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Oxytocin Neurons Enable Social Transmission of Maternal Behavior

Ioana Carcea, Naomi López Caraballo, Bianca J. Marlin, Rumi Ooyama, Justin S. Riceberg, Joyce M. Mendoza Navarro, Maya Opendak, Veronica E. Diaz, Luisa Schuster, Maria I. Alvarado Torres, Harper Lethin, Daniel Ramos, Jessica Minder, Sebastian L. Mendoza, Shizu Hidema, Annegret Falkner, Dayu Lin, Adam Mar, Youssef Z. Wadghiri, Katsuhiko Nishimori, Takefumi Kikusui, Kazutaka Mogi, Regina M. Sullivan, Robert C. Froemke
doi: https://doi.org/10.1101/845495
Ioana Carcea
1Skirball Institute for Biomolecular Medicine
2Neuroscience Institute
3Department of Otolaryngology
4Department of Neuroscience and Physiology, New York University School of Medicine, New York, NY, USA
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Naomi López Caraballo
1Skirball Institute for Biomolecular Medicine
2Neuroscience Institute
3Department of Otolaryngology
4Department of Neuroscience and Physiology, New York University School of Medicine, New York, NY, USA
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Bianca J. Marlin
1Skirball Institute for Biomolecular Medicine
2Neuroscience Institute
3Department of Otolaryngology
4Department of Neuroscience and Physiology, New York University School of Medicine, New York, NY, USA
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Rumi Ooyama
1Skirball Institute for Biomolecular Medicine
2Neuroscience Institute
5Department of Animal Science and Biotechnology, Azabu University, Sagamihara, Kanagawa, Japan
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Justin S. Riceberg
6Department of Neuroscience, Mount Sinai School of Medicine, New York, NY, USA
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Joyce M. Mendoza Navarro
1Skirball Institute for Biomolecular Medicine
2Neuroscience Institute
3Department of Otolaryngology
4Department of Neuroscience and Physiology, New York University School of Medicine, New York, NY, USA
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Maya Opendak
2Neuroscience Institute
4Department of Neuroscience and Physiology, New York University School of Medicine, New York, NY, USA
7Emotional Brain Institute, Nathan Kline Institute for Psychiatric Research, Orangeburg, NY, USA
8Department of Child and Adolescent Psychiatry, New York University School of Medicine, New York, NY, USA
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Veronica E. Diaz
1Skirball Institute for Biomolecular Medicine
2Neuroscience Institute
3Department of Otolaryngology
4Department of Neuroscience and Physiology, New York University School of Medicine, New York, NY, USA
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Luisa Schuster
1Skirball Institute for Biomolecular Medicine
2Neuroscience Institute
3Department of Otolaryngology
4Department of Neuroscience and Physiology, New York University School of Medicine, New York, NY, USA
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Maria I. Alvarado Torres
1Skirball Institute for Biomolecular Medicine
2Neuroscience Institute
3Department of Otolaryngology
4Department of Neuroscience and Physiology, New York University School of Medicine, New York, NY, USA
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Harper Lethin
1Skirball Institute for Biomolecular Medicine
2Neuroscience Institute
3Department of Otolaryngology
4Department of Neuroscience and Physiology, New York University School of Medicine, New York, NY, USA
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Daniel Ramos
1Skirball Institute for Biomolecular Medicine
2Neuroscience Institute
3Department of Otolaryngology
4Department of Neuroscience and Physiology, New York University School of Medicine, New York, NY, USA
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Jessica Minder
1Skirball Institute for Biomolecular Medicine
2Neuroscience Institute
3Department of Otolaryngology
4Department of Neuroscience and Physiology, New York University School of Medicine, New York, NY, USA
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Sebastian L. Mendoza
9Center for Advanced Imaging Innovation and Research, Bernard and Irene Schwartz Center for Biomedical Imaging, Department of Radiology, New York University School of Medicine, New York, NY, USA
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Shizu Hidema
10Department of Molecular and Cell Biology, Graduate School of Agricultural Science, Tohoku University, Miyagi, Japan
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Annegret Falkner
2Neuroscience Institute
4Department of Neuroscience and Physiology, New York University School of Medicine, New York, NY, USA
11Department of Psychiatry, New York University School of Medicine, New York, NY, USA
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Dayu Lin
2Neuroscience Institute
4Department of Neuroscience and Physiology, New York University School of Medicine, New York, NY, USA
11Department of Psychiatry, New York University School of Medicine, New York, NY, USA
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Adam Mar
2Neuroscience Institute
4Department of Neuroscience and Physiology, New York University School of Medicine, New York, NY, USA
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Youssef Z. Wadghiri
9Center for Advanced Imaging Innovation and Research, Bernard and Irene Schwartz Center for Biomedical Imaging, Department of Radiology, New York University School of Medicine, New York, NY, USA
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Katsuhiko Nishimori
10Department of Molecular and Cell Biology, Graduate School of Agricultural Science, Tohoku University, Miyagi, Japan
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Takefumi Kikusui
5Department of Animal Science and Biotechnology, Azabu University, Sagamihara, Kanagawa, Japan
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Kazutaka Mogi
5Department of Animal Science and Biotechnology, Azabu University, Sagamihara, Kanagawa, Japan
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Regina M. Sullivan
2Neuroscience Institute
4Department of Neuroscience and Physiology, New York University School of Medicine, New York, NY, USA
7Emotional Brain Institute, Nathan Kline Institute for Psychiatric Research, Orangeburg, NY, USA
8Department of Child and Adolescent Psychiatry, New York University School of Medicine, New York, NY, USA
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Robert C. Froemke
1Skirball Institute for Biomolecular Medicine
2Neuroscience Institute
3Department of Otolaryngology
4Department of Neuroscience and Physiology, New York University School of Medicine, New York, NY, USA
12Center for Neural Science, New York University, New York, NY, USA
13Howard Hughes Medical Institute Faculty Scholar
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  • For correspondence: robert.froemke@med.nyu.edu
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Abstract

