Paraventricular Nucleus Oxytocin Subsystems Promote Active Paternal Behaviors in Mandarin Voles

• Type of Material: Article
• Authors: Zhixiong He, Shaanxi Normal University; Lizi Zhang, Shaanxi Normal University; Wenjuan Hou, Shaanxi Normal University; Xin Zhang, Shaanxi Normal University; Larry Young, Emory University; Laifu Li, Shaanxi Normal University; Limin Liu, Shaanxi Normal University; Huan Ma, Shaanxi Normal University; Yufeng Xun, Shaanxi Normal University; Zijian Lv, Shaanxi Normal University; Yitong Li, Shaanxi Normal University; Rui Jia, Shaanxi Normal University; Jingang Li, Shaanxi Normal University; Fadao Tai, Shaanxi Normal University
• Language: English
• Date: 2021-08-04
• Publisher: The Society for Neuroscience
• Publication Version: Final Published Version
• Copyright Statement: © 2021 the authors.
• License: Creative Commons Attribution 4.0 International
• Final Published Version (URL): http://dx.doi.org/10.1523/JNEUROSCI.2864-20.2021
• Title of Journal or Parent Work: Journal of neuroscience
• Volume: 41
• Issue: 31
• Start Page: 6699
• End Page: 6713
• Grant/Funding Information: China Postdoctoral Science Foundation Grant 2019M653534;; L.J.Y. was also supported by National Institutes of Health Grants P50MH100023 and R01MH112788.; Natural Science Foundation of Shaanxi Province, China, Grant 2020JQ-412;; Fundamental Research Funds for Central University Grants GK201903065, GK202007008, and GK202103066.; This work was supported by National Natural Science Foundation of China Grants 31670421, 31970424, and 31901082
• Keywords: Neurosciences & Neurology; nucleus accumbens; Social reward; Accumbent oxytocin; Infant; dopamine; Life Sciences & Biomedicine; Maternal behavior; paternal behavior; Individual differences; Science & Technology; Sexual stimuli; oxytocin; Medial preoptic area; Neural responses; Receptor; Neurosciences; Neurons; ventral tegmental area; paraventricular nucleus of the hypothalamus
• Research Categories: Psychology, Behavioral; Health Sciences, Medicine and Surgery; Biology, Neuroscience

Abstract

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.