Increased anxiety and decreased sociability induced by paternal deprivation involve the PVN-PrL OTergic pathway

Author:

He Zhixiong1,Young Larry23,Ma Xin-Ming14,Guo Qianqian1,Wang Limin1,Yang Yang1,Luo Luo1,Yuan Wei1,Li Laifu1,Zhang Jing1,Hou Wenjuan1,Qiao Hui1ORCID,Jia Rui1,Tai Fadao1ORCID

Affiliation:

1. Institute of Brain and Behavioral Sciences, College of Life Sciences, Shaanxi Normal University, Xi’an, China

2. Department of Psychiatry and Behavioral Sciences, Silvio O. Conte Center for Oxytocin and Social Cognition, Center for Translational Social Neuroscience, Yerkes National Primate Research Center, Emory University, Atlanta, United States

3. Center for Social Neural Networks, University of Tsukuba, Tsukuba, Japan

4. Department of Neuroscience, University of Connecticut Health Center, Farmington, United States

Abstract

Early adverse experiences often have devastating consequences. However, whether preweaning paternal deprivation (PD) affects emotional and social behaviors and their underlying neural mechanisms remain unexplored. Using monogamous mandarin voles, we found that PD increased anxiety-like behavior and attenuated social preference in adulthood. PD also decreased the number of oxytocin (OT)-positive neurons projecting from the paraventricular nucleus (PVN) and reduced the levels of the medial prefrontal cortex OT receptor protein in females and of the OT receptor and V1a receptor proteins in males. Intra-prelimbic cortical OT injections reversed the PD-induced changes in anxiety-like behavior and social preferences. Optogenetic activation of the prelimbic cortex OT terminals from PVN OT neurons reversed the PD-induced changes in emotion and social preference behaviors, whereas optogenetic inhibition was anxiogenic and impaired social preference in naive voles. These findings demonstrate that PD increases anxiety-like behavior and attenuates social preferences through the involvement of PVN OT neuron projections to the prelimbic cortex.

Funder

Fundamental Research Funds for Central University of China

National Institutes of Health

Yerkes Regional Primate Research Center

National Natural Science Foundation of China

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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