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      Neuroanatomical Projections of the Species-Specific Tyrosine Hydroxylase-Immunoreactive Cells of the Male Prairie Vole Bed Nucleus of the Stria Terminalis and Medial Amygdala

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          Abstract

          The principal nucleus of the bed nucleus of the stria terminalis (BSTpr) and posterodorsal part of the medial amygdalar nucleus (MEApd) are densely interconnected sites transmitting olfactory information to brain areas mediating sociosexual behaviors. In male prairie voles (Microtus ochrogaster), the BSTpr and MEApd contain hundreds of cells densely immunoreactive for tyrosine hydroxylase (TH). Such tremendous numbers of TH-immunoreactive (TH-ir) cells do not exist in other rodents examined, and studies from our laboratory suggest these cells may be part of a unique chemical network necessary for monogamous behaviors in prairie voles. To obtain information about how these TH-ir cells communicate with other sites involved in social behaviors, we first used biotinylated dextran amine (BDA) to determine sites that receive BSTpr efferents and also contain TH-ir fibers. Only in the medial preoptic area (MPO) and MEApd did we find considerable comingling of BDA-containing and TH-ir fibers. To examine if these sites receive input specifically from BSTpr TH-ir cells, the retrograde tracer Fluorogold was infused into the MPO or MEApd. Almost 80% of TH-ir projections to the MPO originated from the BSTpr or MEApd, involving about 40% of all TH-ir cells in these sites. In contrast, the MEApd received almost no input from TH-ir cells in the BSTpr, and received it primarily from the ventral tegmental area. Retrograde tracing from the BSTpr itself revealed substantial input from MEApd TH-ir cells. Thus, the male prairie vole brain contains a species-specific TH-ir network involving the BSTpr, MEApd, and MPO. By connecting brain sites involved in olfaction, sociality and motivation, this network may be essential for monogamous behaviors in this species.

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          Most cited references77

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          Nucleus accumbens dopamine differentially mediates the formation and maintenance of monogamous pair bonds.

          The involvement of dopamine within the nucleus accumbens in the formation and maintenance of pair bonds was assessed in a series of experiments using the monogamous prairie vole. We show that dopamine transmission that promotes pair bond formation occurs within the rostral shell of the nucleus accumbens, but not in its core or caudal shell. Within this specific brain region, D1- and D2-like receptor activation produced opposite effects: D1-like activation prevented pair bond formation, whereas D2-like activation facilitated it. After extended cohabitation with a female, male voles showed behavior indicative of pair bond maintenance-namely, selective aggression towards unfamiliar females. These voles also showed a significant upregulation in nucleus accumbens D1-like receptors, and blockade of these receptors abolished selective aggression. Thus, neuroplastic reorganization of the nucleus accumbens dopamine system is responsible for the enduring nature of monogamous pair bonding. Finally, we show that this system may also contribute to species-specific social organization.
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            Oxytocin, vasopressin, and social recognition in mammals.

            While pheromones may act as social memory signals, oxytocin and vasopressin acting in the brain appear to be critical for the neural processing of olfactory signatures used for social discrimination. Evidence from a variety of laboratories using a range of animal models, as well as an array of molecular and pharmacological techniques, have helped to determine the neuroanatomical and functional roles oxytocin and vasopressin play in social cognition. In this review we discuss the considerable evidence for the roles of oxytocin and vasopressin in social recognition in rats and mice, as well as in offspring recognition in sheep and mate preference in monogamous voles.
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              Sexual behavior in male rodents.

              The hormonal factors and neural circuitry that control copulation are similar across rodent species, although there are differences in specific behavior patterns. Both estradiol (E) and dihydrotestosterone (DHT) contribute to the activation of mating, although E is more important for copulation and DHT for genital reflexes. Hormonal activation of the medial preoptic area (MPOA) is most effective, although implants in the medial amygdala (MeA) can also stimulate mounting in castrates. Chemosensory inputs from the main and accessory olfactory systems are the most important stimuli for mating in rodents, especially in hamsters, although genitosensory input also contributes. Dopamine agonists facilitate sexual behavior, and serotonin (5-HT) is generally inhibitory, though certain 5-HT receptor subtypes facilitate erection or ejaculation. Norepinephrine agonists and opiates have dose-dependent effects, with low doses facilitating and high doses inhibiting behavior.
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                Author and article information

                Journal
                BBE
                Brain Behav Evol
                10.1159/issn.0006-8977
                Brain, Behavior and Evolution
                S. Karger AG
                0006-8977
                1421-9743
                2011
                June 2011
                06 May 2011
                : 77
                : 3
                : 176-192
                Affiliations
                Neuroscience Program, Michigan State University, East Lansing, Mich., USA
                Author notes
                *Joseph S. Lonstein, 108 Giltner Hall, Michigan State University, East Lansing, MI 48824 (USA), Tel. +1 517 353 8675, E-Mail lonstein@msu.edu
                Article
                326618 Brain Behav Evol 2011;77:176–192
                10.1159/000326618
                21546771
                8c6cd602-0db2-4ab3-9d9d-bd09437ab458
                © 2011 S. Karger AG, Basel

                Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher. Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug. Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.

                History
                : 19 November 2010
                : 21 February 2011
                Page count
                Figures: 10, Tables: 1, Pages: 17
                Categories
                Original Paper

                Geriatric medicine,Neurology,Cardiovascular Medicine,Neurosciences,Clinical Psychology & Psychiatry,Public health
                Medial preoptic area,Bed nucleus of the stria terminalis,Anatomical tracing,Ventral tegmental area,Monogamy,Prairie vole,Dopamine,Social behavior,Amygdala

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