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      Newborn Interneurons in the Accessory Olfactory Bulb Promote Mate Recognition in Female Mice

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          Abstract

          In the olfactory bulb of adult rodents, local interneurons are constantly replaced by immature precursors derived from the subventricular zone. Whether any olfactory sensory process specifically relies on this cell renewal remains largely unclear. By using the well known model of mating-induced imprinting to avoid pregnancy block, which requires accessory olfactory bulb (AOB) function, we demonstrate that this olfactory memory formation critically depends on the presence of newborn granule neurons in this brain region. We show that, in adult female mice, exposure to the male urine compounds involved in mate recognition increases the number of new granule cells surviving in the AOB. This process is modulated by male signals sensed through the vomeronasal organ and, in turn, changes the activity of the downstream amygdaloid and hypothalamic nuclei involved in the pregnancy block response. Chemical depletion of newly generated bulbar interneurons causes strong impairment in mate recognition, thus resulting in a high pregnancy failure rate to familiar mating male odors. Taken together, our results indicate that adult neurogenesis is essential for specific brain functions such as persistent odor learning and mate recognition.

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          Most cited references 63

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          Roles of continuous neurogenesis in the structural and functional integrity of the adult forebrain.

          Neurogenesis occurs continuously in the forebrain of adult mammals, but the functional importance of adult neurogenesis is still unclear. Here, using a genetic labeling method in adult mice, we found that continuous neurogenesis results in the replacement of the majority of granule neurons in the olfactory bulb and a substantial addition of granule neurons to the hippocampal dentate gyrus. Genetic ablation of newly formed neurons in adult mice led to a gradual decrease in the number of granule cells in the olfactory bulb, inhibition of increases in the granule cell number in the dentate gyrus and impairment of behaviors in contextual and spatial memory, which are known to depend on hippocampus. These results suggest that continuous neurogenesis is required for the maintenance and reorganization of the whole interneuron system in the olfactory bulb, the modulation and refinement of the existing neuronal circuits in the dentate gyrus and the normal behaviors involved in hippocampal-dependent memory.
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            Neurogenesis in adult subventricular zone.

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              Preferential incorporation of adult-generated granule cells into spatial memory networks in the dentate gyrus.

              Throughout adulthood, new neurons are continuously added to the dentate gyrus, a hippocampal subregion that is important in spatial learning. Whether these adult-generated granule cells become functionally integrated into memory networks is not known. We used immunohistochemical approaches to visualize the recruitment of new neurons into circuits supporting water maze memory in intact mice. We show that as new granule cells mature, they are increasingly likely to be incorporated into circuits supporting spatial memory. By the time the cells are 4 or more weeks of age, they are more likely than existing granule cells to be recruited into circuits supporting spatial memory. This preferential recruitment supports the idea that new neurons make a unique contribution to memory processing in the dentate gyrus.
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                Author and article information

                Journal
                Front Neurosci
                Front. Neurosci.
                Frontiers in Neuroscience
                Frontiers Research Foundation
                1662-4548
                1662-453X
                06 August 2011
                28 September 2011
                2011
                : 5
                Affiliations
                1simpleDepartment of Animal and Human Biology, University of Turin Turin, Italy
                2simpleDepartment of Molecular Embryology, Max Planck Institute of Immunobiology Freiburg, Germany
                3simpleDepartment of Physiology, University of Saarland School of Medicine Homburg, Germany
                4simpleScientific Institute Cavalieri-Ottolenghi (NICO) Torino, Italy
                Author notes

                Edited by: Angelique Bordey, Yale University School of Medicine, USA

                Reviewed by: Umberto Di Porzio, Genetics and Biophysics Adriano Buzzati Traverso, Italy; Armen Saghatelyan, Université Laval, Canada; Jean-Claude Platel, University Joseph Fourrier, France

                *Correspondence: Paolo Peretto, Scientific Institute Cavalieri-Ottolenghi (NICO), Regione Gonzole, 10, 10043 Orbassano, Torino, Italy. e-mail: paolo.peretto@ 123456unito.it

                Present address: Livio Oboti, Department of Physiology, University of Saarland School of Medicine, 66421 Homburg, Germany, e-mail:l.oboti@mx.uni-saarland.de

                This article was submitted to Frontiers in Neurogenesis, a specialty of Frontiers in Neuroscience.

                Article
                10.3389/fnins.2011.00113
                3182443
                21994486
                Copyright © 2011 Oboti, Schellino, Giachino, Chamero, Pyrski, Leinders-Zufall, Zufall, Fasolo and Peretto.

                This is an open-access article subject to a non-exclusive license between the authors and Frontiers Media SA, which permits use, distribution and reproduction in other forums, provided the original authors and source are credited and other Frontiers conditions are complied with.

                Counts
                Figures: 7, Tables: 1, Equations: 0, References: 62, Pages: 14, Words: 10799
                Categories
                Neuroscience
                Original Research

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