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Involvement of Serotonergic Projections from the Dorsal Raphe to the Medial Preoptic Area in the Regulation of the Pup-Directed Paternal Response of Male Mandarin Voles
Male mammals display different paternal responses to pups, either attacking or killing the young offspring, or contrastingly, caring for them. The neural circuit mechanism underlying the between-individual variation in the pup-directed responsiveness of male mammals remains unclear. Monogamous manda...
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Published in: | International journal of molecular sciences 2023-07, Vol.24 (14), p.11605 |
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description | Male mammals display different paternal responses to pups, either attacking or killing the young offspring, or contrastingly, caring for them. The neural circuit mechanism underlying the between-individual variation in the pup-directed responsiveness of male mammals remains unclear. Monogamous mandarin voles were used to complete the present study. The male individuals were identified as paternal and infanticidal voles, according their behavioral responses to pups. It was found that the serotonin release in the medial preoptic area (MPOA), as well as the serotonergic neuron activity, significantly increased upon licking the pups, but showed no changes after attacking the pups, as revealed by the in vivo fiber photometry of the fluorescence signal from the 5-HT 1.0 sensor and the calcium imaging indicator, respectively. It was verified that the 5-HTergic neural projections to the MPOA originated mainly from the ventral part of the dorsal raphe (vDR). Furthermore, the chemogenetic inhibition of serotonergic projections from the vDR to the MPOA decreased the paternal behaviors and shortened the latency to attack the pups. In contrast, the activation of serotonergic neurons via optogenetics extended the licking duration and inhibited infanticide. Collectively, these results elucidate that the serotonergic projections from the vDR to the MPOA, a previously unrecognized pathway, regulate the paternal responses of virgin male mandarin voles to pups. |
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The neural circuit mechanism underlying the between-individual variation in the pup-directed responsiveness of male mammals remains unclear. Monogamous mandarin voles were used to complete the present study. The male individuals were identified as paternal and infanticidal voles, according their behavioral responses to pups. It was found that the serotonin release in the medial preoptic area (MPOA), as well as the serotonergic neuron activity, significantly increased upon licking the pups, but showed no changes after attacking the pups, as revealed by the in vivo fiber photometry of the fluorescence signal from the 5-HT 1.0 sensor and the calcium imaging indicator, respectively. It was verified that the 5-HTergic neural projections to the MPOA originated mainly from the ventral part of the dorsal raphe (vDR). Furthermore, the chemogenetic inhibition of serotonergic projections from the vDR to the MPOA decreased the paternal behaviors and shortened the latency to attack the pups. In contrast, the activation of serotonergic neurons via optogenetics extended the licking duration and inhibited infanticide. Collectively, these results elucidate that the serotonergic projections from the vDR to the MPOA, a previously unrecognized pathway, regulate the paternal responses of virgin male mandarin voles to pups.</description><identifier>ISSN: 1422-0067</identifier><identifier>ISSN: 1661-6596</identifier><identifier>EISSN: 1422-0067</identifier><identifier>DOI: 10.3390/ijms241411605</identifier><identifier>PMID: 37511364</identifier><language>eng</language><publisher>Switzerland: MDPI AG</publisher><subject>Aggressiveness ; Animals ; Arvicolinae ; Behavior ; Behavior, Animal - physiology ; Casualties ; Dorsal Raphe Nucleus ; Fathers ; Humans ; infanticide ; Male ; Males ; Mental disorders ; Monogamy ; MPOA ; Neural circuitry ; Neurons ; paternal behaviors ; Preoptic Area - metabolism ; Rodents ; Sensors ; Serotonin</subject><ispartof>International journal of molecular sciences, 2023-07, Vol.24 (14), p.11605</ispartof><rights>COPYRIGHT 2023 MDPI AG</rights><rights>2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2023 by the authors. 2023</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c477t-f017ab695591cdfa3322c8a5fea4bd543d584f6124ae7f518df081b55226d4a93</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/2843072704/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/2843072704?