Maternal care is profoundly important for mammalian survival, and non-biological parents can express it after experience with infants. One critical molecular signal for maternal behavior is oxytocin, a hormone centrally released by hypothalamic paraventricular nucleus (PVN). Oxytocin enables plasticity within the auditory cortex, a necessary step for responding to infant vocalizations. To determine how this change occurs during natural experience, we continuously monitored homecage behavior of female virgin mice co-housed for days with an experienced mother and litter, synchronized with recordings from virgin PVN cells, including from oxytocin neurons. Mothers engaged virgins in maternal care by ensuring their nest presence, and demonstrated maternal behavior in self-generated pup retrieval episodes. These social interactions activated virgin PVN and gated behaviorally-relevant cortical plasticity for pup vocalizations. Thus rodents can acquire maternal behavior by social transmission, and our results describe a mechanism for adapting brains of adult caregivers to infant needs via endogenous oxytocin.

One Sentence Summary Mother mice help co-housed virgins become maternal by enacting specific behaviors that activate virgin oxytocin neurons.

Footnotes

  • Response to first round of reviewer comments.

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Oxytocin Neurons Enable Social Transmission of Maternal Behavior
Ioana Carcea, Naomi López Caraballo, Bianca J. Marlin, Rumi Ooyama, Justin S. Riceberg, Joyce M. Mendoza Navarro, Maya Opendak, Veronica E. Diaz, Luisa Schuster, Maria I. Alvarado Torres, Harper Lethin, Daniel Ramos, Jessica Minder, Sebastian L. Mendoza, Shizu Hidema, Annegret Falkner, Dayu Lin, Adam Mar, Youssef Z. Wadghiri, Katsuhiko Nishimori, Takefumi Kikusui, Kazutaka Mogi, Regina M. Sullivan, Robert C. Froemke
bioRxiv 845495; doi: https://doi.org/10.1101/845495
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Oxytocin Neurons Enable Social Transmission of Maternal Behavior
Ioana Carcea, Naomi López Caraballo, Bianca J. Marlin, Rumi Ooyama, Justin S. Riceberg, Joyce M. Mendoza Navarro, Maya Opendak, Veronica E. Diaz, Luisa Schuster, Maria I. Alvarado Torres, Harper Lethin, Daniel Ramos, Jessica Minder, Sebastian L. Mendoza, Shizu Hidema, Annegret Falkner, Dayu Lin, Adam Mar, Youssef Z. Wadghiri, Katsuhiko Nishimori, Takefumi Kikusui, Kazutaka Mogi, Regina M. Sullivan, Robert C. Froemke
bioRxiv 845495; doi: https://doi.org/10.1101/845495

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