Characterization of the oxytocin system regulating affiliative behavior in female prairie voles

doi:10.1016/j.neuroscience.2009.05.055

Neuroscience

Volume 162, Issue 4, 15 September 2009, Pages 892-903

https://doi.org/10.1016/j.neuroscience.2009.05.055 Get rights and content

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 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.

Section snippets

Animals

Prairie and meadow voles were housed in same-sex groups with two to three voles/cage from the time of weaning at 21–23 days of age. Housing consisted of a ventilated 36×18×19 cm Plexiglas cage filled with Bed-o-cobbs Laboratory Animal Bedding (Bed-o-cobbs, Maumee, OH, USA) under a 14:10-h light/dark cycle at 22 °C with access to food (rabbit LabDiet, Richmond, IN, USA) and water ad libitum. The prairie voles were obtained from our laboratory breeding colony that originally derived from

OT release during sociosexual interactions

In vivo microdialysis was performed in female prairie voles at baseline, during a restricted exposure when the male was confined to a wire cage, and during free exposure when mating could occur. OT concentrations in the dialysates were below the level of detectability in the majority of samples. Therefore, samples were categorized as being detectable (>0.05 pg/25 μl sample) or non-detectable (<0.05 pg/25 μl sample) and analyzed using the non-parametric Fisher's exact test. None of the animals

Discussion

OT modulates a wide range of social behaviors, including maternal nurturing and bonding, sexual behavior, and social attachment. In humans, intranasal OT enhances interpersonal trust, eye gaze, recognition of familiar faces, and the ability to infer the emotions of others (Kosfeld et al 2005, Domes et al 2007, Guastella et al 2008, Savaskan et al 2008). Yet remarkably little is known about the origins of neurons that modulate these behaviors. In prairie voles, pharmacological and genetic

Acknowledgments

The authors want to thank Hemu Nair for his assistance in statistical analysis, Tig Rainnie for his gift of antibody and technical assistance, and Lorra Mathews for her excellent job managing our vole colony. Thanks are also due to Jean-Francois Pare and Susan Jenkins for their help with the electron microscopy immunocytochemistry procedures and data collection presented in this manuscript. This study was supported by NIH grants MH064692 to L.J.Y., RR00165 to Yerkes National Primates Research

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Behavioural NeuroscienceResearch PaperCharacterization of the oxytocin system regulating affiliative behavior in female prairie voles

Abstract

Section snippets

Animals

OT release during sociosexual interactions

Discussion

Acknowledgments

Brain Res

Biol Psychiatry

Biol Psychiatry

Brain Res Bull

Brain Res

J Neurosci Methods

Brain Res Bull

Front Neuroendocrinol

Neuroscience

Neuroscience

Horm Behav

Neurosci Lett

Trends Neurosci

Neuroscience

Neuroscience

Neuroscience

Psychoneuroendocrinology

Horm Behav

Uber die neurosekretorische Verknupfung von Hypothalamus und Neurohypophyse

Z Zellforsch Mikrosk Anat

Brain oxytocin correlates with maternal aggression: link to anxiety

J Neurosci

The patterns of afferent innervation of the core and shell in the “accumbens” part of the rat ventral striatum: immunohistochemical detection of retrogradely transported fluoro-gold

J Comp Neurol

Oxytocin: synthesis, secretion, and reproductive functions

Plasma oxytocin increases in the human sexual response

J Clin Endocrinol Metab

Physiological substrates of mammalian monogamy: the prairie vole model

Neurosci Biobehav Rev

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

Behav Neurosci

Oxytocin, vasopressin, and the neurogenetics of sociality

Science

Behavioural Neuroscience
Research Paper
Characterization of the oxytocin system regulating affiliative behavior in female prairie voles