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      Prenatal and Early Postnatal Odorant Exposure Heightens Odor-Evoked Mitral Cell Responses in the Mouse Olfactory Bulb

      research-article
      1 , 2 , 4 , 1 , 2 , 3 , 4 ,
      eNeuro
      Society for Neuroscience
      mitral cells, olfaction, olfactory bulb, plasticity

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          Abstract

          Early sensory experience shapes the anatomy and function of sensory circuits. In the mouse olfactory bulb (OB), prenatal and early postnatal odorant exposure through odorized food (food/odorant pairing) not only increases the volume of activated glomeruli but also increases the number of mitral and tufted cells (M/TCs) connected to activated glomeruli. Given the importance of M/TCs in OB output and in mediating lateral inhibitory networks, increasing the number of M/TCs connected to a single glomerulus may significantly change odorant representation by increasing the total output of that glomerulus and/or by increasing the strength of lateral inhibition mediated by cells connected to the affected glomerulus. Here, we seek to understand the functional impact of this long-term odorant exposure paradigm on the population activity of mitral cells (MCs). We use viral expression of GCaMP6s to examine odor-evoked responses of MCs following prenatal and early postnatal odorant exposure to two dissimilar odorants, methyl salicylate (MS) and hexanal, which are both strong activators of glomeruli on the dorsal OB surface. Previous work suggests that odor familiarity may decrease odor-evoked MC response in rodents. However, we find that early food-based odorant exposure significantly changes MC responses in an unexpected way, resulting in broad increases in the amplitude, number, and reliability of excitatory MC responses across the dorsal OB.

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          Most cited references39

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          Topographic organization of sensory projections to the olfactory bulb.

          The detection of odorant receptor mRNAs within the axon terminals of sensory neurons has permitted us to ask whether neurons expressing a given receptor project their axons to common glomeruli within the olfactory bulb. In situ hybridization with five different receptor probes demonstrates that axons from neurons expressing a given receptor converge on one, or at most, a few glomeruli within the olfactory bulb. Moreover, the position of specific glomeruli is bilaterally symmetric and is constant in different individuals within a species. These data support a model in which exposure to a given odorant may result in the stimulation of a spatially restricted set of glomeruli, such that the individual odorants would be associated with specific topographic patterns of activity within the olfactory bulb.
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            Information coding in the olfactory system: evidence for a stereotyped and highly organized epitope map in the olfactory bulb.

            In the mammalian olfactory system, information from approximately 1000 different odorant receptor types is organized in the nose into four spatial zones. Each zone is a mosaic of randomly distributed neurons expressing different receptor types. In these studies, we have obtained evidence that information highly distributed in the nose is transformed in the olfactory bulb of the brain into a highly organized spatial map. We find that specific odorant receptor gene probes hybridize in situ to small, and distinct, subsets of olfactory bulb glomeruli. The spatial and numerical characteristics of the patterns of hybridization that we observe with different receptor probes indicate that, in the olfactory bulb, olfactory information undergoes a remarkable organization into a fine, and perhaps stereotyped, spatial map. In our view, this map is in essence an epitope map, whose approximately 1000 distinct components are used in a multitude of different combinations to discriminate a vast array of different odors.
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              Representation of odorants by receptor neuron input to the mouse olfactory bulb.

              To visualize odorant representations by receptor neuron input to the mouse olfactory bulb, we loaded receptor neurons with calcium-sensitive dye and imaged odorant-evoked responses from their axon terminals. Fluorescence increases reflected activation of receptor neuron populations converging onto individual glomeruli. We report several findings. First, five glomeruli were identifiable across animals based on their location and odorant responsiveness; all five showed complex response specificities. Second, maps of input were chemotopically organized at near-threshold concentrations but, at moderate concentrations, involved many widely distributed glomeruli. Third, the dynamic range of input to a glomerulus was greater than that reported for individual receptor neurons. Finally, odorant activation slopes could differ across glomeruli, and for different odorants activating the same glomerulus. These results imply a high degree of complexity in odorant representations at the level of olfactory bulb input.
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                Author and article information

                Journal
                eNeuro
                eNeuro
                eneuro
                eneuro
                eNeuro
                eNeuro
                Society for Neuroscience
                2373-2822
                25 September 2017
                26 September 2017
                Sep-Oct 2017
                : 4
                : 5
                : ENEURO.0129-17.2017
                Affiliations
                [1 ]Center for Neuroscience at the University of Pittsburgh, University of Pittsburgh , Pittsburgh, PA
                [2 ]Center for the Neural Basis of Cognition, Pittsburgh, PA
                [3 ]Department of Biological Sciences, Carnegie Mellon University , Pittsburgh, PA
                [4 ]Department of Neurobiology, University of Pittsburgh , Pittsburgh, PA
                Author notes

                The authors declare no competing financial interests.

                Author contributions: A.L. and N.N.U. designed research; A.L. performed research; A.L. analyzed data; A.L. and N.N.U. wrote the paper.

                This work was supported by National Institute on Deafness and Other Communication Disorders Grants RO1DC011184 (to N.N.U.) and F30DC015161 (to A.L.) and by the Pennsylvania Department of Health Commonwealth Universal Research Enhancement Program (N.N.U.).

                Correspondence should be addressed to Nathaniel N. Urban, Department of Neurobiology, University of Pittsburgh, E1440 BSTWR, 200 Lothrop Street, Pittsburgh, PA 15213, E-mail: nurban@ 123456pitt.edu .
                Author information
                http://orcid.org/0000-0003-0729-4390
                Article
                eN-NWR-0129-17
                10.1523/ENEURO.0129-17.2017
                5613225
                28955723
                096d4b73-2c52-4ebb-a491-bc11e5fbe418
                Copyright © 2017 Liu and Urban

                This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

                History
                : 12 April 2017
                : 13 August 2017
                : 14 August 2017
                Page count
                Figures: 8, Tables: 6, Equations: 0, References: 44, Pages: 23, Words: 13616
                Funding
                Funded by: http://doi.org/10.13039/100000055 HHS | NIH | National Institute on Deafness and Other Communication Disorders (NIDCD)
                Award ID: F30DC015161
                Award ID: RO1DC011184
                Funded by: Pennsylvania Department of Health Commonwealth Universal Research Enhancement Program
                Categories
                8
                8.1
                New Research
                Sensory and Motor Systems
                Custom metadata
                September/October 2017

                mitral cells,olfaction,olfactory bulb,plasticity
                mitral cells, olfaction, olfactory bulb, plasticity

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