Becoming a mother entails anatomical changes in the ventral striatum of the human brain that facilitate its responsiveness to offspring cues
•Pregnancy renders anatomical reductions in the human ventral striatum (VStr).•VStr decreases are associated with stronger responses to offspring cues in the VStr.•Pregnancy may adaptively tune the reward circuit to promote offspring responsivity. In mothers, offspring cues are associated with a pow...
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creator | Hoekzema, Elseline Tamnes, Christian K. Berns, Puck Barba-Müller, Erika Pozzobon, Cristina Picado, Marisol Lucco, Florencio Martínez-García, Magdalena Desco, Manuel Ballesteros, Agustín Crone, Eveline A. Vilarroya, Oscar Carmona, Susanna |
description | •Pregnancy renders anatomical reductions in the human ventral striatum (VStr).•VStr decreases are associated with stronger responses to offspring cues in the VStr.•Pregnancy may adaptively tune the reward circuit to promote offspring responsivity.
In mothers, offspring cues are associated with a powerful reinforcing value that motivates maternal care. Animal studies show that this is mediated by dopamine release into the nucleus accumbens, a core component of the brain’s reward system located in the ventral striatum (VStr). The VStr is also known to respond to infant signals in human mothers. However, it is unknown whether pregnancy modifies the anatomy or functionality of this structure, and whether such modifications underlie its strong reactivity to offspring cues. Therefore, we analyzed structural and functional neuroimaging data from a unique pre-conception prospective cohort study involving first-time mothers investigated before and after their pregnancy as well as nulliparous control women scanned at similar time intervals. First, we delineated the anatomy of the VStr in each subject’s neuroanatomical space and examined whether there are volumetric changes in this structure across sessions. Then, we tested if these changes could predict the mothers’ brain responses to visual stimuli of their infants. We found decreases in the right VStr and a trend for left VStr reductions in the women who were pregnant between sessions compared to the women who were not. Furthermore, VStr volume reductions across pregnancy were associated with infant-related VStr responses in the postpartum period, with stronger volume decreases predicting stronger functional activation to offspring cues. These findings provide the first indications that the transition to motherhood renders anatomical adaptations in the VStr that promote the strong responsiveness of a mother’s reward circuit to cues of her infant. |
doi_str_mv | 10.1016/j.psyneuen.2019.104507 |
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In mothers, offspring cues are associated with a powerful reinforcing value that motivates maternal care. Animal studies show that this is mediated by dopamine release into the nucleus accumbens, a core component of the brain’s reward system located in the ventral striatum (VStr). The VStr is also known to respond to infant signals in human mothers. However, it is unknown whether pregnancy modifies the anatomy or functionality of this structure, and whether such modifications underlie its strong reactivity to offspring cues. Therefore, we analyzed structural and functional neuroimaging data from a unique pre-conception prospective cohort study involving first-time mothers investigated before and after their pregnancy as well as nulliparous control women scanned at similar time intervals. First, we delineated the anatomy of the VStr in each subject’s neuroanatomical space and examined whether there are volumetric changes in this structure across sessions. Then, we tested if these changes could predict the mothers’ brain responses to visual stimuli of their infants. We found decreases in the right VStr and a trend for left VStr reductions in the women who were pregnant between sessions compared to the women who were not. Furthermore, VStr volume reductions across pregnancy were associated with infant-related VStr responses in the postpartum period, with stronger volume decreases predicting stronger functional activation to offspring cues. These findings provide the first indications that the transition to motherhood renders anatomical adaptations in the VStr that promote the strong responsiveness of a mother’s reward circuit to cues of her infant.