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Complete Connectomic Reconstruction of Olfactory Projection Neurons in the Fly Brain.

Authors
  • Bates, Alexander S1
  • Schlegel, Philipp2
  • Roberts, Ruairi J V3
  • Drummond, Nikolas3
  • Tamimi, Imaan F M3
  • Turnbull, Robert3
  • Zhao, Xincheng4
  • Marin, Elizabeth C3
  • Popovici, Patricia D1
  • Dhawan, Serene3
  • Jamasb, Arian3
  • Javier, Alexandre3
  • Serratosa Capdevila, Laia3
  • Li, Feng5
  • Rubin, Gerald M5
  • Waddell, Scott6
  • Bock, Davi D7
  • Costa, Marta3
  • Jefferis, Gregory S X E8
  • 1 Neurobiology Division, MRC Laboratory of Molecular Biology, Cambridge CB2 0QH, UK.
  • 2 Neurobiology Division, MRC Laboratory of Molecular Biology, Cambridge CB2 0QH, UK; Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, UK.
  • 3 Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, UK.
  • 4 Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, UK; Department of Entomology, College of Plant Protection, Henan Agricultural University, Zhengzhou 450002, China. , (China)
  • 5 Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, VA 20147, USA.
  • 6 Centre for Neural Circuits and Behaviour, The University of Oxford, Oxford OX1 3SR, UK.
  • 7 Department of Neurological Sciences, Larner College of Medicine, University of Vermont, VT 05405, USA.
  • 8 Neurobiology Division, MRC Laboratory of Molecular Biology, Cambridge CB2 0QH, UK; Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, UK. Electronic address: [email protected]
Type
Published Article
Journal
Current biology : CB
Publication Date
Aug 17, 2020
Volume
30
Issue
16
Identifiers
DOI: 10.1016/j.cub.2020.06.042
PMID: 32619485
Source
Medline
Keywords
Language
English
License
Unknown

Abstract

Nervous systems contain sensory neurons, local neurons, projection neurons, and motor neurons. To understand how these building blocks form whole circuits, we must distil these broad classes into neuronal cell types and describe their network connectivity. Using an electron micrograph dataset for an entire Drosophila melanogaster brain, we reconstruct the first complete inventory of olfactory projections connecting the antennal lobe, the insect analog of the mammalian olfactory bulb, to higher-order brain regions in an adult animal brain. We then connect this inventory to extant data in the literature, providing synaptic-resolution "holotypes" both for heavily investigated and previously unknown cell types. Projection neurons are approximately twice as numerous as reported by light level studies; cell types are stereotyped, but not identical, in cell and synapse numbers between brain hemispheres. The lateral horn, the insect analog of the mammalian cortical amygdala, is the main target for this olfactory information and has been shown to guide innate behavior. Here, we find new connectivity motifs, including axo-axonic connectivity between projection neurons, feedback, and lateral inhibition of these axons by a large population of neurons, and the convergence of different inputs, including non-olfactory inputs and memory-related feedback onto third-order olfactory neurons. These features are less prominent in the mushroom body calyx, the insect analog of the mammalian piriform cortex and a center for associative memory. Our work provides a complete neuroanatomical platform for future studies of the adult Drosophila olfactory system. Copyright © 2020 MRC Laboratory of Molecular Biology. Published by Elsevier Inc. All rights reserved.

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