Literature DB >> 26643557

Central oxytocin receptors mediate mating-induced partner preferences and enhance correlated activation across forebrain nuclei in male prairie voles.

Zachary V Johnson1, Hasse Walum2, Yaseen A Jamal3, Yao Xiao4, Alaine C Keebaugh5, Kiyoshi Inoue6, Larry J Young7.   

Abstract

Oxytocin (OT) is a deeply conserved nonapeptide that acts both peripherally and centrally to modulate reproductive physiology and sociosexual behavior across divergent taxa, including humans. In vertebrates, the distribution of the oxytocin receptor (OTR) in the brain is variable within and across species, and OTR signaling is critical for a variety of species-typical social and reproductive behaviors, including affiliative and pair bonding behaviors in multiple socially monogamous lineages of fishes, birds, and mammals. Early work in prairie voles suggested that the endogenous OT system modulates mating-induced partner preference formation in females but not males; however, there is significant evidence that central OTRs may modulate pair bonding behavior in both sexes. In addition, it remains unclear how transient windows of central OTR signaling during sociosexual interaction modulate neural activity to produce enduring shifts in sociobehavioral phenotypes, including the formation of selective social bonds. Here we re-examine the role of the central OT system in partner preference formation in male prairie voles using a selective OTR antagonist delivered intracranially. We then use the same antagonist to examine how central OTRs modulate behavior and immediate early gene (Fos) expression, a metric of neuronal activation, in males during brief sociosexual interaction with a female. Our results suggest that, as in females, OTR signaling is critical for partner preference formation in males and enhances correlated activation across sensory and reward processing brain areas during sociosexual interaction. These results are consistent with the hypothesis that central OTR signaling facilitates social bond formation by coordinating activity across a pair bonding neural network.
Copyright © 2015 Elsevier Inc. All rights reserved.

Entities:  

Keywords:  Functional connectivity; Immediate-early gene; Monogamy; Pair bonding; Social attachment; Social decision-making network

Mesh:

Substances:

Year:  2015        PMID: 26643557      PMCID: PMC4768463          DOI: 10.1016/j.yhbeh.2015.11.011

Source DB:  PubMed          Journal:  Horm Behav        ISSN: 0018-506X            Impact factor:   3.587


  73 in total

Review 1.  Frank A. Beach Award. Oxytocin and vasopressin receptors and species-typical social behaviors.

Authors:  L J Young
Journal:  Horm Behav       Date:  1999-12       Impact factor: 3.587

2.  The effects of oxytocin and vasopressin on partner preferences in male and female prairie voles (Microtus ochrogaster).

Authors:  M M Cho; A C DeVries; J R Williams; C S Carter
Journal:  Behav Neurosci       Date:  1999-10       Impact factor: 1.912

Review 3.  Cellular mechanisms of social attachment.

Authors:  L J Young; M M Lim; B Gingrich; T R Insel
Journal:  Horm Behav       Date:  2001-09       Impact factor: 3.587

4.  Oxytocin in the medial amygdala is essential for social recognition in the mouse.

Authors:  J N Ferguson; J M Aldag; T R Insel; L J Young
Journal:  J Neurosci       Date:  2001-10-15       Impact factor: 6.167

5.  Extraordinary diversity in vasopressin (V1a) receptor distributions among wild prairie voles (Microtus ochrogaster): patterns of variation and covariation.

Authors:  Steven M Phelps; Larry J Young
Journal:  J Comp Neurol       Date:  2003-11-24       Impact factor: 3.215

6.  Nucleus accumbens oxytocin and dopamine interact to regulate pair bond formation in female prairie voles.

Authors:  Y Liu; Z X Wang
Journal:  Neuroscience       Date:  2003       Impact factor: 3.590

7.  Vasopressin-dependent neural circuits underlying pair bond formation in the monogamous prairie vole.

Authors:  M M Lim; L J Young
Journal:  Neuroscience       Date:  2004       Impact factor: 3.590

8.  Enhanced partner preference in a promiscuous species by manipulating the expression of a single gene.

Authors:  Miranda M Lim; Zuoxin Wang; Daniel E Olazábal; Xianghui Ren; Ernest F Terwilliger; Larry J Young
Journal:  Nature       Date:  2004-06-17       Impact factor: 49.962

9.  Oxytocin receptor distribution reflects social organization in monogamous and polygamous voles.

Authors:  T R Insel; L E Shapiro
Journal:  Proc Natl Acad Sci U S A       Date:  1992-07-01       Impact factor: 11.205

10.  Development of partner preferences in female prairie voles (Microtus ochrogaster): the role of social and sexual experience.

