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      Functional and anatomical specificity in a higher olfactory centre

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          Abstract

          Most sensory systems are organized into parallel neuronal pathways that process distinct aspects of incoming stimuli. In the insect olfactory system, second order projection neurons target both the mushroom body, required for learning, and the lateral horn (LH), proposed to mediate innate olfactory behavior. Mushroom body neurons form a sparse olfactory population code, which is not stereotyped across animals. In contrast, odor coding in the LH remains poorly understood. We combine genetic driver lines, anatomical and functional criteria to show that the Drosophila LH has ~1400 neurons and >165 cell types. Genetically labeled LHNs have stereotyped odor responses across animals and on average respond to three times more odors than single projection neurons. LHNs are better odor categorizers than projection neurons, likely due to stereotyped pooling of related inputs. Our results reveal some of the principles by which a higher processing area can extract innate behavioral significance from sensory stimuli.

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          Most cited references43

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          The mushroom body of adult Drosophila characterized by GAL4 drivers.

          The mushroom body is required for a variety of behaviors of Drosophila melanogaster. Different types of intrinsic and extrinsic mushroom body neurons might underlie its functional diversity. There have been many GAL4 driver lines identified that prominently label the mushroom body intrinsic neurons, which are known as "Kenyon cells." Under one constant experimental condition, we analyzed and compared the the expression patterns of 25 GAL4 drivers labeling the mushroom body. As an internet resource, we established a digital catalog indexing representative confocal data of them. Further more, we counted the number of GAL4-positive Kenyon cells in each line. We found that approximately 2,000 Kenyon cells can be genetically labeled in total. Three major Kenyon cell subtypes, the gamma, alpha'/beta', and alpha/beta neurons, respectively, contribute to 33, 18, and 49% of 2,000 Kenyon cells. Taken together, this study lays groundwork for functional dissection of the mushroom body.
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            Role of GABAergic inhibition in shaping odor-evoked spatiotemporal patterns in the Drosophila antennal lobe.

            Drosophila olfactory receptor neurons project to the antennal lobe, the insect analog of the mammalian olfactory bulb. GABAergic synaptic inhibition is thought to play a critical role in olfactory processing in the antennal lobe and olfactory bulb. However, the properties of GABAergic neurons and the cellular effects of GABA have not been described in Drosophila, an important model organism for olfaction research. We have used whole-cell patch-clamp recording, pharmacology, immunohistochemistry, and genetic markers to investigate how GABAergic inhibition affects olfactory processing in the Drosophila antennal lobe. We show that many axonless local neurons (LNs) in the adult antennal lobe are GABAergic. GABA hyperpolarizes antennal lobe projection neurons (PNs) via two distinct conductances, blocked by a GABAA- and GABAB-type antagonist, respectively. Whereas GABAA receptors shape PN odor responses during the early phase of odor responses, GABAB receptors mediate odor-evoked inhibition on longer time scales. The patterns of odor-evoked GABAB-mediated inhibition differ across glomeruli and across odors. Finally, we show that LNs display broad but diverse morphologies and odor preferences, suggesting a cellular basis for odor- and glomerulus-dependent patterns of inhibition. Together, these results are consistent with a model in which odors elicit stimulus-specific spatial patterns of GABA release, and as a result, GABAergic inhibition increases the degree of difference between the neural representations of different odors.
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              Transformation of olfactory representations in the Drosophila antennal lobe.

              Molecular genetics has revealed a precise stereotypy in the projection of primary olfactory sensory neurons onto secondary neurons. A major challenge is to understand how this mapping translates into odor responses in these second-order neurons. We investigated this question in Drosophila using whole-cell recordings in vivo. We observe that monomolecular odors generally elicit responses in large ensembles of antennal lobe neurons. Comparison of odor-evoked activity from afferents and postsynaptic neurons in the same glomerulus revealed that second-order neurons display broader tuning and more complex responses than their primary afferents. This indicates a major transformation of odor representations, implicating lateral interactions within the antennal lobe.
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                Author and article information

                Contributors
                Role: Reviewing Editor
                Role: Senior Editor
                Journal
                eLife
                Elife
                eLife
                eLife
                eLife Sciences Publications, Ltd
                2050-084X
                21 May 2019
                2019
                : 8
                : e44590
                Affiliations
                [1 ]deptNeurobiology Division MRC Laboratory of Molecular Biology CambridgeUnited Kingdom
                [2 ]deptDepartment of Neuroscience, Physiology and Pharmacology University College London LondonUnited Kingdom
                [3 ]deptNeurophysiology of Behaviour Laboratory The Francis Crick Institute LondonUnited Kingdom
                [4 ]deptJanelia Research Campus Howard Hughes Medical Institute Chevy ChaseUnited States
                [5 ]deptDepartment of Zoology University of Cambridge CambridgeUnited Kingdom
                National Centre for Biological Sciences, Tata Institute of Fundamental Research India
                National Centre for Biological Sciences, Tata Institute of Fundamental Research India
                National Centre for Biological Sciences, Tata Institute of Fundamental Research India
                Technical University of Munich Germany
                Author information
                https://orcid.org/0000-0002-0431-5849
                https://orcid.org/0000-0002-1195-0445
                https://orcid.org/0000-0002-3990-8724
                https://orcid.org/0000-0001-9666-3682
                http://orcid.org/0000-0001-9260-3156
                http://orcid.org/0000-0002-6727-7579
                http://orcid.org/0000-0002-8218-7926
                https://orcid.org/0000-0002-0587-9355
                Article
                44590
                10.7554/eLife.44590
                6550879
                31112127
                78193b34-13e5-4492-b65d-e2cf216b50cf
                © 2019, Frechter et al

                This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

                History
                : 20 December 2018
                : 12 April 2019
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100000780, European Commission;
                Award ID: ERC CoG 649111
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100000265, Medical Research Council;
                Award ID: U105188491
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100000780, European Commission;
                Award ID: ERC StG 211089
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100004440, Wellcome;
                Award ID: 203261/Z/16/Z
                Award Recipient :
                The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
                Categories
                Research Article
                Neuroscience
                Custom metadata
                The Drosophila lateral horn, a higher olfactory brain area, contains >165 genetically defined cell types with stereotyped odour responses across animals and improved odor categorisation compared with their inputs.

                Life sciences
                olfaction,neuroscience,cell type,drosophila,lateral horn,neuroanatomy,d. melanogaster
                Life sciences
                olfaction, neuroscience, cell type, drosophila, lateral horn, neuroanatomy, d. melanogaster

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