Paraventricular nucleus oxytocin subsystems promote active paternal behaviors in mandarin voles
Open accessAbstract
Paternal care plays a critical role in the development of brain and behaviors in offspring in monogamous species. However, the neurobiological mechanisms, especially the neuronal circuity, underlying paternal care is largely unknown. Using socially monogamous male mandarin voles (Microtus mandarinus) with high levels of paternal care, we found that paraventricular nucleus of the hypothalamus (PVN) to ventral tegmental area (VTA) or nucleus accumbens (NAc) oxytocin (OT) neurons are activated during paternal care. Chemogenetic activation/inhibition of the PVN OT projection to VTA promoted/decreased paternal care, respectively. Chemogenetic inhibition of the PVN to VTA OT pathway reduced dopamine (DA) release in the NAc of male mandarin voles during licking and grooming of pups as revealed by in vivo fiber photometry. Optogenetic activation/inhibition of the VTA to NAc DA pathway possibly enhanced/suppressed paternal behaviors, respectively. Furthermore, chemogenetic activation/inhibition of PVN to NAc OT circuit enhanced/inhibited paternal care. This finding is a first step toward delineating the neuronal circuity underlying paternal care and may have implications for treating abnormalities in paternal care associated with paternal postpartum depression or paternal abuse. SIGNIFICANCE STATEMENT Paternal behavior is essential for offspring survival and development in some mammalian species. However, the circuit mechanisms underlying the paternal brain are poorly understood. We show that manipulation of paraventricular nucleus of the hypothalamus (PVN) to ventral tegmental area (VTA) oxytocin (OT) projections as well as VTA to nucleus accumbens (NAc) DA projections promote paternal behaviors. Inhibition the PVN to VTA OT pathway reduces DA release in the NAc during pup licking and grooming. PVN to NAc OT circuit is also essential for paternal behaviors. Our findings identify two new neural circuits that modulate paternal behaviors.
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The emergence of paternal behavior is driven in part by oxytocin activity in the mesolimbic dopamine system.
“The emergence of paternal behavior, similar to maternal behavior, is driven in part by OT activity in the mesolimbic DA system [36,37].”
From The Neurobiology of Love and Pair Bonding from Human and Animal Perspectives (2023) · cites this paper as [37]
The Abstract reports that manipulating oxytocin projections to the ventral tegmental area changed paternal care in male mandarin voles, and inhibiting those projections reduced dopamine release in the nucleus accumbens during pup care. The Paternal behavior test section shows that the study examined fathers caring for their own pups, not the emergence or onset of paternal behavior. The source therefore supports a role for this circuit in active paternal care, but not the claim about its emergence. (LLM, conf=0.86)
Experimental — accuracy not yet measuredIn mandarin voles, paternal behavior is facilitated by the activation of oxytocin projection neurons from the paraventricular nucleus of the hypothalamus to the ventral tegmental area and nucleus accumbens.
“In mandarin voles (Microtus mandarinus), paternal behavior is faciliated by the activation of OT projection neurons from the paraventricular nucleus of the hypothalamus (PVN) to the VTA and NAc [37].”
From The Neurobiology of Love and Pair Bonding from Human and Animal Perspectives (2023) · cites this paper as [37]
Paraventricular oxytocin projections to the ventral tegmental area and nucleus accumbens promote paternal behaviors in mandarin voles.
“Other loci of PVN OXT action include the VTA and NAcc as PVN OXT projections to these areas promote paternal behaviors in mandarin voles ( 126).”
From Oxytocin, Vasopressin, and Social Behavior: From Neural Circuits to Clinical Opportunities (2022) · cites this paper as [126]
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- Authors
- He, Z., Zhang, L., Hou, W., Zhang, X., Young, L. J., Li, L., Liu, L., Ma, H., Xun, Y., Lv, Z., Li, Y., Jia, R., Li, J., & Tai, F.
- Affiliations
- Shaanxi Normal University (CN)
- University of Tsukuba (JP)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2021-07-05
- Volume
- 41
- Issue
- 31
- Pages
- 6699-6713
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC8336703
- OpenAlex
- W3178714822
- Cited by
- 45
- References
- 63
- Citations by year
- 2026: 6 · 2025: 13 · 2024: 15 · 2023: 4 · 2022: 6 · 2021: 1
- FWCI
- 6.37
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Neuroscience (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Chinese Academy of Sciences
- Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences
- China Postdoctoral Science Foundation (2019M653534)
- Natural Science Foundation of Shaanxi Province (2020JQ, 2020JQ-412)
- National Institutes of Health
- Directorate for Biological Sciences
- National Institute of Mental Health (R01MH112788, P50MH100023)
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
- Keywords
- paternal care, oxytocin, paraventricular nucleus, ventral tegmental area, nucleus accumbens, dopamine release, chemogenetic manipulation, optogenetic manipulation, neural circuits, mandarin vole, paternal postpartum depression
- MeSH terms
- Animals, Behavior, Animal, Arvicolinae, Male, Neural Pathways, Oxytocin, Paraventricular Hypothalamic Nucleus, Paternal Behavior
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