatory center in the preoptic area (POA) is unknown. Using rats, here, we identify prostaglandin EP3 receptor-expressing POA neurons (POA^EP3R neurons) as a pivotal bidirectional controller in the central thermoregulatory mechanism. POA^EP3R neurons are activated in response to elevated ambient temperature but inhibited by prostaglandin E₂, a pyrogenic mediator. Chemogenetic stimulation of POA^EP3R neurons at room temperature reduces body temperature by enhancing heat dissipation, whereas inhibition of them elicits hyperthermia involving brown fat thermogenesis, mimicking fever. POA^EP3R neurons innervate sympathoexcitatory neurons in the dorsomedial hypothalamus (DMH) via tonic (ceaseless) inhibitory signaling. Although many POA^EP3R neuronal cell bodies express a glutamatergic messenger RNA marker, their axons in the DMH predominantly release γ-aminobutyric acid (GABA), and their GABAergic terminals are increased by chronic heat exposure. These findings demonstrate that tonic GABAergic inhibitory signaling from POA^EP3R neurons is a fundamental determinant of body temperature for thermal homeostasis and fever.

SUBMITTER: Nakamura Y

PROVIDER: S-EPMC9788766 | biostudies-literature | 2022 Dec

REPOSITORIES: biostudies-literature

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Prostaglandin EP3 receptor-expressing preoptic neurons bidirectionally control body temperature via tonic GABAergic signaling.

Nakamura Yoshiko Y Yahiro Takaki T Fukushima Akihiro A Kataoka Naoya N Hioki Hiroyuki H Nakamura Kazuhiro K

Science advances 20221223 51

The bidirectional controller of the thermoregulatory center in the preoptic area (POA) is unknown. Using rats, here, we identify prostaglandin EP3 receptor-expressing POA neurons (POAEP3R neurons) as a pivotal bidirectional controller in the central thermoregulatory mechanism. POAEP3R neurons are activated in response to elevated ambient temperature but inhibited by prostaglandin E2, a pyrogenic mediator. Chemogenetic stimulation of POAEP3R neurons at ...[more]

PMID: 36563142

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Project description:Oxytocin is involved in the regulation of social behaviors including parental behaviors in a variety of species. Oxytocin triggers social behaviors by binding to oxytocin receptors (OXTRs) in various parts of the brain. OXTRs are present in the preoptic area (POA) where hormone-sensitive sexually dimorphic nuclei exist. The present study was conducted to examine whether sex differences exist in the distribution of neurons expressing OXTRs in the POA. Using OXTR-Venus (an enhanced variant of yellow fluorescent protein) mice, the distribution of OXTR-Venus cells in the POA was compared between sexes. The total number of OXTR-Venus cells in the medial POA (MPOA) was significantly greater in females than in males. No detectable OXTR-Venus cells were observed in the anteroventral periventricular nucleus (AVPV) within the MPOA in most of the brain sections from males. We further examined the total number of OXTR-Venus cells in the AVPV and the rest of the MPOA between the sexes. The total number of OXTR-Venus cells in the AVPV in females (615 ± 43) was significantly greater than that in males (14 ± 2), whereas the total number of OXTR-Venus cells in the rest of the MPOA did not differ significantly between the sexes. Thus, the sexually dimorphic expression of OXTR-Venus specifically occurred in the AVPV, but not in the rest of the MPOA. We also examined whether the expression of OXTR in the AVPV is driven by the female gonadal hormone, estrogen. Immunocytochemistry and single-cell RT-PCR revealed the presence of the estrogen receptor α in OXTR-Venus cells in the female AVPV. Moreover, ovariectomy resulted in the absence of OXTR-Venus expression in the AVPV, whereas estrogen replacement therapy restored OXTR-Venus expression. These results demonstrate that the expression of OXTR in the AVPV is primarily female specific and estrogen dependent. The presence of the sexually dimorphic expression of OXTR in the AVPV suggests the involvement of OXTR neurons in the AVPV in the regulation of female-specific behavior and/or physiology.

Dataset Information

Prostaglandin EP3 receptor-expressing preoptic neurons bidirectionally control body temperature via tonic GABAergic signaling.

Publications

Prostaglandin EP3 receptor-expressing preoptic neurons bidirectionally control body temperature via tonic GABAergic signaling.

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