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; Robert C. Froemke

doi:10.1038/s41586-021-03814-7

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 MarYoussef Z. Wadghiri, Katsuhiko Nishimori, Takefumi Kikusui, Kazutaka Mogi, Regina M. Sullivan, Robert C. Froemke

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Abstract

Maternal care, including by non-biological parents, is important for offspring survival^1–8. Oxytocin^1,2,9–15, 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.

Original language	English
Pages (from-to)	553-557
Number of pages	5
Journal	Nature
Volume	596
Issue number	7873
DOIs	https://doi.org/10.1038/s41586-021-03814-7
State	Published - 26 Aug 2021

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Carcea, I., Caraballo, N. L., Marlin, B. J., Ooyama, R., Riceberg, J. S., Mendoza Navarro, J. M., Opendak, M., Diaz, V. E., Schuster, L., Alvarado Torres, M. I., Lethin, H., Ramos, D., Minder, J., Mendoza, S. L., Bair-Marshall, C. J., Samadjopoulos, G. H., Hidema, S., Falkner, A., Lin, D., ... Froemke, R. C. (2021). Oxytocin neurons enable social transmission of maternal behaviour. Nature, 596(7873), 553-557. https://doi.org/10.1038/s41586-021-03814-7

@article{aa6179edb897465bad80a35f87e7f8aa,

title = "Oxytocin neurons enable social transmission of maternal behaviour",

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.",

author = "Ioana Carcea and Caraballo, {Naomi L{\'o}pez} and Marlin, {Bianca J.} and Rumi Ooyama and Riceberg, {Justin S.} and {Mendoza Navarro}, {Joyce M.} and Maya Opendak and Diaz, {Veronica E.} and Luisa Schuster and {Alvarado Torres}, {Maria I.} and Harper Lethin and Daniel Ramos and Jessica Minder and Mendoza, {Sebastian L.} and Bair-Marshall, {Chloe J.} and Samadjopoulos, {Grace H.} and Shizu Hidema and Annegret Falkner and Dayu Lin and Adam Mar and Wadghiri, {Youssef Z.} and Katsuhiko Nishimori and Takefumi Kikusui and Kazutaka Mogi and Sullivan, {Regina M.} and Froemke, {Robert C.}",

note = "Publisher Copyright: {\textcopyright} 2021, The Author(s).",

year = "2021",

month = aug,

day = "26",

doi = "10.1038/s41586-021-03814-7",

language = "English",

volume = "596",

pages = "553--557",

journal = "Nature",

issn = "0028-0836",

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number = "7873",

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Carcea, I, Caraballo, NL, Marlin, BJ, Ooyama, R, Riceberg, JS, Mendoza Navarro, JM, Opendak, M, Diaz, VE, Schuster, L, Alvarado Torres, MI, Lethin, H, Ramos, D, Minder, J, Mendoza, SL, Bair-Marshall, CJ, Samadjopoulos, GH, Hidema, S, Falkner, A, Lin, D, Mar, A, Wadghiri, YZ, Nishimori, K, Kikusui, T, Mogi, K, Sullivan, RM & Froemke, RC 2021, 'Oxytocin neurons enable social transmission of maternal behaviour', Nature, vol. 596, no. 7873, pp. 553-557. https://doi.org/10.1038/s41586-021-03814-7

TY - JOUR

T1 - Oxytocin neurons enable social transmission of maternal behaviour

AU - Carcea, Ioana

AU - Caraballo, Naomi López

AU - Marlin, Bianca J.

AU - Ooyama, Rumi

AU - Riceberg, Justin S.

AU - Mendoza Navarro, Joyce M.

AU - Opendak, Maya

AU - Diaz, Veronica E.

AU - Schuster, Luisa

AU - Alvarado Torres, Maria I.

AU - Lethin, Harper

AU - Ramos, Daniel

AU - Minder, Jessica

AU - Mendoza, Sebastian L.

AU - Bair-Marshall, Chloe J.

AU - Samadjopoulos, Grace H.

AU - Hidema, Shizu

AU - Falkner, Annegret

AU - Lin, Dayu

AU - Mar, Adam

AU - Wadghiri, Youssef Z.

AU - Nishimori, Katsuhiko

AU - Kikusui, Takefumi

AU - Mogi, Kazutaka

AU - Sullivan, Regina M.

AU - Froemke, Robert C.

PY - 2021/8/26

Y1 - 2021/8/26

N2 - 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.

AB - 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.

UR - http://www.scopus.com/inward/record.url?scp=85112330408&partnerID=8YFLogxK

U2 - 10.1038/s41586-021-03814-7

DO - 10.1038/s41586-021-03814-7

M3 - Article

C2 - 34381215

AN - SCOPUS:85112330408

SN - 0028-0836

VL - 596

SP - 553

EP - 557

JO - Nature

JF - Nature

IS - 7873

ER -

Oxytocin neurons enable social transmission of maternal behaviour

Abstract

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