Oxytocin neurons enable social transmission of maternal behaviour

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, Chloe J. Bair-Marshall, Grace H. Samadjopoulos, Shizu Hidema, Annegret Falkner, Dayu Lin, Adam Mar, Youssef Z. Wadghiri, Katsuhiko Nishimori, Takefumi Kikusui, Kazutaka Mogi, Regina M. Sullivan and Robert C. Froemke ()
Additional contact information
Ioana Carcea: New York University School of Medicine
Naomi López Caraballo: New York University School of Medicine
Bianca J. Marlin: New York University School of Medicine
Rumi Ooyama: New York University School of Medicine
Justin S. Riceberg: Mount Sinai School of Medicine
Joyce M. Mendoza Navarro: New York University School of Medicine
Maya Opendak: New York University School of Medicine
Veronica E. Diaz: New York University School of Medicine
Luisa Schuster: New York University School of Medicine
Maria I. Alvarado Torres: New York University School of Medicine
Harper Lethin: New York University School of Medicine
Daniel Ramos: New York University School of Medicine
Jessica Minder: New York University School of Medicine
Sebastian L. Mendoza: New York University School of Medicine
Chloe J. Bair-Marshall: New York University School of Medicine
Grace H. Samadjopoulos: The State University of New Jersey
Shizu Hidema: Department of Obesity and Internal Inflammation, Fukushima Medical University
Annegret Falkner: New York University School of Medicine
Dayu Lin: New York University School of Medicine
Adam Mar: New York University School of Medicine
Youssef Z. Wadghiri: New York University School of Medicine
Katsuhiko Nishimori: Department of Obesity and Internal Inflammation, Fukushima Medical University
Takefumi Kikusui: Azabu University
Kazutaka Mogi: Azabu University
Regina M. Sullivan: New York University School of Medicine
Robert C. Froemke: New York University School of Medicine

Nature, 2021, vol. 596, issue 7873, 553-557

Abstract: Abstract Maternal care, including by non-biological parents, is important for offspring survival1–8. Oxytocin1,2,9–15, which is released by the hypothalamic paraventricular nucleus (PVN), is a critical maternal hormone. In mice, oxytocin enables neuroplasticity in the auditory cortex for maternal recognition of pup distress15. However, it is unclear how initial parental experience promotes hypothalamic signalling and cortical plasticity for reliable maternal care. Here we continuously monitored the behaviour of female virgin mice co-housed with an experienced mother and litter. This documentary approach was synchronized with neural recordings from the virgin PVN, including oxytocin neurons. These cells were activated as virgins were enlisted in maternal care by experienced mothers, who shepherded virgins into the nest and demonstrated pup retrieval. Virgins visually observed maternal retrieval, which activated PVN oxytocin neurons and promoted alloparenting. Thus rodents can acquire maternal behaviour by social transmission, providing a mechanism for adapting the brains of adult caregivers to infant needs via endogenous oxytocin.

Date: 2021
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DOI: 10.1038/s41586-021-03814-7

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