Sex differences in neural projections of fear memory processing in mice and humans

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  • dc.contributor.author Florido Torres, Antonio Luis
  • dc.contributor.author Velasco, Eric R.
  • dc.contributor.author Romero, Leire R.
  • dc.contributor.author Acharya, Neha
  • dc.contributor.author Marin Blasco, Ignacio J.
  • dc.contributor.author Nabás, Jaime F.
  • dc.contributor.author Pérez-Caballero, Laura
  • dc.contributor.author Rivero, Guadalupe
  • dc.contributor.author Olabarrieta, Estíbaliz
  • dc.contributor.author Nuñez-delMoral, Amaia
  • dc.contributor.author González-Parra, Jose Antonio
  • dc.contributor.author Porta-Casteràs, Daniel
  • dc.contributor.author Cano, Marta
  • dc.contributor.author Steward, Trevor
  • dc.contributor.author Antony, Monica S.
  • dc.contributor.author Cardoner, Narcís
  • dc.contributor.author Torrubia, Rafael
  • dc.contributor.author Jackson, Alexander C.
  • dc.contributor.author Fullana Rivas, Miguel Ángel
  • dc.contributor.author Andero, Raül
  • dc.date.accessioned 2025-07-17T06:07:57Z
  • dc.date.available 2025-07-17T06:07:57Z
  • dc.date.issued 2024
  • dc.description.abstract It remains unexplored in the field of fear memory whether functional neuronal connectivity between two brain areas is necessary for one sex but not the other. Here, we show that chemogenetic silencing of centromedial (CeM)-Tac2 fibers in the lateral posterior BNST (BNSTpl) decreased fear memory consolidation in male mice but not females. Optogenetic excitation of CeM-Tac2 fibers in the BNSTpl exhibited enhanced inhibitory postsynaptic currents in males compared to females. In vivo calcium imaging analysis revealed a sex-dimorphic fear memory engram in the BNSTpl. Furthermore, in humans, the single-nucleotide polymorphism (SNP) in the Tac2 receptor (rs2765) (TAC3R) decreased CeM-BNST connectivity in a fear task, impaired fear memory consolidation, and increased the expression of the TAC3R mRNA in AA-carrier men but not in women. These sex differences in critical neuronal circuits underlying fear memory formation may be relevant to human neuropsychiatric disorders with fear memory alterations such as posttraumatic stress disorder.
  • dc.description.sponsorship A.F. was a recipient of the Generalitat de Catalunya predoctoral fellowship FI_B00030. E.R.V. was supported by a BES-2017-080870 FPI-2017 fellowship from MINECO. L.R.R. was supported by a PRE2021-099771 fellowship from MINECO. L.P.C. was supported by an FJC2018-037958-I (MCIU). D.P.-C. was supported by a FI19/00251 fellowship from ISCIII. G.R. and E.O. were supported by the Basque Government (IT1512/22). A.N. was a recipient of a predoctoral fellowship from the Basque Government. T.S. was supported by an NHMRC/MRFF Investigator Grant (MRF1193736), a BBRF Young Investigator Grant, and a University of Melbourne McKenzie Fellowship. M.C. was funded by a Sara Borrell postdoctoral contract (CD20/00189). N.C. was supported by ERANET-Neuron JTC 2019 ISCIII AC19/00088. M.S.A. and A.C.J. are supported by the NIH (R01MH112739 to A.C.J.). R.A. was supported by ERANET-Neuron JTC 2019 ISCIII AC19/00077, Fundacion Koplowitz, RETOS-MINECO PID2020-112705RB-I00 funded by MCIN/AEI/10.13039/501100011033, by “ERDF, A way of making Europe” and MCIN/AEI/10.13039/501100011033, La Caixa HR22-00737, and REIS MCIN/AEI/10.13039/501100011033. R.A.’s work was also produced with the support of a 2022 Leonardo Grant for Researchers and Cultural Creators, and the foundation takes no responsibility for the opinions, statements, and contents of this project, which are entirely the responsibility of its authors.
  • dc.format.mimetype application/pdf
  • dc.identifier.citation Florido A, Velasco ER, Romero LR, Acharya N, Marin Blasco IJ, Nabás JF, et al. Sex differences in neural projections of fear memory processing in mice and humans. Sci Adv. 2024 Jul 12;10(28):eadk3365. DOI: 10.1126/sciadv.adk3365
  • dc.identifier.doi http://dx.doi.org/10.1126/sciadv.adk3365
  • dc.identifier.issn 2375-2548
  • dc.identifier.uri http://hdl.handle.net/10230/70939
  • dc.language.iso eng
  • dc.publisher American Association for the Advancement of Science (AAAS)
  • dc.relation.ispartof Sci Adv. 2024 Jul 12;10(28):eadk3365
  • dc.relation.projectID info:eu-repo/grantAgreement/ES/2PE/PID2020-112705RB-I00
  • dc.rights This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial license (http://creativecommons.org/licenses/by-nc/4.0/), which permits use, distribution, and reproduction in any medium, so long as the resultant use is not for commercial advantage and provided the original work is properly cited.
  • dc.rights.accessRights info:eu-repo/semantics/openAccess
  • dc.rights.uri http://creativecommons.org/licenses/by-nc/4.0/
  • dc.subject.other Circuit neuronal
  • dc.title Sex differences in neural projections of fear memory processing in mice and humans
  • dc.type info:eu-repo/semantics/article
  • dc.type.version info:eu-repo/semantics/publishedVersion

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