Antagonistic circuits mediating infanticide and maternal care in female mice

In many species, including mice, female animals show markedly different pup-directed behaviours based on their reproductive state 1 , 2 . Naive wild female mice often kill pups, while lactating female mice are dedicated to pup caring 3 , 4 . The neural mechanisms that mediate infanticide and its swi...

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Vydáno v:	Nature (London) Ročník 618; číslo 7967; s. 1006 - 1016
Hlavní autoři:	Mei, Long, Yan, Rongzhen, Yin, Luping, Sullivan, Regina M., Lin, Dayu
Médium:	Journal Article
Jazyk:	angličtina
Vydáno:	London Nature Publishing Group UK 29.06.2023 Nature Publishing Group
Témata:	13/51 631/378/3919 631/378/3920 64/60 9/74 Animals Behavior Brain ESR1 protein Estrogen receptors Excitability Female Females Humanities and Social Sciences Hypothalamus Hypotheses Infanticide Laboratories Lactation Maternal behavior Maternal Behavior - physiology Mice multidisciplinary Neural Pathways - physiology Preoptic area Preoptic area (medial) Preoptic Area - cytology Preoptic Area - physiology Reproductive behavior Science Science (multidisciplinary) Stria terminalis Thalamus - cytology Thalamus - physiology
ISSN:	0028-0836, 1476-4687, 1476-4687
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Abstract	In many species, including mice, female animals show markedly different pup-directed behaviours based on their reproductive state 1 , 2 . Naive wild female mice often kill pups, while lactating female mice are dedicated to pup caring 3 , 4 . The neural mechanisms that mediate infanticide and its switch to maternal behaviours during motherhood remain unclear. Here, on the basis of the hypothesis that maternal and infanticidal behaviours are supported by distinct and competing neural circuits 5 , 6 , we use the medial preoptic area (MPOA), a key site for maternal behaviours 7 – 11 , as a starting point and identify three MPOA-connected brain regions that drive differential negative pup-directed behaviours. Functional manipulation and in vivo recording reveal that oestrogen receptor α (ESR1)-expressing cells in the principal nucleus of the bed nucleus of stria terminalis (BNSTpr ESR1 ) are necessary, sufficient and naturally activated during infanticide in female mice. MPOA ESR1 and BNSTpr ESR1 neurons form reciprocal inhibition to control the balance between positive and negative infant-directed behaviours. During motherhood, MPOA ESR1 and BNSTpr ESR1 cells change their excitability in opposite directions, supporting a marked switch of female behaviours towards the young. ESR1-expressing cells in the principal nucleus of the bed nucleus of stria terminalis are necessary, sufficient and naturally activated during infanticide, and they form reciprocal inhibition with the maternal cells to control young-directed behaviours in female mice.
AbstractList	In many species, including mice, female animals show markedly different pup-directed behaviours based on their reproductive state1,2. Naive wild female mice often kill pups, while lactating female mice are dedicated to pup caring3,4. The neural mechanisms that mediate infanticide and its switch to maternal behaviours during motherhood remain unclear. Here, on the basis of the hypothesis that maternal and infanticidal behaviours are supported by distinct and competing neural circuits5,6, we use the medial preoptic area (MPOA), a key site for maternal behaviours7-11, as a starting point and identify three MPOA-connected brain regions that drive differential negative pup-directed behaviours. Functional manipulation and in vivo recording reveal that oestrogen receptor a (ESR1)-expressing cells in the principal nucleus of the bed nucleus of stria terminalis (BNSTprESR1) are necessary, sufficient and naturally activated during infanticide in female mice. MPOAESR1 and BNSTprESR1 neurons form reciprocal inhibition to control the balance between positive and negative infant-directed behaviours. During motherhood, MPOAESR1 and BNSTprESR1 cells change their excitability in opposite directions, supporting a marked switch of female behaviours towards the young. In many species, including mice, female animals show markedly different pup-directed behaviours based on their reproductive state 1 , 2 . Naive wild female mice often kill pups, while lactating female mice are dedicated to pup caring 3 , 4 . The neural mechanisms that mediate infanticide and its switch to maternal behaviours during motherhood remain unclear. Here, on the basis of the hypothesis that maternal and infanticidal behaviours are supported by distinct and competing neural circuits 5 , 6 , we use the medial preoptic area (MPOA), a key site for maternal behaviours 7 – 11 , as a starting point and identify three MPOA-connected brain regions that drive differential negative pup-directed behaviours. Functional manipulation and in vivo recording reveal that oestrogen receptor α (ESR1)-expressing cells in the principal nucleus of the bed nucleus of stria terminalis (BNSTpr ESR1 ) are necessary, sufficient and naturally activated during infanticide in female mice. MPOA ESR1 and BNSTpr ESR1 neurons form reciprocal inhibition to control the balance between positive and negative infant-directed behaviours. During motherhood, MPOA ESR1 and BNSTpr ESR1 cells change their excitability in opposite