Authors:  J R Williams; K C Catania; C S Carter
Journal:  Horm Behav       Date:  1992-09       Impact factor: 3.587

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  54 in total

Review 1.  Evolutionary diversity as a catalyst for biological discovery.

Authors:  Zachary V Johnson; Larry J Young
Journal:  Integr Zool       Date:  2018-11       Impact factor: 2.654

2.  Sexually dimorphic role of oxytocin in medaka mate choice.

Authors:  Saori Yokoi; Kiyoshi Naruse; Yasuhiro Kamei; Satoshi Ansai; Masato Kinoshita; Mari Mito; Shintaro Iwasaki; Shuntaro Inoue; Teruhiro Okuyama; Shinichi Nakagawa; Larry J Young; Hideaki Takeuchi
Journal:  Proc Natl Acad Sci U S A       Date:  2020-02-18       Impact factor: 11.205

3.  Pair bond formation leads to a sustained increase in global cerebral glucose metabolism in monogamous male titi monkeys (Callicebus cupreus).

Authors:  Nicole Maninger; Katie Hinde; Sally P Mendoza; William A Mason; Rebecca H Larke; Benjamin J Ragen; Michael R Jarcho; Simon R Cherry; Douglas J Rowland; Emilio Ferrer; Karen L Bales
Journal:  Neuroscience       Date:  2017-02-24       Impact factor: 3.590

4.  Oxytocin receptor knockout prairie voles generated by CRISPR/Cas9 editing show reduced preference for social novelty and exaggerated repetitive behaviors.

Authors:  Kengo Horie; Kiyoshi Inoue; Shingo Suzuki; Saki Adachi; Saori Yada; Takashi Hirayama; Shizu Hidema; Larry J Young; Katsuhiko Nishimori
Journal:  Horm Behav       Date:  2018-11-08       Impact factor: 3.587

Review 5.  Circuits for social learning: A unified model and application to Autism Spectrum Disorder.

Authors:  Marilena M DeMayo; Larry J Young; Ian B Hickie; Yun Ju C Song; Adam J Guastella
Journal:  Neurosci Biobehav Rev       Date:  2019-09-24       Impact factor: 8.989

6.  Intranasal oxytocin modulates neural functional connectivity during human social interaction.

Authors:  James K Rilling; Xiangchuan Chen; Xu Chen; Ebrahim Haroon
Journal:  Am J Primatol       Date:  2018-02-10       Impact factor: 2.371

Review 7.  Oxytocin and vasopressin neural networks: Implications for social behavioral diversity and translational neuroscience.

Authors:  Zachary V Johnson; Larry J Young
Journal:  Neurosci Biobehav Rev       Date:  2017-05       Impact factor: 8.989

8.  A single prolonged stress paradigm produces enduring impairments in social bonding in monogamous prairie voles.

Authors:  Aki Arai; Yu Hirota; Naoki Miyase; Shiori Miyata; Larry J Young; Yoji Osako; Kazunari Yuri; Shinichi Mitsui
Journal:  Behav Brain Res       Date:  2016-08-10       Impact factor: 3.332

9.  A unified circuit for social behavior.

Authors:  Meera E Modi; Mustafa Sahin
Journal:  Neurobiol Learn Mem       Date:  2018-08-24       Impact factor: 2.877

10.  Mating and social exposure induces an opioid-dependent conditioned place preference in male but not in female prairie voles (Microtus ochrogaster).

Authors:  M Ulloa; W Portillo; N F Díaz; L J Young; F J Camacho; V M Rodríguez; R G Paredes
Journal:  Horm Behav       Date:  2017-11-08       Impact factor: 3.587

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