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,25753,27924,27925,37012,37013,44590,53791,53793,74998</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37511364$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Lv, Zijian</creatorcontrib><creatorcontrib>Li, Lu</creatorcontrib><creatorcontrib>Li, Yin</creatorcontrib><creatorcontrib>Zhang, Lizi</creatorcontrib><creatorcontrib>Guo, Xing</creatorcontrib><creatorcontrib>Huang, Caihong</creatorcontrib><creatorcontrib>Hou, Wenjuan</creatorcontrib><creatorcontrib>Qu, Yishan</creatorcontrib><creatorcontrib>Liu, Limin</creatorcontrib><creatorcontrib>Li, Yitong</creatorcontrib><creatorcontrib>He, Zhixiong</creatorcontrib><creatorcontrib>Tai, Fadao</creatorcontrib><title>Involvement of Serotonergic Projections from the Dorsal Raphe to the Medial Preoptic Area in the Regulation of the Pup-Directed Paternal Response of Male Mandarin Voles</title><title>International journal of molecular sciences</title><addtitle>Int J Mol Sci</addtitle><description>Male mammals display different paternal responses to pups, either attacking or killing the young offspring, or contrastingly, caring for them. The neural circuit mechanism underlying the between-individual variation in the pup-directed responsiveness of male mammals remains unclear. Monogamous mandarin voles were used to complete the present study. The male individuals were identified as paternal and infanticidal voles, according their behavioral responses to pups. It was found that the serotonin release in the medial preoptic area (MPOA), as well as the serotonergic neuron activity, significantly increased upon licking the pups, but showed no changes after attacking the pups, as revealed by the in vivo fiber photometry of the fluorescence signal from the 5-HT 1.0 sensor and the calcium imaging indicator, respectively. It was verified that the 5-HTergic neural projections to the MPOA originated mainly from the ventral part of the dorsal raphe (vDR). Furthermore, the chemogenetic inhibition of serotonergic projections from the vDR to the MPOA decreased the paternal behaviors and shortened the latency to attack the pups. In contrast, the activation of serotonergic neurons via optogenetics extended the licking duration and inhibited infanticide. Collectively, these results elucidate that the serotonergic projections from the vDR to the MPOA, a previously unrecognized pathway, regulate the paternal responses of virgin male mandarin voles to pups.</description><subject>Aggressiveness</subject><subject>Animals</subject><subject>Arvicolinae</subject><subject>Behavior</subject><subject>Behavior, Animal - physiology</subject><subject>Casualties</subject><subject>Dorsal Raphe Nucleus</subject><subject>Fathers</subject><subject>Humans</subject><subject>infanticide</subject><subject>Male</subject><subject>Males</subject><subject>Mental disorders</subject><subject>Monogamy</subject><subject>MPOA</subject><subject>Neural circuitry</subject><subject>Neurons</subject><subject>paternal behaviors</subject><subject>Preoptic Area - metabolism</subject><subject>Rodents</subject><subject>Sensors</subject><subject>Serotonin</subject><issn>1422-0067</issn><issn>1661-6596</issn><issn>1422-0067</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><sourceid>DOA</sourceid><recordid>eNpdkk1v1DAQhiMEoqVw5IoiceGS4s84OaFVS2GlVqzKx9Vy7HHqVRIHO1mJf9SfibNbqi7ywfbrd56xx5NlbzE6p7RGH922j4RhhnGJ-LPsFDNCCoRK8fzJ-iR7FeMWIUIJr19mJ1RwjGnJTrP79bDz3Q56GKbc2_w7BD_5AULrdL4Jfgt6cn6IuQ2-z6c7yC99iKrLb9WYNpPfazdgXNI2Afw4pcBVAJW7YX92C-3cqQWy8BdlM4_FpQuJDCbfqAnCsAAhjikRLK4b1SWoGowKifLLdxBfZy-s6iK8eZjPsp9Xn39cfC2uv31ZX6yuC82EmAqLsFBNWXNeY22sopQQXSluQbHGcEYNr5gtMWEKhOW4MhZVuOGckNIwVdOzbH3gGq-2cgyuV-GP9MrJveBDK1VIb-xAGtIQwRUpecMZ06JCKSNlGNG60ZhXifXpwBrnpgejU42D6o6gxyeDu5Ot38mEqJAgNBE-PBCC_z1DnGTvooauUwP4OUpSMYZqVlUsWd__Z936eans3kUTTqDFdX5wtanE0g3Wp8Q6DQO90-njrUv6SqTycVKL5QbFIUAHH2MA-3h9jOTSgfKoA5P_3dM3P7r_tRz9C9bj2Fg</recordid><startdate>20230718</startdate><enddate>20230718</enddate><creator>Lv, Zijian</creator><creator>Li, Lu</creator><creator>Li, Yin</creator><creator>Zhang, Lizi</creator><creator>Guo, Xing</creator><creator>Huang, Caihong</creator><creator>Hou, Wenjuan</creator><creator>Qu, Yishan</creator><creator>Liu, Limin</creator><creator>Li, Yitong</creator><creator>He, Zhixiong</creator><creator>Tai, Fadao</creator><general>MDPI AG</general><general>MDPI</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>3V.</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>8G5</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BENPR</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>GUQSH</scope><scope>K9.