directions, supporting a marked switch of female behaviours towards the young. ESR1-expressing cells in the principal nucleus of the bed nucleus of stria terminalis are necessary, sufficient and naturally activated during infanticide, and they form reciprocal inhibition with the maternal cells to control young-directed behaviours in female mice. In many species, including mice, females show strikingly different pup-directed behaviors based on their reproductive state1,2. Naïve wild female mice often kill pups, while lactating females are dedicated to pup caring3,4. The neural mechanisms that mediate infanticide and its switch to maternal behaviors during motherhood remain unclear. Here, based on the hypothesis that maternal and infanticidal behaviors are supported by distinct and competing neural circuits5,6, we used the medial preoptic area (MPOA), a key site for maternal behaviors7–11, as a starting point and identified three MPOA-connected brain regions that drive differential negative pup-directed behaviors. Further functional manipulation and in vivo recording revealed that estrogen receptor alpha (Esr1) expressing cells in the principal nucleus of the bed nucleus of stria terminalis (BNSTprEsr1) are necessary, sufficient, and naturally activated during infanticide in female mice. MPOAEsr1 and BNSTprEsr1 neurons form reciprocal inhibition to control the balance between positive and negative infant-directed behaviors. During motherhood, MPOAEsr1 and BNSTprEsr1 cells change their excitability in opposite directions, supporting a drastic switch of female behaviors towards the young. In many species, including mice, female animals show markedly different pup-directed behaviours based on their reproductive state . Naive wild female mice often kill pups, while lactating female mice are dedicated to pup caring . The neural mechanisms that mediate infanticide and its switch to maternal behaviours during motherhood remain unclear. Here, on the basis of the hypothesis that maternal and infanticidal behaviours are supported by distinct and competing neural circuits , we use the medial preoptic area (MPOA), a key site for maternal behaviours , as a starting point and identify three MPOA-connected brain regions that drive differential negative pup-directed behaviours. Functional manipulation and in vivo recording reveal that oestrogen receptor α (ESR1)-expressing cells in the principal nucleus of the bed nucleus of stria terminalis (BNSTpr ) are necessary, sufficient and naturally activated during infanticide in female mice. MPOA and BNSTpr neurons form reciprocal inhibition to control the balance between positive and negative infant-directed behaviours. During motherhood, MPOA and BNSTpr cells change their excitability in opposite directions, supporting a marked switch of female behaviours towards the young. In many species, including mice, female animals show markedly different pup-directed behaviours based on their reproductive state1,2. Naive wild female mice often kill pups, while lactating female mice are dedicated to pup caring3,4. The neural mechanisms that mediate infanticide and its switch to maternal behaviours during motherhood remain unclear. Here, on the basis of the hypothesis that maternal and infanticidal behaviours are supported by distinct and competing neural circuits5,6, we use the medial preoptic area (MPOA), a key site for maternal behaviours7-11, as a starting point and identify three MPOA-connected brain regions that drive differential negative pup-directed behaviours. Functional manipulation and in vivo recording reveal that oestrogen receptor α (ESR1)-expressing cells in the principal nucleus of the bed nucleus of stria terminalis (BNSTprESR1) are necessary, sufficient and naturally activated during infanticide in female mice. MPOAESR1 and BNSTprESR1 neurons form reciprocal inhibition to control the balance between positive and negative infant-directed behaviours. During motherhood, MPOAESR1 and BNSTprESR1 cells change their excitability in opposite directions, supporting a marked switch of female behaviours towards the young.In many species, including mice, female animals show markedly different pup-directed behaviours based on their reproductive state1,2. Naive wild female mice often kill pups, while lactating female mice are dedicated to pup caring3,4. The neural mechanisms that mediate infanticide and its switch to maternal behaviours during motherhood remain unclear. Here, on the basis of the hypothesis that maternal and infanticidal behaviours are supported by distinct and competing neural circuits5,6, we use the medial preoptic area (MPOA), a key site for maternal behaviours7-11, as a starting point and identify three MPOA-connected brain regions that drive differential negative pup-directed behaviours. Functional manipulation and in vivo recording reveal that oestrogen receptor α (ESR1)-expressing cells in the principal nucleus of the bed nucleus of stria terminalis (BNSTprESR1) are necessary, sufficient and naturally activated during infanticide in female mice. MPOAESR1 and BNSTprESR1 neurons form reciprocal inhibition to control the balance between positive and negative infant-directed behaviours. During motherhood, MPOAESR1 and BNSTprESR1 cells change their excitability in opposite directions, supporting a marked switch of female behaviours towards the young.
