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      Sexual Behavior Increases Cell Proliferation in the Rostral Migratory Stream and Promotes the Differentiation of the New Cells into Neurons in the Accessory Olfactory Bulb of Female Rats

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          Abstract

          We have previously demonstrated, that 15 days after female rats pace the sexual interaction, there is an increase in the number of new cells that reach the granular cell layer (GrL) of the accessory olfactory bulb (AOB). The aim of the present study was to evaluate, if the first sexual experience in the female rat increases cell proliferation in the subventricular zone (SVZ) and the rostral migratory stream (RMS). We also tested if this behavior promotes the survival of the new cells that integrate into the main olfactory bulb (MOB) and AOB 45 days after the behavioral test. Sexually, naive female rats were injected with the DNA synthesis marker 5′-bromo-2′-deoxyuridine (BrdU) on the day of the behavioral test. They were randomly divided into the following groups: Female rats placed alone in the mating cage (1); Females exposed to amyl acetate odor [banana scent, (2)]; Females that could see, hear, and smell the male but physical contact was not possible [exposed to male, (3)]; Female rats that could pace the sexual interaction (4); and females that mated without the possibility of pacing the sexual interaction (5). Animals were sacrificed 2 days after the behavioral test (proliferation) or 45 days later (survival). Our results show that 2 days after females were exposed to banana scent or to the male, they had a higher number of cells in the SVZ. Females, that mated in pace and no-paced conditions had more new cells in the RMS. At 45 days, no significant differences were found in the number of new cells that survived in the MOB or in the AOB. However, mating increased the percentage of new cells, that differentiated into neurons in the GrL of the AOB. These new cells expressed c-Fos after a second sexual encounter just before the females were sacrificed. No significant differences in plasma levels of estradiol and progesterone were observed between groups. Our results indicate that the first sexual experience increases cell proliferation in the RMS and mating 45 days later enhances the number of new cells that differentiate into neurons in the AOB. These new neurons are activated by sexual stimulation.

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          Most cited references57

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          Long-distance neuronal migration in the adult mammalian brain.

          During the development of the mammalian brain, neuronal precursors migrate to their final destination from their site of birth in the ventricular and subventricular zones (VZ and SVZ, respectively). SVZ cells in the walls of the lateral ventricle continue to proliferate in the brain of adult mice and can generate neurons in vitro, but their fate in vivo is unknown. Here SVZ cells from adult mice that carry a neuronal-specific transgene were grafted into the brain of adult recipients. In addition, the fate of endogenous SVZ cells was examined by microinjection of tritiated thymidine or a vital dye that labeled a discrete population of SVZ cells. Grafted and endogenous SVZ cells in the lateral ventricle of adult mice migrate long distances and differentiate into neurons in the olfactory bulb.
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            Pregnancy-stimulated neurogenesis in the adult female forebrain mediated by prolactin.

            Neurogenesis occurs in the olfactory system of the adult brain throughout life, in both invertebrates and vertebrates, but its physiological regulation is not understood. We show that the production of neuronal progenitors is stimulated in the forebrain subventricular zone of female mice during pregnancy and that this effect is mediated by the hormone prolactin. The progenitors then migrate to produce new olfactory interneurons, a process likely to be important for maternal behavior, because olfactory discrimination is critical for recognition and rearing of offspring. Neurogenesis occurs even in females that mate with sterile males. These findings imply that forebrain olfactory neurogenesis may contribute to adaptive behaviors in mating and pregnancy.
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              An exteroceptive block to pregnancy in the mouse.

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                Author and article information

                Contributors
                Journal
                Front Neurosci
                Front Neurosci
                Front. Neurosci.
                Frontiers in Neuroscience
                Frontiers Media S.A.
                1662-4548
                1662-453X
                26 February 2016
                2016
                : 10
                : 48
                Affiliations
                [1] 1Instituto de Neurobiología, Universidad Nacional Autónoma de México Mexico, Mexico
                [2] 2Departamento de Biología de la Reproducción, Universidad Autónoma Metropolitana-Iztapalapa Mexico, Mexico
                Author notes

                Edited by: Laura López-Mascaraque, Instituto Cajal-Consejo Superior de Investigaciones Científicas, Spain

                Reviewed by: Luis Miguel Garcia-Segura, Consejo Superior de Investigaciones Científicas, Spain; Carmen Agustín-Pavón, Universitat Jaume I, Spain

                *Correspondence: Raúl G. Paredes rparedes@ 123456unam.mx

                This article was submitted to Neurogenesis, a section of the journal Frontiers in Neuroscience

                Article
                10.3389/fnins.2016.00048
                4767934
                26955325
                5d3654cf-d371-461a-9a0a-b427197c413c
                Copyright © 2016 Corona, Retana-Márquez, Portillo and Paredes.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 15 December 2015
                : 03 February 2016
                Page count
                Figures: 6, Tables: 5, Equations: 0, References: 67, Pages: 15, Words: 10863
                Funding
                Funded by: Consejo Nacional de Ciencia y Tecnología 10.13039/501100007350
                Award ID: 167101
                Award ID: 252756 y Fronteras 374
                Funded by: Dirección General Asuntos del Personal Académico, Universidad Nacional Autónoma de México 10.13039/501100006087
                Award ID: IN210215
                Award ID: IN203615
                Categories
                Neuroscience
                Original Research

                Neurosciences
                neurogenesis and sexual behavior,cell proliferation,cell survival,paced mating,olfactory bulbs

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