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      Estrogen Receptor-α in the Bed Nucleus of the Stria Terminalis Regulates Social Affiliation in Male Prairie Voles ( Microtus ochrogaster)

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          Abstract

          Estrogen receptor alpha (ERα) typically masculinizes male behavior, while low levels of ERα in the medial amygdala (MeA) and the bed nucleus of the stria terminalis (BST) are associated with high levels of male prosocial behavior. In the males of the highly social prairie vole ( Microtus ochrogaster), increasing ERα in the MeA inhibited the expression of spontaneous alloparental behavior and produced a preference for novel females. To test for the effects of increased ERα in the BST, a viral vector was used to enhance ERα expression in the BST of adult male prairie voles. Following treatment, adult males were tested for alloparental behavior with 1–3-day-old pups, and for heterosexual social preference and affiliation. Treatment did not affect alloparental behavior as 73% of ERα-BST males and 62.5% of control males were alloparental. Increasing ERα in the BST affected heterosexual affiliation, with ERα-BST males spending significantly less total time in side-by-side contact with females relative to time spent with control males. ERα-BST males did not show a preference for either the familiar or novel female. These findings differed significantly from those reported in ERα-MeA enhanced males, where ERα inhibited alloparental behavior and produced a preference for a novel female. The findings from this study suggest two things: first, that increased ERα in the BST decreases social affiliation and second, that altering ERα in different regions of the social neural circuit differentially impacts the expression of social behavior.

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          Most cited references30

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

          Oxytocin (OT) knock-out mice fail to recognize familiar conspecifics after repeated social exposures, despite normal olfactory and spatial learning abilities. OT treatment fully restores social recognition. Here we demonstrate that OT acts in the medial amygdala during the initial exposure to facilitate social recognition. OT given before, but not after, the initial encounter restores social recognition in OT knock-out mice. Using c-Fos immunoreactivity (Fos-IR) as a marker of neuronal activation in this initial encounter, we found similar neuronal activation in the wild-type (WT) and OT knock-out mouse in olfactory bulbs, piriform cortex, cortical amygdala, and the lateral septum. Wild-type, but not OT knock-out mice exhibited an induction of Fos-IR in the medial amygdala. Projections sites of the medial amygdala also failed to show a Fos-IR induction in the OT knock-out mice. OT knock-out, but not WT, mice showed dramatic increases in Fos-IR in the somatosensory cortex and the hippocampus, suggesting alternative processing of social cues in these animals. With site-specific injections of OT and an OT antagonist, we demonstrate that OT receptor activation in the medial amygdala is both necessary and sufficient for social recognition in the mouse.
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            The effects of oxytocin and vasopressin on partner preferences in male and female prairie voles (Microtus ochrogaster).

            This study compared the effects of centrally administered oxytocin (OT) and arginine vasopressin (AVP) on partner preference formation and social contact in male and female prairie voles (Microtus ochrogaster). After 1 hr of cohabitation and pretreatment with either AVP or OT, both males and females exhibited increased social contact and significant preference for the familiar partner. After pretreatment with either an OT receptor antagonist (OTA) or an AVP (V1a) receptor antagonist (AVPA), neither OT nor AVP induced a partner preference. In addition, treatment with OT+OTA or AVP+AVPA was associated with low levels of social contact in both sexes. Either AVP or OT is sufficient to facilitate social contact if either the OT or AVP receptor is available. However, the formation of partner preferences may require access to both AVP and OT receptors.
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              Species differences in paternal behavior and aggression in peromyscus and their associations with vasopressin immunoreactivity and receptors.

              Previous comparative studies have suggested that the distribution of arginine vasopressin (AVP) pathways within the brain is associated with species-typical patterns of social behavior. In the current study, male parental behavior and aggression were compared in two species of Peromyscus. As predicted based on other studies, male mice from a monogamous species, the California mouse Peromyscus californicus, spent more time providing parental care to offspring than males from a polygamous species, the white-footed mouse Peromyscus leucopus. Sexually naive male California mice also attacked opponents more rapidly than white-footed mice during resident-intruder and neutral aggression tests. Since AVP has been shown to modulate these behaviors, we compared the distribution of vasopressinergic neurons and receptors. We predicted that greater AVP-immunoreactive (AVP-ir) staining in the bed nucleus of the stria terminalis and AVP receptor density in the lateral septum would occur in the species with low levels of paternal care because this pattern was found in similar comparisons with sexually naive monogamous and polygamous voles. In contrast, in our study, monogamous male mice showed more AVP-ir staining in the bed nucleus of the stria terminalis than the polygamous species, as well as more AVP receptors in the lateral septum. Parental behavior therefore does not appear to predict differences in patterns of AVP-ir staining and receptor distribution across species or vice versa. We propose the hypothesis that aggression may be better correlated with species patterns of AVP-ir staining density and receptor distribution. Copyright 1999 Academic Press.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2010
                27 January 2010
                : 5
                : 1
                : e8931
                Affiliations
                [1 ]Department of Biology, University of Memphis, Memphis, Tennessee, United States of America
                [2 ]Department of Biology and Integrated Bioscience Program, The University of Akron, Akron, Ohio, United States of America
                [3 ]Neurologix Inc, Laboratory of Neurobiology and Behavior, The Rockefeller University, New York, New York, United States of America
                [4 ]Kansei, Behavioral and Brain Sciences Graduate School of Comprehensive Human Sciences, University of Tsukuba, Tsukuba, Ibaraki, Japan
                Centre National de la Recherche Scientifique, France
                Author notes

                Conceived and designed the experiments: BC. Performed the experiments: KL. Analyzed the data: KL KK. Contributed reagents/materials/analysis tools: SM SO. Wrote the paper: KL BC KK.

                [¤]

                Current address: Department of Psychology, Program in Neuroscience, Florida State University, Tallahassee, Florida, United States of America

                Article
                09-PONE-RA-14329R1
                10.1371/journal.pone.0008931
                2811737
                20111713
                9b34d39d-59bd-4674-b826-e64d549a50b5
                Lei et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                : 18 November 2009
                : 23 December 2009
                Page count
                Pages: 5
                Categories
                Research Article
                Neuroscience
                Neuroscience/Behavioral Neuroscience
                Physiology/Endocrinology

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                Uncategorized

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