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Complete connectomic reconstruction of olfactory projection neurons in the fly brain

View ORCID ProfileA.S. Bates, View ORCID ProfileP. Schlegel, View ORCID ProfileR.J.V. Roberts, View ORCID ProfileN. Drummond, View ORCID ProfileI.F.M. Tamimi, View ORCID ProfileR. Turnbull, View ORCID ProfileX. Zhao, View ORCID ProfileE.C. Marin, View ORCID ProfileP.D. Popovici, View ORCID ProfileS. Dhawan, View ORCID ProfileA. Jamasb, View ORCID ProfileA. Javier, View ORCID ProfileF. Li, View ORCID ProfileG.M. Rubin, View ORCID ProfileS. Waddell, View ORCID ProfileD.D. Bock, View ORCID ProfileM. Costa, View ORCID ProfileG.S.X.E. Jefferis
doi: https://doi.org/10.1101/2020.01.19.911453
A.S. Bates
Neurobiology Division, MRC Laboratory of Molecular Biology, Cambridge, United Kingdom
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P. Schlegel
Neurobiology Division, MRC Laboratory of Molecular Biology, Cambridge, United KingdomDepartment of Zoology, University of Cambridge, Cambridge, United Kingdom
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  • ORCID record for P. Schlegel
R.J.V. Roberts
Department of Zoology, University of Cambridge, Cambridge, United Kingdom
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N. Drummond
Department of Zoology, University of Cambridge, Cambridge, United Kingdom
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  • ORCID record for N. Drummond
I.F.M. Tamimi
Department of Zoology, University of Cambridge, Cambridge, United Kingdom
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R. Turnbull
Department of Zoology, University of Cambridge, Cambridge, United Kingdom
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X. Zhao
Department of Zoology, University of Cambridge, Cambridge, United KingdomDepartment of Entomology, Henan Agricultural University, Zhengzhou, China
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E.C. Marin
Department of Zoology, University of Cambridge, Cambridge, United Kingdom
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P.D. Popovici
Neurobiology Division, MRC Laboratory of Molecular Biology, Cambridge, United Kingdom
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S. Dhawan
Department of Zoology, University of Cambridge, Cambridge, United Kingdom
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A. Jamasb
Department of Zoology, University of Cambridge, Cambridge, United Kingdom
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A. Javier
Department of Zoology, University of Cambridge, Cambridge, United Kingdom
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F. Li
Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
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G.M. Rubin
Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
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S. Waddell
Centre for Neural Circuits and Behaviour, The University of Oxford, United Kingdom
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D.D. Bock
Department of Neurological Sciences, Larner College of Medicine, United States
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M. Costa
Department of Zoology, University of Cambridge, Cambridge, United Kingdom
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G.S.X.E. Jefferis
Neurobiology Division, MRC Laboratory of Molecular Biology, Cambridge, United KingdomDepartment of Zoology, University of Cambridge, Cambridge, United Kingdom
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  • For correspondence: jefferis@mrc-lmb.cam.ac.uk
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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 analogue 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 analogue of the mammalian cortical amygdala, is the main target for this olfactory information and has been shown to guide innate behaviour. Here, we find new connectivity motifs, including: axo-axonic connectivity between projection neurons; feedback and lateral inhibition of these axons by local neurons; and the convergence of different inputs, including non-olfactory inputs and memory-related feedback onto lateral horn neurons. This differs from the configuration of the second most prominent target for olfactory projection neurons: the mushroom body calyx, the insect analogue of the mammalian piriform cortex and a centre for associative memory. Our work provides a complete neuroanatomical platform for future studies of the adult Drosophila olfactory system.

Highlights

  • First complete parts list for second-order neurons of an adult olfactory system

  • Quantification of left-right stereotypy in cell and synapse number

  • Axo-axonic connections form hierarchical communities in the lateral horn

  • Local neurons and memory-related feedback target projection neuron axons

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted January 20, 2020.
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Complete connectomic reconstruction of olfactory projection neurons in the fly brain
A.S. Bates, P. Schlegel, R.J.V. Roberts, N. Drummond, I.F.M. Tamimi, R. Turnbull, X. Zhao, E.C. Marin, P.D. Popovici, S. Dhawan, A. Jamasb, A. Javier, F. Li, G.M. Rubin, S. Waddell, D.D. Bock, M. Costa, G.S.X.E. Jefferis
bioRxiv 2020.01.19.911453; doi: https://doi.org/10.1101/2020.01.19.911453
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Complete connectomic reconstruction of olfactory projection neurons in the fly brain
A.S. Bates, P. Schlegel, R.J.V. Roberts, N. Drummond, I.F.M. Tamimi, R. Turnbull, X. Zhao, E.C. Marin, P.D. Popovici, S. Dhawan, A. Jamasb, A. Javier, F. Li, G.M. Rubin, S. Waddell, D.D. Bock, M. Costa, G.S.X.E. Jefferis
bioRxiv 2020.01.19.911453; doi: https://doi.org/10.1101/2020.01.19.911453

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