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      Information flow, cell types and stereotypy in a full olfactory connectome

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          Abstract

          The hemibrain connectome provides large-scale connectivity and morphology information for the majority of the central brain of Drosophila melanogaster. Using this data set, we provide a complete description of the Drosophila olfactory system, covering all first, second and lateral horn-associated third-order neurons. We develop a generally applicable strategy to extract information flow and layered organisation from connectome graphs, mapping olfactory input to descending interneurons. This identifies a range of motifs including highly lateralised circuits in the antennal lobe and patterns of convergence downstream of the mushroom body and lateral horn. Leveraging a second data set we provide a first quantitative assessment of inter- versus intra-individual stereotypy. Comparing neurons across two brains (three hemispheres) reveals striking similarity in neuronal morphology across brains. Connectivity correlates with morphology and neurons of the same morphological type show similar connection variability within the same brain as across two brains.

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          Most cited references130

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          The Structure of the Nervous System of the Nematode Caenorhabditis elegans

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            Mushroom body memoir: from maps to models.

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              A connectome and analysis of the adult Drosophila central brain

              The neural circuits responsible for animal behavior remain largely unknown. We summarize new methods and present the circuitry of a large fraction of the brain of the fruit fly Drosophila melanogaster. Improved methods include new procedures to prepare, image, align, segment, find synapses in, and proofread such large data sets. We define cell types, refine computational compartments, and provide an exhaustive atlas of cell examples and types, many of them novel. We provide detailed circuits consisting of neurons and their chemical synapses for most of the central brain. We make the data public and simplify access, reducing the effort needed to answer circuit questions, and provide procedures linking the neurons defined by our analysis with genetic reagents. Biologically, we examine distributions of connection strengths, neural motifs on different scales, electrical consequences of compartmentalization, and evidence that maximizing packing density is an important criterion in the evolution of the fly’s brain.
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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
                25 May 2021
                2021
                : 10
                : e66018
                Affiliations
                [1 ]Neurobiology Division, MRC Laboratory of Molecular Biology CambridgeUnited Kingdom
                [2 ]Department of Zoology, University of Cambridge CambridgeUnited Kingdom
                [3 ]Janelia Research Campus, Howard Hughes Medical Institute AshburnUnited States
                [4 ]Department of Neurobiology, Harvard Medical School BostonUnited States
                Brandeis University United States
                Harvard University United States
                Brandeis University United States
                Howard Hughes Medical Institute, Stanford University United States
                Author notes
                [†]

                These authors contributed equally to this work.

                [‡]

                These authors also contributed equally to this work.

                Author information
                https://orcid.org/0000-0002-5633-1314
                https://orcid.org/0000-0002-1195-0445
                https://orcid.org/0000-0003-4054-0784
                https://orcid.org/0000-0002-2078-1145
                https://orcid.org/0000-0001-6333-0072
                https://orcid.org/0000-0002-6658-9175
                https://orcid.org/0000-0001-8762-8703
                https://orcid.org/0000-0001-7425-8555
                https://orcid.org/0000-0001-5948-3092
                https://orcid.org/0000-0002-0587-9355
                Article
                66018
                10.7554/eLife.66018
                8298098
                34032214
                a34264bd-a2a9-46fc-92be-1502c4dff139
                © 2021, Schlegel 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
                : 22 December 2020
                : 24 May 2021
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/100004440, Wellcome Trust;
                Award ID: Collaborative Award 203261/Z/16/Z
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100000781, European Research Council;
                Award ID: Consolidator grant 649111
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100000265, Medical Research Council;
                Award ID: Core support MC-U105188491
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000002, National Institutes of Health;
                Award ID: BRAIN Initiative grant 1RF1MH120679-01
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000002, National Institutes of Health;
                Award ID: F31 fellowship DC016196
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100001645, Boehringer Ingelheim Fonds;
                Award ID: PhD Fellowship
                Award Recipient :
                Funded by: Herchel Smith;
                Award ID: Studentship
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000002, National Institutes of Health;
                Award ID: R01DC008174
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000011, Howard Hughes Medical Institute;
                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
                Synaptic resolution analysis of a full olfactory connectome reveals lateralised circuits, convergence of innate and learned pathways, and shows that homologous neurons are highly stereotyped within and across brains.

                Life sciences
                connectomics,olfaction,stereotypy,neuroanatomy,synapses,drosophila,d. melanogaster
                Life sciences
                connectomics, olfaction, stereotypy, neuroanatomy, synapses, drosophila, d. melanogaster

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