</description><identifier>ISSN: 0306-4530</identifier><identifier>EISSN: 1873-3360</identifier><identifier>DOI: 10.1016/j.psyneuen.2019.104507</identifier><identifier>PMID: 31757430</identifier><language>eng</language><publisher>England: Elsevier Ltd</publisher><subject>Adult ; Cues ; Facial Recognition - physiology ; Female ; Humans ; Magnetic Resonance Imaging ; Maternal Behavior - physiology ; Maternal brain ; MRI ; Neuroimaging ; Nucleus accumbens ; Parity ; Postpartum Period - physiology ; Pregnancy ; Pregnancy - physiology ; Prospective Studies ; Reward ; Reward circuit ; Ventral striatum ; Ventral Striatum - anatomy & histology ; Ventral Striatum - diagnostic imaging ; Ventral Striatum - physiology</subject><ispartof>Psychoneuroendocrinology, 2020-02, Vol.112, p.104507-104507, Article 104507</ispartof><rights>2019 The Authors</rights><rights>Copyright © 2019 The Authors. Published by Elsevier Ltd.. All rights reserved.</rights><rights>info:eu-repo/semantics/openAccess</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c440t-f9384b2c9bdca6004c653e9a552a64877b66b9a0c8994785b9b6db1dfcddaed93</citedby><cites>FETCH-LOGICAL-c440t-f9384b2c9bdca6004c653e9a552a64877b66b9a0c8994785b9b6db1dfcddaed93</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S030645301931248X$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>230,314,776,780,881,3537,26544,27901,27902,65306</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31757430$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Hoekzema, Elseline</creatorcontrib><creatorcontrib>Tamnes, Christian K.</creatorcontrib><creatorcontrib>Berns, Puck</creatorcontrib><creatorcontrib>Barba-Müller, Erika</creatorcontrib><creatorcontrib>Pozzobon, Cristina</creatorcontrib><creatorcontrib>Picado, Marisol</creatorcontrib><creatorcontrib>Lucco, Florencio</creatorcontrib><creatorcontrib>Martínez-García, Magdalena</creatorcontrib><creatorcontrib>Desco, Manuel</creatorcontrib><creatorcontrib>Ballesteros, Agustín</creatorcontrib><creatorcontrib>Crone, Eveline A.</creatorcontrib><creatorcontrib>Vilarroya, Oscar</creatorcontrib><creatorcontrib>Carmona, Susanna</creatorcontrib><title>Becoming a mother entails anatomical changes in the ventral striatum of the human brain that facilitate its responsiveness to offspring cues</title><title>Psychoneuroendocrinology</title><addtitle>Psychoneuroendocrinology</addtitle><description>•Pregnancy renders anatomical reductions in the human ventral striatum (VStr).•VStr decreases are associated with stronger responses to offspring cues in the VStr.•Pregnancy may adaptively tune the reward circuit to promote offspring responsivity.
In mothers, offspring cues are associated with a powerful reinforcing value that motivates maternal care. Animal studies show that this is mediated by dopamine release into the nucleus accumbens, a core component of the brain’s reward system located in the ventral striatum (VStr). The VStr is also known to respond to infant signals in human mothers. However, it is unknown whether pregnancy modifies the anatomy or functionality of this structure, and whether such modifications underlie its strong reactivity to offspring cues. Therefore, we analyzed structural and functional neuroimaging data from a unique pre-conception prospective cohort study involving first-time mothers investigated before and after their pregnancy as well as nulliparous control women scanned at similar time intervals. First, we delineated the anatomy of the VStr in each subject’s neuroanatomical space and examined whether there are volumetric changes in this structure across sessions. Then, we tested if these changes could predict the mothers’ brain responses to visual stimuli of their infants. We found decreases in the right VStr and a trend for left VStr reductions in the women who were pregnant between sessions compared to the women who were not. Furthermore, VStr volume reductions across pregnancy were associated with infant-related VStr responses in the postpartum period, with stronger volume decreases predicting stronger functional activation to offspring cues. These findings provide the first indications that the transition to motherhood renders anatomical adaptations in the VStr that promote the strong responsiveness of a mother’s reward circuit to cues of her infant.