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Oxytocin Neurons Enable Social Transmission of Maternal Behavior

Ioana Carcea, Naomi López Caraballo, Bianca J. Marlin, Rumi Ooyama, 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
Skirball Institute for Biomolecular Medicine, New York University School of Medicine, New York, NY, USANeuroscience Institute, New York University School of Medicine, New York, NY, USADepartment of Otolaryngology, New York University School of Medicine, New York, NY, USADepartment of Neuroscience and Physiology, New York University School of Medicine, New York, NY, USA
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Naomi López Caraballo
Skirball Institute for Biomolecular Medicine, New York University School of Medicine, New York, NY, USANeuroscience Institute, New York University School of Medicine, New York, NY, USADepartment of Otolaryngology, New York University School of Medicine, New York, NY, USADepartment of Neuroscience and Physiology, New York University School of Medicine, New York, NY, USA
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Bianca J. Marlin
Skirball Institute for Biomolecular Medicine, New York University School of Medicine, New York, NY, USANeuroscience Institute, New York University School of Medicine, New York, NY, USADepartment of Otolaryngology, New York University School of Medicine, New York, NY, USADepartment of Neuroscience and Physiology, New York University School of Medicine, New York, NY, USA
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Rumi Ooyama
Skirball Institute for Biomolecular Medicine, New York University School of Medicine, New York, NY, USANeuroscience Institute, New York University School of Medicine, New York, NY, USADepartment of Animal Science and Biotechnology, Azabu University, Sagamihara, Kanagawa, Japan
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Joyce M. Mendoza Navarro
Skirball Institute for Biomolecular Medicine, New York University School of Medicine, New York, NY, USANeuroscience Institute, New York University School of Medicine, New York, NY, USADepartment of Otolaryngology, New York University School of Medicine, New York, NY, USADepartment of Neuroscience and Physiology, New York University School of Medicine, New York, NY, USA
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Maya Opendak
Neuroscience Institute, New York University School of Medicine, New York, NY, USADepartment of Neuroscience and Physiology, New York University School of Medicine, New York, NY, USAEmotional Brain Institute, Nathan Kline Institute for Psychiatric Research, Orangeburg, NY, USADepartment of Child and Adolescent Psychiatry, New York University School of Medicine, New York, NY, USA
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Veronica E. Diaz
Skirball Institute for Biomolecular Medicine, New York University School of Medicine, New York, NY, USANeuroscience Institute, New York University School of Medicine, New York, NY, USADepartment of Otolaryngology, New York University School of Medicine, New York, NY, USADepartment of Neuroscience and Physiology, New York University School of Medicine, New York, NY, USA
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Luisa Schuster
Skirball Institute for Biomolecular Medicine, New York University School of Medicine, New York, NY, USANeuroscience Institute, New York University School of Medicine, New York, NY, USADepartment of Otolaryngology, New York University School of Medicine, New York, NY, USADepartment of Neuroscience and Physiology, New York University School of Medicine, New York, NY, USA
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Maria I. Alvarado Torres
Skirball Institute for Biomolecular Medicine, New York University School of Medicine, New York, NY, USANeuroscience Institute, New York University School of Medicine, New York, NY, USADepartment of Otolaryngology, New York University School of Medicine, New York, NY, USADepartment of Neuroscience and Physiology, New York University School of Medicine, New York, NY, USA
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Harper Lethin
Skirball Institute for Biomolecular Medicine, New York University School of Medicine, New York, NY, USANeuroscience Institute, New York University School of Medicine, New York, NY, USADepartment of Otolaryngology, New York University School of Medicine, New York, NY, USADepartment of Neuroscience and Physiology, New York University School of Medicine, New York, NY, USA
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Daniel Ramos
Skirball Institute for Biomolecular Medicine, New York University School of Medicine, New York, NY, USANeuroscience Institute, New York University School of Medicine, New York, NY, USADepartment of Otolaryngology, New York University School of Medicine, New York, NY, USADepartment of Neuroscience and Physiology, New York University School of Medicine, New York, NY, USA
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Jessica Minder
Skirball Institute for Biomolecular Medicine, New York University School of Medicine, New York, NY, USANeuroscience Institute, New York University School of Medicine, New York, NY, USADepartment of Otolaryngology, New York University School of Medicine, New York, NY, USADepartment of Neuroscience and Physiology, New York University School of Medicine, New York, NY, USA
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Sebastian L. Mendoza
Center 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
Department of Molecular and Cell Biology, Graduate School of Agricultural Science, Tohoku University, Miyagi, Japan
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Annegret Falkner
Neuroscience Institute, New York University School of Medicine, New York, NY, USADepartment of Neuroscience and Physiology, New York University School of Medicine, New York, NY, USAPrinceton Neuroscience Institute, Princeton, NJ, USADepartment of Psychiatry, New York University School of Medicine, New York, NY, USA
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Dayu Lin
Neuroscience Institute, New York University School of Medicine, New York, NY, USADepartment of Neuroscience and Physiology, New York University School of Medicine, New York, NY, USADepartment of Psychiatry, New York University School of Medicine, New York, NY, USA
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Adam Mar
Neuroscience Institute, New York University School of Medicine, New York, NY, USADepartment of Neuroscience and Physiology, New York University School of Medicine, New York, NY, USA
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Youssef Z. Wadghiri
Center 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
Department of Molecular and Cell Biology, Graduate School of Agricultural Science, Tohoku University, Miyagi, Japan
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Takefumi Kikusui
Department of Animal Science and Biotechnology, Azabu University, Sagamihara, Kanagawa, Japan
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Kazutaka Mogi
Department of Animal Science and Biotechnology, Azabu University, Sagamihara, Kanagawa, Japan
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Regina M. Sullivan
Neuroscience Institute, New York University School of Medicine, New York, NY, USADepartment of Neuroscience and Physiology, New York University School of Medicine, New York, NY, USAEmotional Brain Institute, Nathan Kline Institute for Psychiatric Research, Orangeburg, NY, USADepartment of Child and Adolescent Psychiatry, New York University School of Medicine, New York, NY, USA
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Robert C. Froemke
Skirball Institute for Biomolecular Medicine, New York University School of Medicine, New York, NY, USANeuroscience Institute, New York University School of Medicine, New York, NY, USADepartment of Otolaryngology, New York University School of Medicine, New York, NY, USADepartment of Neuroscience and Physiology, New York University School of Medicine, New York, NY, USACenter for Neural Science, New York University, New York, NY, USAHoward 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 maternal behaviors can also be expressed by non-biological parents after experience with infants. One critical molecular signal for maternal behavior is oxytocin, a hormone released in the brain 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 in vivo recordings from virgin PVN cells, including from identified oxytocin neurons. Mothers engaged virgins in maternal care by ensuring that virgins were in the nest, and demonstrated maternal behavior in self-generated pup retrieval episodes. These social interactions activated virgin PVN and gated behaviorally-relevant cortical plasticity for pup distress calls. Thus rodent maternal behavior can be learned by social transmission, and our results describe a mechanism for adapting the 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.

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Posted November 17, 2019.
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Oxytocin Neurons Enable Social Transmission of Maternal Behavior
Ioana Carcea, Naomi López Caraballo, Bianca J. Marlin, Rumi Ooyama, 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, 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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