Sex differences in neural projections of fear memory processing in mice and humans
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)- fibers in the lateral posterior BNST (BNSTpl) decreased fear memory consolid...
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| creator | Florido, Antonio Velasco, Eric R Romero, Leire R Acharya, Neha Marin Blasco, Ignacio J Nabás, Jaime F Perez-Caballero, Laura Rivero, Guadalupe Olabarrieta, Estíbaliz Nuñez-delMoral, Amaia González-Parra, Jose A Porta-Casteràs, Daniel Cano, Marta Steward, Trevor Antony, Monica S Cardoner, Narcís Torrubia, Rafael Jackson, Alexander C Fullana, Miquel A Andero, Raül |
| description | 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)-
fibers in the lateral posterior BNST (BNSTpl) decreased fear memory consolidation in male mice but not females. Optogenetic excitation of CeM-
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) (
) decreased CeM-BNST connectivity in a fear task, impaired fear memory consolidation, and increased the expression of the
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. |
| doi_str_mv | 10.1126/sciadv.adk3365 |
| format | Article |
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fibers in the lateral posterior BNST (BNSTpl) decreased fear memory consolidation in male mice but not females. Optogenetic excitation of CeM-
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) (
) decreased CeM-BNST connectivity in a fear task, impaired fear memory consolidation, and increased the expression of the
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.</description><identifier>ISSN: 2375-2548</identifier><identifier>EISSN: 2375-2548</identifier><identifier>DOI: 10.1126/sciadv.adk3365</identifier><identifier>PMID: 38985873</identifier><language>eng</language><publisher>United States: American Association for the Advancement of Science</publisher><subject>Adult ; Animals ; Fear - physiology ; Female ; Humans ; Male ; Memory - physiology ; Mice ; Neuroscience ; Polymorphism, Single Nucleotide ; SciAdv r-articles ; Sex Characteristics</subject><ispartof>Science advances, 2024-07, Vol.10 (28), p.eadk3365</ispartof><rights>Copyright © 2024 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC). 2024 The Authors</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c236t-497ef7e2dd53a7acc53ea35dd1368870c35d14412feedfacac7645ee6b0430643</cites><orcidid>0000-0002-2537-4047 ; 0000-0002-1749-7055 ; 0000-0002-5040-0913 ; 0009-0008-7296-7671 ; 0000-0003-3641-8903 ; 0000-0003-3116-8175 ; 0000-0003-0675-9483 ; 0000-0002-6826-6572 ; 0000-0001-7489-3946 ; 0000-0003-3863-5223 ; 0000-0002-2315-2213 ; 0000-0002-3921-3607 ; 0000-0001-5096-2871 ; 0000-0001-6184-0706 ; 0000-0001-7842-3298 ; 0000-0002-8778-5618</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC11235172/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC11235172/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38985873$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Florido, Antonio</creatorcontrib><creatorcontrib>Velasco, Eric R</creatorcontrib><creatorcontrib>Romero, Leire R</creatorcontrib><creatorcontrib>Acharya, Neha</creatorcontrib><creatorcontrib>Marin Blasco, Ignacio J</creatorcontrib><creatorcontrib>Nabás, Jaime F</creatorcontrib><creatorcontrib>Perez-Caballero, Laura</creatorcontrib><creatorcontrib>Rivero, Guadalupe</creatorcontrib><creatorcontrib>Olabarrieta, Estíbaliz</creatorcontrib><creatorcontrib>Nuñez-delMoral, Amaia</creatorcontrib><creatorcontrib>González-Parra, Jose A</creatorcontrib><creatorcontrib>Porta-Casteràs, Daniel</creatorcontrib><creatorcontrib>Cano, Marta</creatorcontrib><creatorcontrib>Steward, Trevor</creatorcontrib><creatorcontrib>Antony, Monica S</creatorcontrib><creatorcontrib>Cardoner, Narcís</creatorcontrib><creatorcontrib>Torrubia, Rafael</creatorcontrib><creatorcontrib>Jackson, Alexander C</creatorcontrib><creatorcontrib>Fullana, Miquel A</creatorcontrib><creatorcontrib>Andero, Raül</creatorcontrib><title>Sex differences in neural projections of fear memory processing in mice and humans</title><title>Science advances</title><addtitle>Sci Adv</addtitle><description>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)-
fibers in the lateral posterior BNST (BNSTpl) decreased fear memory consolidation in male mice but not females. Optogenetic excitation of CeM-
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) (
) decreased CeM-BNST connectivity in a fear task, impaired fear memory consolidation, and increased the expression of the
