Membrane progesterone and oestrogen receptors modulate GABAergic transmission in the prefrontal cortex of prepubertal male, but not female, mice

Abstract The sex hormones progesterone (P) and oestrogen (E) reorganize GABAergic transmission in the prefrontal cortex (PFC) during the transition from childhood to adolescence, generating a new excitatory–inhibitory balance necessary for the computational capacity of the mature PFC. Little is know...

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Main Authors: Aitana Vázquez‐Sola, Hortensia Torres‐Torrelo, Josué García Yagüe
Format: Article
Language:English
Published: Wiley 2025-06-01
Series:Experimental Physiology
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Online Access:https://doi.org/10.1113/EP092439
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author Aitana Vázquez‐Sola
Hortensia Torres‐Torrelo
Josué García Yagüe
author_facet Aitana Vázquez‐Sola
Hortensia Torres‐Torrelo
Josué García Yagüe
author_sort Aitana Vázquez‐Sola
collection DOAJ
description Abstract The sex hormones progesterone (P) and oestrogen (E) reorganize GABAergic transmission in the prefrontal cortex (PFC) during the transition from childhood to adolescence, generating a new excitatory–inhibitory balance necessary for the computational capacity of the mature PFC. Little is known, however, about the hormone receptors involved or whether there are sex differences in the modulation of GABAergic transmission they exert. We hypothesize that P and E can rapidly (within minutes) modulate GABAergic currents through G protein‐coupled receptors, namely membrane P receptors (mPRs) and the G protein‐coupled E receptor (GPER), respectively, in PFC. First, we quantified the expression of P and E receptors in PFC using quantitative RT‐PCR. Secondly, we recorded synaptic (phasic) and extrasynaptic (tonic) GABAergic currents in basal conditions and in response to the activation of mPRs and GPER using patch‐clamp recordings in PFC neurons of prepubertal female and male mice. Expression levels of mPRs differed in the PFC of females and males, but no differences were found in the basal levels of phasic or tonic GABAergic currents between sexes. Interestingly, selective activation of mPRs increased tonic GABAergic transmission in males but not in females, and activation of GPER increased phasic GABAergic transmission only in males. We also demonstrated that GABAergic modulation exerted by mPRs and GPER was dependent on protein kinase A and C. This study sheds light on new mechanisms by which P and E can rapidly modulate GABAergic transmission in PFC neurons through the activation of mPRs and GPER.
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spelling doaj-art-4de5a9b1687c4bbc8774267f2ef634a22025-08-20T03:07:05ZengWileyExperimental Physiology0958-06701469-445X2025-06-01110688889810.1113/EP092439Membrane progesterone and oestrogen receptors modulate GABAergic transmission in the prefrontal cortex of prepubertal male, but not female, miceAitana Vázquez‐Sola0Hortensia Torres‐Torrelo1Josué García Yagüe2Grupo de Neurofisiología Celular, Departamento de Ciencias Médicas Básicas, Facultad de Medicina, Instituto de Medicina Molecular Aplicada‐Nemesio Díez (IMMA‐ND)Universidad San Pablo‐CEU, CEU Universities, Urbanización Montepríncipe s/nMadridSpainGrupo de Neurofisiología Celular, Departamento de Ciencias Médicas Básicas, Facultad de Medicina, Instituto de Medicina Molecular Aplicada‐Nemesio Díez (IMMA‐ND)Universidad San Pablo‐CEU, CEU Universities, Urbanización Montepríncipe s/nMadridSpainGrupo de Neurofisiología Celular, Departamento de Ciencias Médicas Básicas, Facultad de Medicina, Instituto de Medicina Molecular Aplicada‐Nemesio Díez (IMMA‐ND)Universidad San Pablo‐CEU, CEU Universities, Urbanización Montepríncipe s/nMadridSpainAbstract The sex hormones progesterone (P) and oestrogen (E) reorganize GABAergic transmission in the prefrontal cortex (PFC) during the transition from childhood to adolescence, generating a new excitatory–inhibitory balance necessary for the computational capacity of the mature PFC. Little is known, however, about the hormone receptors involved or whether there are sex differences in the modulation of GABAergic transmission they exert. We hypothesize that P and E can rapidly (within minutes) modulate GABAergic currents through G protein‐coupled receptors, namely membrane P receptors (mPRs) and the G protein‐coupled E receptor (GPER), respectively, in PFC. First, we quantified the expression of P and E receptors in PFC using quantitative RT‐PCR. Secondly, we recorded synaptic (phasic) and extrasynaptic (tonic) GABAergic currents in basal conditions and in response to the activation of mPRs and GPER using patch‐clamp recordings in PFC neurons of prepubertal female and male mice. Expression levels of mPRs differed in the PFC of females and males, but no differences were found in the basal levels of phasic or tonic GABAergic currents between sexes. Interestingly, selective activation of mPRs increased tonic GABAergic transmission in males but not in females, and activation of GPER increased phasic GABAergic transmission only in males. We also demonstrated that GABAergic modulation exerted by mPRs and GPER was dependent on protein kinase A and C. This study sheds light on new mechanisms by which P and E can rapidly modulate GABAergic transmission in PFC neurons through the activation of mPRs and GPER.https://doi.org/10.1113/EP092439GABAergic transmissionG protein‐coupled oestrogen receptormembrane progesterone receptorprefrontal cortexsex differences
spellingShingle Aitana Vázquez‐Sola
Hortensia Torres‐Torrelo
Josué García Yagüe
Membrane progesterone and oestrogen receptors modulate GABAergic transmission in the prefrontal cortex of prepubertal male, but not female, mice
Experimental Physiology
GABAergic transmission
G protein‐coupled oestrogen receptor
membrane progesterone receptor
prefrontal cortex
sex differences
title Membrane progesterone and oestrogen receptors modulate GABAergic transmission in the prefrontal cortex of prepubertal male, but not female, mice
title_full Membrane progesterone and oestrogen receptors modulate GABAergic transmission in the prefrontal cortex of prepubertal male, but not female, mice
title_fullStr Membrane progesterone and oestrogen receptors modulate GABAergic transmission in the prefrontal cortex of prepubertal male, but not female, mice
title_full_unstemmed Membrane progesterone and oestrogen receptors modulate GABAergic transmission in the prefrontal cortex of prepubertal male, but not female, mice
title_short Membrane progesterone and oestrogen receptors modulate GABAergic transmission in the prefrontal cortex of prepubertal male, but not female, mice
title_sort membrane progesterone and oestrogen receptors modulate gabaergic transmission in the prefrontal cortex of prepubertal male but not female mice
topic GABAergic transmission
G protein‐coupled oestrogen receptor
membrane progesterone receptor
prefrontal cortex
sex differences
url https://doi.org/10.1113/EP092439
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