Characterization of the Oxytocin System Regulating Affiliative Behavior in Female Prairie Voles

• Type of Material: Article
• Authors: Heather E. Ross, Emory University; Charlene D. Cole, Emory University; Yoland Smith, Emory University; Inga D. Neumann, University of Regensburg, Germany; Rainer Landgraf, Max Planck Institute of Psychiatry, Germany; Anne Z. Murphy, Georgia State University; Larry J. Young, Emory University
• Language: English
• Date: 2009-09-15
• Publisher: Elsevier: 12 months
• Publication Version: Author Accepted Manuscript (After Peer Review)
• Copyright Statement: © 2009 IBRO. Published by Elsevier Ltd. All rights reserved.
• License: Creative Commons Attribution-NonCommerical-NoDerivs 3.0 Unported
• Final Published Version (URL): http://dx.crossref.org/10.1016%2Fj.neuroscience.2009.05.055
• Title of Journal or Parent Work: Neuroscience
• ISSN: 0306-4522
• Volume: 162
• Issue: 4
• Start Page: 892
• End Page: 903
• Grant/Funding Information: This study was supported by NIH grants MH064692 to LJY, RR00165 to Yerkes National Primates Research Center, NSF STC IBN-9876754 and a collaborative DAAD / NSF grant (IDN, LJY).
• Keywords: supraoptic nucleus; neurohypophysial peptides; paraventricular nucleus; alloparental behavior; pair bonding; nucleus accumbens
• Research Categories: Biology, Neuroscience

Abstract

Oxytocin regulates partner preference formation and alloparental behavior in the socially monogamous prairie vole (Microtus ochrogaster) by activating oxytocin receptors in the nucleus accumbens of females. Mating facilitates partner preference formation, and oxytocin-immunoreactive fibers in the nucleus accumbens have been described in prairie voles. However, there has been no direct evidence of oxytocin release in the nucleus accumbens during sociosexual interactions, and the origin of the oxytocin fibers is unknown. Here we show for the first time that extracellular concentrations of oxytocin are increased in the nucleus accumbens of female prairie vole during unrestricted interactions with a male. We further show that the distribution of oxytocin-immunoreactive fibers in the nucleus accumbens is conserved in prairie voles, mice and rats, despite remarkable species differences in oxytocin receptor binding in the region. Using a combination of site-specific and peripheral infusions of the retrograde tracer, Fluorogold, we demonstrate that the nucleus accumbens oxytocin-immunoreactive fibers likely originate from paraventricular and supraoptic hypothalamic neurons. This distribution of retrogradely labeled neurons is consistent with the hypothesis that striatal oxytocin fibers arise from collaterals of magnocellular neurons of the neurohypophysial system. If correct, this may serve to coordinate peripheral and central release of oxytocin with appropriate behavioral responses associated with reproduction, including pair bonding after mating, and maternal responsiveness following parturition and during lactation.