IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-31635-3.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-31635-3
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-31635-3?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    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. 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.
    3. 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.
    4. 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.
    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.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Luis M. Franco & Michael J. Goard, 2024. "Differential stability of task variable representations in retrosplenial cortex," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    2. Hannah Muysers & Hung-Ling Chen & Johannes Hahn & Shani Folschweiller & Torfi Sigurdsson & Jonas-Frederic Sauer & Marlene Bartos, 2024. "A persistent prefrontal reference frame across time and task rules," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    3. Taylor J. Malone & Nai-Wen Tien & Yan Ma & Lian Cui & Shangru Lyu & Garret Wang & Duc Nguyen & Kai Zhang & Maxym V. Myroshnychenko & Jean Tyan & Joshua A. Gordon & David A. Kupferschmidt & Yi Gu, 2024. "A consistent map in the medial entorhinal cortex supports spatial memory," Nature Communications, Nature, vol. 15(1), pages 1-22, December.
    4. Seetha Krishnan & Chad Heer & Chery Cherian & Mark E. J. Sheffield, 2022. "Reward expectation extinction restructures and degrades CA1 spatial maps through loss of a dopaminergic reward proximity signal," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    5. 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.
    6. François G. C. Blot & Joshua J. White & Amy van Hattem & Licia Scotti & Vaishnavi Balaji & Youri Adolfs & R. Jeroen Pasterkamp & Chris I. De Zeeuw & Martijn Schonewille, 2023. "Purkinje cell microzones mediate distinct kinematics of a single movement," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    7. Yann Vanrobaeys & Utsav Mukherjee & Lucy Langmack & Stacy E. Beyer & Ethan Bahl & Li-Chun Lin & Jacob J. Michaelson & Ted Abel & Snehajyoti Chatterjee, 2023. "Mapping the spatial transcriptomic signature of the hippocampus during memory consolidation," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    8. Paul J. Lamothe-Molina & Andreas Franzelin & Lennart Beck & Dong Li & Lea Auksutat & Tim Fieblinger & Laura Laprell & Joachim Alhbeck & Christine E. Gee & Matthias Kneussel & Andreas K. Engel & Claus , 2022. "ΔFosB accumulation in hippocampal granule cells drives cFos pattern separation during spatial learning," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    9. Guillaume Etter & Suzanne Veldt & Jisoo Choi & Sylvain Williams, 2023. "Optogenetic frequency scrambling of hippocampal theta oscillations dissociates working memory retrieval from hippocampal spatiotemporal codes," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    10. E. R. Velasco & A. Florido & Á Flores & E. Senabre & A. Gomez-Gomez & A. Torres & A. Roca & S. Norrholm & E. L. Newman & P. Das & R. A. Ross & A. Lori & O. J. Pozo & K. J. Ressler & L. L. Garcia-Estev, 2022. "PACAP-PAC1R modulates fear extinction via the ventromedial hypothalamus," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    11. Ian Covert & Rohan Gala & Tim Wang & Karel Svoboda & Uygar Sümbül & Su-In Lee, 2023. "Predictive and robust gene selection for spatial transcriptomics," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    12. Vincent Douchamps & Matteo Volo & Alessandro Torcini & Demian Battaglia & Romain Goutagny, 2024. "Gamma oscillatory complexity conveys behavioral information in hippocampal networks," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    13. Thibault Cholvin & Marlene Bartos, 2022. "Hemisphere-specific spatial representation by hippocampal granule cells," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    14. Olga Gliko & Matt Mallory & Rachel Dalley & Rohan Gala & James Gornet & Hongkui Zeng & Staci A. Sorensen & Uygar Sümbül, 2024. "High-throughput analysis of dendrite and axonal arbors reveals transcriptomic correlates of neuroanatomy," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    15. Heather C. Ratigan & Seetha Krishnan & Shai Smith & Mark E. J. Sheffield, 2023. "A thalamic-hippocampal CA1 signal for contextual fear memory suppression, extinction, and discrimination," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    16. Chong Guo & Vincent Huson & Evan Z. Macosko & Wade G. Regehr, 2021. "Graded heterogeneity of metabotropic signaling underlies a continuum of cell-intrinsic temporal responses in unipolar brush cells," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    17. Alexandra T. Keinath & Coralie-Anne Mosser & Mark P. Brandon, 2022. "The representation of context in mouse hippocampus is preserved despite neural drift," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    18. Francesco Ceccarelli & Lorenzo Ferrucci & Fabrizio Londei & Surabhi Ramawat & Emiliano Brunamonti & Aldo Genovesio, 2023. "Static and dynamic coding in distinct cell types during associative learning in the prefrontal cortex," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    19. Blake J. Laham & Sahana S. Murthy & Monica Hanani & Mona Clappier & Sydney Boyer & Betsy Vasquez & Elizabeth Gould, 2022. "The estrous cycle modulates early-life adversity effects on mouse avoidance behavior through progesterone signaling," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    20. Wendy Xueyi Wang & Julie L. Lefebvre, 2022. "Morphological pseudotime ordering and fate mapping reveal diversification of cerebellar inhibitory interneurons," Nature Communications, Nature, vol. 13(1), pages 1-21, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-31635-3. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.