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Sex-specific regulation of inhibition and network activity by local aromatase in the mouse hippocampus

Author

Listed:
  • Alicia Hernández-Vivanco

    (Instituto Cajal (CSIC))

  • Nuria Cano-Adamuz

    (Instituto Cajal (CSIC))

  • Alberto Sánchez-Aguilera

    (Instituto Cajal (CSIC)
    Universidad Complutense de Madrid IdISSC)

  • Alba González-Alonso

    (Instituto Cajal (CSIC))

  • Alberto Rodríguez-Fernández

    (Instituto Cajal (CSIC))

  • Íñigo Azcoitia

    (Universidad Complutense de Madrid
    Centro de Investigación Biomédica en Red de Fragilidad y Envejecimiento Saludable (CIBERFES))

  • Liset Menendez de la Prida

    (Instituto Cajal (CSIC))

  • Pablo Méndez

    (Instituto Cajal (CSIC))

Abstract

Cognitive function relies on a balanced interplay between excitatory and inhibitory neurons (INs), but the impact of estradiol on IN function is not fully understood. Here, we characterize the regulation of hippocampal INs by aromatase, the enzyme responsible for estradiol synthesis, using a combination of molecular, genetic, functional and behavioral tools. The results show that CA1 parvalbumin-expressing INs (PV-INs) contribute to brain estradiol synthesis. Brain aromatase regulates synaptic inhibition through a mechanism that involves modification of perineuronal nets enwrapping PV-INs. In the female brain, aromatase modulates PV-INs activity, the dynamics of network oscillations and hippocampal-dependent memory. Aromatase regulation of PV-INs and inhibitory synapses is determined by the gonads and independent of sex chromosomes. These results suggest PV-INs are mediators of estrogenic regulation of behaviorally-relevant activity.

Suggested Citation

  • Alicia Hernández-Vivanco & Nuria Cano-Adamuz & Alberto Sánchez-Aguilera & Alba González-Alonso & Alberto Rodríguez-Fernández & Íñigo Azcoitia & Liset Menendez de la Prida & Pablo Méndez, 2022. "Sex-specific regulation of inhibition and network activity by local aromatase in the mouse hippocampus," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-31635-3
    DOI: 10.1038/s41467-022-31635-3
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    1. Ane Charlotte Christensen & Kristian Kinden Lensjø & Mikkel Elle Lepperød & Svenn-Arne Dragly & Halvard Sutterud & Jan Sigurd Blackstad & Marianne Fyhn & Torkel Hafting, 2021. "Perineuronal nets stabilize the grid cell network," Nature Communications, Nature, vol. 12(1), pages 1-17, December.
    2. A. Florido & E. R. Velasco & C. M. Soto-Faguás & A. Gomez-Gomez & L. Perez-Caballero & P. Molina & R. Nadal & O. J. Pozo & C. A. Saura & R. Andero, 2021. "Sex differences in fear memory consolidation via Tac2 signaling in mice," Nature Communications, Nature, vol. 12(1), pages 1-19, December.
    3. Kenneth D Harris & Hannah Hochgerner & Nathan G Skene & Lorenza Magno & Linda Katona & Carolina Bengtsson Gonzales & Peter Somogyi & Nicoletta Kessaris & Sten Linnarsson & Jens Hjerling-Leffler, 2018. "Classes and continua of hippocampal CA1 inhibitory neurons revealed by single-cell transcriptomics," PLOS Biology, Public Library of Science, vol. 16(6), pages 1-37, June.
    4. Flavio Donato & Santiago Belluco Rompani & Pico Caroni, 2013. "Parvalbumin-expressing basket-cell network plasticity induced by experience regulates adult learning," Nature, Nature, vol. 504(7479), pages 272-276, December.
    5. Thomas Hainmueller & Marlene Bartos, 2018. "Parallel emergence of stable and dynamic memory engrams in the hippocampus," Nature, Nature, vol. 558(7709), pages 292-296, June.
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