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      A micro-CT-based standard brain atlas of the bumblebee

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          Abstract

          In recent years, bumblebees have become a prominent insect model organism for a variety of biological disciplines, particularly to investigate learning behaviors as well as visual performance. Understanding these behaviors and their underlying neurobiological principles requires a clear understanding of brain anatomy. Furthermore, to be able to compare neuronal branching patterns across individuals, a common framework is required, which has led to the development of 3D standard brain atlases in most of the neurobiological insect model species. Yet, no bumblebee 3D standard brain atlas has been generated. Here we present a brain atlas for the buff-tailed bumblebee Bombus terrestris using micro-computed tomography (micro-CT) scans as a source for the raw data sets, rather than traditional confocal microscopy, to produce the first ever micro-CT-based insect brain atlas. We illustrate the advantages of the micro-CT technique, namely, identical native resolution in the three cardinal planes and 3D structure being better preserved. Our Bombus terrestris brain atlas consists of 30 neuropils reconstructed from ten individual worker bees, with micro-CT allowing us to segment neuropils completely intact, including the lamina, which is a tissue structure often damaged when dissecting for immunolabeling. Our brain atlas can serve as a platform to facilitate future neuroscience studies in bumblebees and illustrates the advantages of micro-CT for specific applications in insect neuroanatomy.

          Supplementary information

          The online version contains supplementary material available at 10.1007/s00441-021-03482-z.

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          A GAL4-driver line resource for Drosophila neurobiology.

          We established a collection of 7,000 transgenic lines of Drosophila melanogaster. Expression of GAL4 in each line is controlled by a different, defined fragment of genomic DNA that serves as a transcriptional enhancer. We used confocal microscopy of dissected nervous systems to determine the expression patterns driven by each fragment in the adult brain and ventral nerve cord. We present image data on 6,650 lines. Using both manual and machine-assisted annotation, we describe the expression patterns in the most useful lines. We illustrate the utility of these data for identifying novel neuronal cell types, revealing brain asymmetry, and describing the nature and extent of neuronal shape stereotypy. The GAL4 lines allow expression of exogenous genes in distinct, small subsets of the adult nervous system. The set of DNA fragments, each driving a documented expression pattern, will facilitate the generation of additional constructs for manipulating neuronal function. Copyright © 2012 The Authors. Published by Elsevier Inc. All rights reserved.
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            The neuronal architecture of the mushroom body provides a logic for associative learning

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              An Anatomically Constrained Model for Path Integration in the Bee Brain

              Path integration is a widespread navigational strategy in which directional changes and distance covered are continuously integrated on an outward journey, enabling a straight-line return to home. Bees use vision for this task – a celestial-cue based visual compass, and an optic-flow based visual odometer – but the underlying neural integration mechanisms are unknown. Using intracellular electrophysiology, we show that polarized-light based compass-neurons and optic-flow-based speed-encoding neurons converge in the central complex of the bee brain, and through block-face electron microscopy we identify potential integrator cells. Based on plausible output targets for these cells, we propose a complete circuit for path integration and steering in the central complex, with anatomically-identified neurons suggested for each processing step. The resulting model-circuit is thus fully constrained biologically and provides a functional interpretation for many previously unexplained architectural features of the central complex. Moreover, we show that the receptive fields of the newly discovered speed neurons can support path integration for the holonomic motion (i.e. a ground velocity that is not precisely aligned with body orientation) typical of bee-flight, a feature not captured in any previously proposed model of path integration. In a broader context, the model-circuit presented provides a general mechanism for producing steering signals by comparing current and desired headings – suggesting a more basic function for central-complex connectivity from which path integration may have evolved.

                Author and article information

                Contributors
                keram.pfeiffer@uni-wuerzburg.de
                Journal
                Cell Tissue Res
                Cell Tissue Res
                Cell and Tissue Research
                Springer Berlin Heidelberg (Berlin/Heidelberg )
                0302-766X
                1432-0878
                28 June 2021
                28 June 2021
                2021
                : 386
                : 1
                : 29-45
                Affiliations
                [1 ]GRID grid.8379.5, ISNI 0000 0001 1958 8658, Department of Behavioral Physiology and Sociobiology, Biocenter, , University of Würzburg, ; 97074 Würzburg, Germany
                [2 ]GRID grid.7445.2, ISNI 0000 0001 2113 8111, Department of Life Sciences, , Imperial College London, ; Silwood Park, Buckhurst Road, Ascot, Berkshire, SL5 7PY UK
                Author information
                http://orcid.org/0000-0002-4539-6681
                http://orcid.org/0000-0001-9389-1284
                http://orcid.org/0000-0001-5348-2304
                Article
                3482
                10.1007/s00441-021-03482-z
                8526489
                34181089
                b208eabd-64e9-4a0b-b6d2-60b59d1d01b6
                © The Author(s) 2021

                Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 19 December 2020
                : 3 June 2021
                Funding
                Funded by: Julius-Maximilians-Universität Würzburg (3088)
                Categories
                Regular Article
                Custom metadata
                © Springer-Verlag GmbH Germany, part of Springer Nature 2021

                Molecular medicine
                bombus terrestris,insect standard brain atlas,iterative shape averaging,neuropils,reconstruction

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