Author	Sullivan, Regina M. Yan, Rongzhen Yin, Luping Lin, Dayu Mei, Long
AuthorAffiliation	3 Department of Psychiatry, New York University Langone Medical Center, New York, NY, USA; Center for Neural Science, New York University, New York, NY, USA 2 Emotional Brain Institute, Nathan Kline Institute, Child and Adolescent Psychiatry, New York University Langone Medical Center, New York, NY USA 1 Neuroscience Institute, New York University Langone Medical Center, New York, NY, USA
AuthorAffiliation_xml	– name: 1 Neuroscience Institute, New York University Langone Medical Center, New York, NY, USA – name: 2 Emotional Brain Institute, Nathan Kline Institute, Child and Adolescent Psychiatry, New York University Langone Medical Center, New York, NY USA – name: 3 Department of Psychiatry, New York University Langone Medical Center, New York, NY, USA; Center for Neural Science, New York University, New York, NY, USA
Author_xml	– sequence: 1 givenname: Long orcidid: 0000-0003-1434-2389 surname: Mei fullname: Mei, Long email: Long.Mei@nyulangone.org organization: Neuroscience Institute, New York University Langone Medical Center – sequence: 2 givenname: Rongzhen surname: Yan fullname: Yan, Rongzhen organization: Neuroscience Institute, New York University Langone Medical Center – sequence: 3 givenname: Luping surname: Yin fullname: Yin, Luping organization: Neuroscience Institute, New York University Langone Medical Center – sequence: 4 givenname: Regina M. surname: Sullivan fullname: Sullivan, Regina M. organization: Emotional Brain Institute, Nathan Kline Institute, Child and Adolescent Psychiatry, New York University Langone Medical Center – sequence: 5 givenname: Dayu orcidid: 0000-0003-2006-0791 surname: Lin fullname: Lin, Dayu email: Dayu.Lin@nyulangone.org organization: Neuroscience Institute, New York University Langone Medical Center, Department of Psychiatry, New York University Langone Medical Center, Center for Neural Science, New York University
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/37286598$$D View this record in MEDLINE/PubMed
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Copyright	The Author(s), under exclusive licence to Springer Nature Limited 2023. Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law. 2023. The Author(s), under exclusive licence to Springer Nature Limited. Copyright Nature Publishing Group Jun 29, 2023
Copyright_xml	– notice: The Author(s), under exclusive licence to Springer Nature Limited 2023. Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law. – notice: 2023. The Author(s), under exclusive licence to Springer Nature Limited. – notice: Copyright Nature Publishing Group Jun 29, 2023
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Notes	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Author Contribution statement Equal contribution D.L. and M.L. conceived the project, designed experiments, analyzed data and wrote the paper. D.L. supervised the project. M.L. performed most experiments and prepared figures. R.Y. and L.Y. performed slice recording experiments and prepared related figures. R.S. provided critical feedback on the experiments.
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Snippet	In many species, including mice, female animals show markedly different pup-directed behaviours based on their reproductive state 1 , 2 . Naive wild female... In many species, including mice, female animals show markedly different pup-directed behaviours based on their reproductive state . Naive wild female mice... In many species, including mice, female animals show markedly different pup-directed behaviours based on their reproductive state1,2. Naive wild female mice... In many species, including mice, females show strikingly different pup-directed behaviors based on their reproductive state1,2. Naïve wild female mice often...
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SubjectTerms	13/51 631/378/3919 631/378/3920 64/60 9/74 Animals Behavior Brain ESR1 protein Estrogen receptors Excitability Female Females Humanities and Social Sciences Hypothalamus Hypotheses Infanticide Laboratories Lactation Maternal behavior Maternal Behavior - physiology Mice multidisciplinary Neural Pathways - physiology Preoptic area Preoptic area (medial) Preoptic Area - cytology Preoptic Area - physiology Reproductive behavior Science Science (multidisciplinary) Stria terminalis Thalamus - cytology Thalamus - physiology
Title	Antagonistic circuits mediating infanticide and maternal care in female mice
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