</scope><scope>M0S</scope><scope>M1P</scope><scope>M2O</scope><scope>MBDVC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>Q9U</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20230718</creationdate><title>Involvement of Serotonergic Projections from the Dorsal Raphe to the Medial Preoptic Area in the Regulation of the Pup-Directed Paternal Response of Male Mandarin Voles</title><author>Lv, Zijian ; Li, Lu ; Li, Yin ; Zhang, Lizi ; Guo, Xing ; Huang, Caihong ; Hou, Wenjuan ; Qu, Yishan ; Liu, Limin ; Li, Yitong ; He, Zhixiong ; Tai, Fadao</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c477t-f017ab695591cdfa3322c8a5fea4bd543d584f6124ae7f518df081b55226d4a93</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Aggressiveness</topic><topic>Animals</topic><topic>Arvicolinae</topic><topic>Behavior</topic><topic>Behavior, Animal - physiology</topic><topic>Casualties</topic><topic>Dorsal Raphe Nucleus</topic><topic>Fathers</topic><topic>Humans</topic><topic>infanticide</topic><topic>Male</topic><topic>Males</topic><topic>Mental disorders</topic><topic>Monogamy</topic><topic>MPOA</topic><topic>Neural circuitry</topic><topic>Neurons</topic><topic>paternal behaviors</topic><topic>Preoptic Area - metabolism</topic><topic>Rodents</topic><topic>Sensors</topic><topic>Serotonin</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Lv, Zijian</creatorcontrib><creatorcontrib>Li, Lu</creatorcontrib><creatorcontrib>Li, Yin</creatorcontrib><creatorcontrib>Zhang, Lizi</creatorcontrib><creatorcontrib>Guo, Xing</creatorcontrib><creatorcontrib>Huang, Caihong</creatorcontrib><creatorcontrib>Hou, Wenjuan</creatorcontrib><creatorcontrib>Qu, Yishan</creatorcontrib><creatorcontrib>Liu, Limin</creatorcontrib><creatorcontrib>Li, Yitong</creatorcontrib><creatorcontrib>He, Zhixiong</creatorcontrib><creatorcontrib>Tai, Fadao</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>ProQuest Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Research Library (Alumni Edition)</collection><collection>ProQuest Central (Alumni)</collection><collection>ProQuest Central</collection><collection>ProQuest Central Essentials</collection><collection>AUTh Library subscriptions: ProQuest Central</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>Research Library Prep</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>PML(ProQuest Medical Library)</collection><collection>ProQuest_Research Library</collection><collection>Research Library (Corporate)</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>ProQuest Central Basic</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>Directory of Open Access Journals</collection><jtitle>International journal of molecular sciences</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Lv, Zijian</au><au>Li, Lu</au><au>Li, Yin</au><au>Zhang, Lizi</au><au>Guo, Xing</au><au>Huang, Caihong</au><au>Hou, Wenjuan</au><au>Qu, Yishan</au><au>Liu, Limin</au><au>Li, Yitong</au><au>He, Zhixiong</au><au>Tai, Fadao</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Involvement of Serotonergic Projections from the Dorsal Raphe to the Medial Preoptic Area in the Regulation of the Pup-Directed Paternal Response of Male Mandarin Voles</atitle><jtitle>International journal of molecular sciences</jtitle><addtitle>Int J Mol Sci</addtitle><date>2023-07-18</date><risdate>2023</risdate><volume>24</volume><issue>14</issue><spage>11605</spage><pages>11605-</pages><issn>1422-0067</issn><issn>1661-6596</issn><eissn>1422-0067</eissn><abstract>Male mammals display different paternal responses to pups, either attacking or killing the young offspring, or contrastingly, caring for them. The neural circuit mechanism underlying the between-individual variation in the pup-directed responsiveness of male mammals remains unclear. Monogamous mandarin voles were used to complete the present study. The male individuals were identified as paternal and infanticidal voles, according their behavioral responses to pups. It was found that the serotonin release in the medial preoptic area (MPOA), as well as the serotonergic neuron activity, significantly increased upon licking the pups, but showed no changes after attacking the pups, as revealed by the in vivo fiber photometry of the fluorescence signal from the 5-HT 1.0 sensor and the calcium imaging indicator, respectively. It was verified that the 5-HTergic neural projections to the MPOA originated mainly from the ventral part of the dorsal raphe (vDR). Furthermore, the chemogenetic inhibition of serotonergic projections from the vDR to the MPOA decreased the paternal behaviors and shortened the latency to attack the pups. In contrast, the activation of serotonergic neurons via optogenetics extended the licking duration and inhibited infanticide. Collectively, these results elucidate that the serotonergic projections from the vDR to the MPOA, a previously unrecognized pathway, regulate the paternal responses of virgin male mandarin voles to pups.</abstract><cop>Switzerland</cop><pub>MDPI AG</pub><pmid>37511364</pmid><doi>10.3390/ijms241411605</doi><oa>free_for_read</oa></addata></record> |
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subjects | Aggressiveness Animals Arvicolinae Behavior Behavior, Animal - physiology Casualties Dorsal Raphe Nucleus Fathers Humans infanticide Male Males Mental disorders Monogamy MPOA Neural circuitry Neurons paternal behaviors Preoptic Area - metabolism Rodents Sensors Serotonin |
title | Involvement of Serotonergic Projections from the Dorsal Raphe to the Medial Preoptic Area in the Regulation of the Pup-Directed Paternal Response of Male Mandarin Voles |
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