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.</description><subject>Adult</subject><subject>Animals</subject><subject>Fear - physiology</subject><subject>Female</subject><subject>Humans</subject><subject>Male</subject><subject>Memory - physiology</subject><subject>Mice</subject><subject>Neuroscience</subject><subject>Polymorphism, Single Nucleotide</subject><subject>SciAdv r-articles</subject><subject>Sex Characteristics</subject><issn>2375-2548</issn><issn>2375-2548</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpVkc1PAjEQxRujEYJcPZoevYDtdtsuJ2OIX4mJiR_nprRTKLIttiyR_94lIMHTTPJ-8-ZlBqFLSoaUFuImG6_teqjtF2OCn6BuwSQfFLysTo_6DurnPCeE0FIITkfnqMOqUcUrybro7R1-sPXOQYJgIGMfcIAm6QVepjgHs_IxZBwddqATrqGOabOVWjb7MN3ytTeAdbB41tQ65At05vQiQ39fe-jz4f5j_DR4eX18Ht-9DEzBxGpQjiQ4CYW1nGmpjeEMNOPWUiaqShLT9rQsaeEArNNGGylKDiAmpGRElKyHbne-y2ZSgzUQVm1stUy-1mmjovbqvxL8TE3jWrW3Y5zKonW43juk-N1AXqnaZwOLhQ4Qm6wYkZWknHPWosMdalLMOYE77KFkayjU7hlq_4x24Oo43QH_Oz37BeuYiYI</recordid><startdate>20240712</startdate><enddate>20240712</enddate><creator>Florido, Antonio</creator><creator>Velasco, Eric R</creator><creator>Romero, Leire R</creator><creator>Acharya, Neha</creator><creator>Marin Blasco, Ignacio J</creator><creator>Nabás, Jaime F</creator><creator>Perez-Caballero, Laura</creator><creator>Rivero, Guadalupe</creator><creator>Olabarrieta, Estíbaliz</creator><creator>Nuñez-delMoral, Amaia</creator><creator>González-Parra, Jose A</creator><creator>Porta-Casteràs, Daniel</creator><creator>Cano, Marta</creator><creator>Steward, Trevor</creator><creator>Antony, Monica S</creator><creator>Cardoner, Narcís</creator><creator>Torrubia, Rafael</creator><creator>Jackson, Alexander C</creator><creator>Fullana, Miquel A</creator><creator>Andero, Raül</creator><general>American Association for the Advancement of Science</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-2537-4047</orcidid><orcidid>https://orcid.org/0000-0002-1749-7055</orcidid><orcidid>https://orcid.org/0000-0002-5040-0913</orcidid><orcidid>https://orcid.org/0009-0008-7296-7671</orcidid><orcidid>https://orcid.org/0000-0003-3641-8903</orcidid><orcidid>https://orcid.org/0000-0003-3116-8175</orcidid><orcidid>https://orcid.org/0000-0003-0675-9483</orcidid><orcidid>https://orcid.org/0000-0002-6826-6572</orcidid><orcidid>https://orcid.org/0000-0001-7489-3946</orcidid><orcidid>https://orcid.org/0000-0003-3863-5223</orcidid><orcidid>https://orcid.org/0000-0002-2315-2213</orcidid><orcidid>https://orcid.org/0000-0002-3921-3607</orcidid><orcidid>https://orcid.org/0000-0001-5096-2871</orcidid><orcidid>https://orcid.org/0000-0001-6184-0706</orcidid><orcidid>https://orcid.org/0000-0001-7842-3298</orcidid><orcidid>https://orcid.org/0000-0002-8778-5618</orcidid></search><sort><creationdate>20240712</creationdate><title>Sex differences in neural projections of fear memory processing in mice and humans</title><author>Florido, Antonio ; 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Here, we show that chemogenetic silencing of centromedial (CeM)-
fibers in the lateral posterior BNST (BNSTpl) decreased fear memory consolidation in male mice but not females. Optogenetic excitation of CeM-
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) (
) decreased CeM-BNST connectivity in a fear task, impaired fear memory consolidation, and increased the expression of the
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.</abstract><cop>United States</cop><pub>American Association for the Advancement of Science</pub><pmid>38985873</pmid><doi>10.1126/sciadv.adk3365</doi><orcidid>https://orcid.org/0000-0002-2537-4047</orcidid><orcidid>https://orcid.org/0000-0002-1749-7055</orcidid><orcidid>https://orcid.org/0000-0002-5040-0913</orcidid><orcidid>https://orcid.org/0009-0008-7296-7671</orcidid><orcidid>https://orcid.org/0000-0003-3641-8903</orcidid><orcidid>https://orcid.org/0000-0003-3116-8175</orcidid><orcidid>https://orcid.org/0000-0003-0675-9483</orcidid><orcidid>https://orcid.org/0000-0002-6826-6572</orcidid><orcidid>https://orcid.org/0000-0001-7489-3946</orcidid><orcidid>https://orcid.org/0000-0003-3863-5223</orcidid><orcidid>https://orcid.org/0000-0002-2315-2213</orcidid><orcidid>https://orcid.org/0000-0002-3921-3607</orcidid><orcidid>https://orcid.org/0000-0001-5096-2871</orcidid><orcidid>https://orcid.org/0000-0001-6184-0706</orcidid><orcidid>https://orcid.org/0000-0001-7842-3298</orcidid><orcidid>https://orcid.org/0000-0002-8778-5618</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Adult Animals Fear - physiology Female Humans Male Memory - physiology Mice Neuroscience Polymorphism, Single Nucleotide SciAdv r-articles Sex Characteristics |
| title | Sex differences in neural projections of fear memory processing in mice and humans |
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