</description><subject>Adult</subject><subject>Cues</subject><subject>Facial Recognition - physiology</subject><subject>Female</subject><subject>Humans</subject><subject>Magnetic Resonance Imaging</subject><subject>Maternal Behavior - physiology</subject><subject>Maternal brain</subject><subject>MRI</subject><subject>Neuroimaging</subject><subject>Nucleus accumbens</subject><subject>Parity</subject><subject>Postpartum Period - physiology</subject><subject>Pregnancy</subject><subject>Pregnancy - physiology</subject><subject>Prospective Studies</subject><subject>Reward</subject><subject>Reward circuit</subject><subject>Ventral striatum</subject><subject>Ventral Striatum - anatomy & histology</subject><subject>Ventral Striatum - diagnostic imaging</subject><subject>Ventral Striatum - physiology</subject><issn>0306-4530</issn><issn>1873-3360</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>3HK</sourceid><recordid>eNqFkc1u1DAUhSMEotPCKxQv2WRw4p_EO6CCglSJDaytG-em41FiD75Opb4DD42n02HLytLxd86176mq64ZvG97oD_vtgR4Drhi2LW9MEaXi3Ytq0_SdqIXQ_GW14YLrWirBL6pLoj3nXPe6fV1diKZTnRR8U_35jC4uPtwzYEvMO0wMQwY_E4MAuVw5mJnbQbhHYj6wgrCHgqQiU04e8rqwOD3pu3WBwIYETxxkNoHzs8-QkflMLCEdYiBf_EjEcizGiQ7pON6tSG-qVxPMhG-fz6vq19cvP2--1Xc_br_ffLqrnZQ815MRvRxaZ4bRgeZcOq0EGlCqBS37rhu0Hgxw1xsju14NZtDj0IyTG0fA0Yir6t0p1yVP2QcbYgLb8F61tpNGykK8PxGHFH-Xl2W7eHI4zxAwrmTb4waNanpVUH0Oi0QJJ1s-tEB6LIH22JXd23NX9tiVPXVVjNfPM9ZhwfGf7VxOAT6eACy7ePCYLDmPweHoE7psx-j_N-MvA56rRA</recordid><startdate>20200201</startdate><enddate>20200201</enddate><creator>Hoekzema, Elseline</creator><creator>Tamnes, Christian K.</creator><creator>Berns, Puck</creator><creator>Barba-Müller, Erika</creator><creator>Pozzobon, Cristina</creator><creator>Picado, Marisol</creator><creator>Lucco, Florencio</creator><creator>Martínez-García, Magdalena</creator><creator>Desco, Manuel</creator><creator>Ballesteros, Agustín</creator><creator>Crone, Eveline A.</creator><creator>Vilarroya, Oscar</creator><creator>Carmona, Susanna</creator><general>Elsevier Ltd</general><scope>6I.</scope><scope>AAFTH</scope><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>3HK</scope></search><sort><creationdate>20200201</creationdate><title>Becoming a mother entails anatomical changes in the ventral striatum of the human brain that facilitate its responsiveness to offspring cues</title><author>Hoekzema, Elseline ; Tamnes, Christian K. ; Berns, Puck ; Barba-Müller, Erika ; Pozzobon, Cristina ; Picado, Marisol ; Lucco, Florencio ; Martínez-García, Magdalena ; Desco, Manuel ; Ballesteros, Agustín ; Crone, Eveline A. ; Vilarroya, Oscar ; Carmona, Susanna</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c440t-f9384b2c9bdca6004c653e9a552a64877b66b9a0c8994785b9b6db1dfcddaed93</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Adult</topic><topic>Cues</topic><topic>Facial Recognition - physiology</topic><topic>Female</topic><topic>Humans</topic><topic>Magnetic Resonance Imaging</topic><topic>Maternal Behavior - physiology</topic><topic>Maternal brain</topic><topic>MRI</topic><topic>Neuroimaging</topic><topic>Nucleus accumbens</topic><topic>Parity</topic><topic>Postpartum Period - physiology</topic><topic>Pregnancy</topic><topic>Pregnancy - physiology</topic><topic>Prospective Studies</topic><topic>Reward</topic><topic>Reward circuit</topic><topic>Ventral striatum</topic><topic>Ventral Striatum - anatomy & histology</topic><topic>Ventral Striatum - diagnostic imaging</topic><topic>Ventral Striatum - physiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Hoekzema, Elseline</creatorcontrib><creatorcontrib>Tamnes, Christian K.