PreprintCited by 8Neuroendocrine regulation and behaviorNeurogenesis and neuroplasticity mechanismsInfant Health and Development

Oxytocin Neurons Enable Social Transmission of Maternal Behavior

Carcea, Ioana, Caraballo, Naomi López, Marlin, Bianca J., Ooyama, Rumi, Riceberg, Justin S., Mendoza Navarro, Joyce M., Opendak, Maya, Diaz, Veronica E. +16 more·2019·bioRxiv (Cold Spring Harbor Laboratory)

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.

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  • Once plasticity has occurred, blocking cortical oxytocin receptors did not substantially affect pup retrieval abilities.

    “Once plasticity has occurred, blocking cortical oxytocin receptors did not substantially affect pup retrieval abilities”

    From Oxytocin, Neural Plasticity, and Social Behavior (2021) · cites this paper as Carcea et al. 2019

    In “Virgins observed mothers demonstrating maternal behavior” (page unavailable), suppressing hypothalamic oxytocin neurons after virgins began retrieving did not significantly affect retrieval. But the paper’s cortical oxytocin-receptor blockade was tested before observational learning, not after plasticity had occurred. It therefore does not establish the claimed result for cortical receptor blockade. (LLM, conf=0.86)

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  • PVN neurons did not fire substantially during spontaneous interactions with pups, and initially, virgin animals stayed away from the dam and the nest.

    “PVN neurons did not fire substantially during spontaneous interactions with pups, and initially, virgin animals stayed away from the dam and the nest.”

    From Oxytocin, Neural Plasticity, and Social Behavior (2021) · cites this paper as Carcea et al. 2019

    Fig. S5 (Anatomy; page unavailable) reports that virgin mice’s PVN neurons responded more robustly to short interactions with dams than with pups, supporting the comparison but not a categorical lack of substantial firing during pup interactions. The co-housing results report less time in the nest on day one than on later days, but do not establish that virgins initially stayed away from both the dam and the nest. (LLM, conf=0.82)

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  • Recordings in PVN taken simultaneously with fiber photometry in auditory cortex showed that bursts of activity in the hypothalamus produced bigger cortical responses, which increased just prior to individual virgins beginning to retrieve pups.

    “Recordings in PVN taken simultaneously with fiber photometry in auditory cortex showed that bursts of activity in the hypothalamus produced bigger cortical responses, which increased just prior to individual virgins beginning to retrieve pups.”

    From Oxytocin, Neural Plasticity, and Social Behavior (2021) · cites this paper as Carcea et al. 2019

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  • Inexperienced female mice can learn aspects of maternal behavior from interactions with and observations of experienced mothers, leading to cortical plasticity that builds on an intrinsic initial sensitivity to some pup call features.

    “Thus, inexperienced females can learn aspects of maternal behavior from interactions with and observations of experienced mothers, leading to cortical plasticity that builds on an intrinsic initial sensitivity to some pup call features (Carcea et al. 2019, Schiavo et al. 2020).”

    From Oxytocin, Neural Plasticity, and Social Behavior (2021) · cites this paper as Carcea et al. 2019

    The Discussion and ‘Social transmission of maternal behavior by observation’ sections report that virgin females learn pup retrieval through interactions with and observation of experienced mothers. The ‘PVN activity predicts single-trial modulation and plasticity of auditory cortex’ section reports increased cortical responses to pup calls, but says responses before co-housing were minimal; it does not establish an intrinsic initial sensitivity to particular call features. Page numbers are unavailable in our copy. (LLM, conf=0.84)

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  • Over hours, mother animals began shepherding virgins toward the nest, agonistically chasing them toward the pups, and this shepherding behavior and virgin nest entry activated a fraction of PVN and the identified oxytocin neurons.

    “Over hours, mother animals began shepherding virgins toward the nest, agonistically chasing them toward the pups, and this shepherding behavior and virgin nest entry activated a fraction of PVN and the identified oxytocin neurons (Figure 5b).”

    From Oxytocin, Neural Plasticity, and Social Behavior (2021) · cites this paper as Carcea et al. 2019

    “Mother mice shepherd virgins to the nest for co-caring” reports that mothers chased virgins back toward the nest and that shepherding emerged over hours to days. “Shepherding and nest entry activate virgin PVN oxytocin neurons” reports activation of subsets of virgin PVN and optically identified oxytocin neurons. The paper does not characterize the chasing as agonistic; it says shepherding seemed quite different from maternal aggression. (LLM, conf=0.88)

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Research works printed but not linked: 6

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Authors
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., Hidema, S., Falkner, A., Lin, D., Mar, A., Wadghiri, Y. Z., Nishimori, K., Kikusui, T., Mogi, K., Sullivan, R. M., & Froemke, R. C.
Affiliations
  • New York University (US)
  • Azabu University (JP)
  • Icahn School of Medicine at Mount Sinai (US)
  • Nathan Kline Institute for Psychiatric Research (US)
  • NYU Langone Health (US)
  • Tohoku University (JP)
  • Howard Hughes Medical Institute (US)
Corresponding author
Froemke, Robert C.
Venue
bioRxiv (Cold Spring Harbor Laboratory)
Publisher
openRxiv
Published
2019-11-17
OpenAlex
W2986243128
Cited by
8
References
9
Citations by year
2023: 1 · 2022: 2 · 2021: 5
Type
posted content
Language
en
Open access
closed
Locations
bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
Topics
  • Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
  • Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
  • Health Sciences › Health Professions › Pharmacy › Infant Health and Development
Keywords
oxytocin neurons, maternal behavior, paraventricular nucleus, hypothalamus, auditory cortex plasticity, infant vocalizations, pup retrieval, cohousing, nest guarding

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