</creatorcontrib><creatorcontrib>Berns, Puck</creatorcontrib><creatorcontrib>Barba-Müller, Erika</creatorcontrib><creatorcontrib>Pozzobon, Cristina</creatorcontrib><creatorcontrib>Picado, Marisol</creatorcontrib><creatorcontrib>Lucco, Florencio</creatorcontrib><creatorcontrib>Martínez-García, Magdalena</creatorcontrib><creatorcontrib>Desco, Manuel</creatorcontrib><creatorcontrib>Ballesteros, Agustín</creatorcontrib><creatorcontrib>Crone, Eveline A.</creatorcontrib><creatorcontrib>Vilarroya, Oscar</creatorcontrib><creatorcontrib>Carmona, Susanna</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>NORA - Norwegian Open Research Archives</collection><jtitle>Psychoneuroendocrinology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Hoekzema, Elseline</au><au>Tamnes, Christian K.</au><au>Berns, Puck</au><au>Barba-Müller, Erika</au><au>Pozzobon, Cristina</au><au>Picado, Marisol</au><au>Lucco, Florencio</au><au>Martínez-García, Magdalena</au><au>Desco, Manuel</au><au>Ballesteros, Agustín</au><au>Crone, Eveline A.</au><au>Vilarroya, Oscar</au><au>Carmona, Susanna</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Becoming a mother entails anatomical changes in the ventral striatum of the human brain that facilitate its responsiveness to offspring cues</atitle><jtitle>Psychoneuroendocrinology</jtitle><addtitle>Psychoneuroendocrinology</addtitle><date>2020-02-01</date><risdate>2020</risdate><volume>112</volume><spage>104507</spage><epage>104507</epage><pages>104507-104507</pages><artnum>104507</artnum><issn>0306-4530</issn><eissn>1873-3360</eissn><abstract>•Pregnancy renders anatomical reductions in the human ventral striatum (VStr).•VStr decreases are associated with stronger responses to offspring cues in the VStr.•Pregnancy may adaptively tune the reward circuit to promote offspring responsivity.
In mothers, offspring cues are associated with a powerful reinforcing value that motivates maternal care. Animal studies show that this is mediated by dopamine release into the nucleus accumbens, a core component of the brain’s reward system located in the ventral striatum (VStr). The VStr is also known to respond to infant signals in human mothers. However, it is unknown whether pregnancy modifies the anatomy or functionality of this structure, and whether such modifications underlie its strong reactivity to offspring cues. Therefore, we analyzed structural and functional neuroimaging data from a unique pre-conception prospective cohort study involving first-time mothers investigated before and after their pregnancy as well as nulliparous control women scanned at similar time intervals. First, we delineated the anatomy of the VStr in each subject’s neuroanatomical space and examined whether there are volumetric changes in this structure across sessions. Then, we tested if these changes could predict the mothers’ brain responses to visual stimuli of their infants. We found decreases in the right VStr and a trend for left VStr reductions in the women who were pregnant between sessions compared to the women who were not. Furthermore, VStr volume reductions across pregnancy were associated with infant-related VStr responses in the postpartum period, with stronger volume decreases predicting stronger functional activation to offspring cues. These findings provide the first indications that the transition to motherhood renders anatomical adaptations in the VStr that promote the strong responsiveness of a mother’s reward circuit to cues of her infant.</abstract><cop>England</cop><pub>Elsevier Ltd</pub><pmid>31757430</pmid><doi>10.1016/j.psyneuen.2019.104507</doi><tpages>1</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Adult Cues Facial Recognition - physiology Female Humans Magnetic Resonance Imaging Maternal Behavior - physiology Maternal brain MRI Neuroimaging Nucleus accumbens Parity Postpartum Period - physiology Pregnancy Pregnancy - physiology Prospective Studies Reward Reward circuit Ventral striatum Ventral Striatum - anatomy & histology Ventral Striatum - diagnostic imaging Ventral Striatum - physiology |
title | Becoming a mother entails anatomical changes in the ventral striatum of the human brain that facilitate its responsiveness to offspring cues |
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