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Systematic annotation of a complete adult male Drosophila nerve cord connectome reveals principles of functional organisation

View ORCID ProfileElizabeth C. Marin, View ORCID ProfileBilly J. Morris, View ORCID ProfileTomke Stürner, View ORCID ProfileAndrew S. Champion, View ORCID ProfileDominik Krzeminski, View ORCID ProfileGriffin Badalamente, View ORCID ProfileMarina Gkantia, View ORCID ProfileChristopher R. Dunne, View ORCID ProfileKatharina Eichler, View ORCID ProfileShin-ya Takemura, View ORCID ProfileImaan F. M. Tamimi, View ORCID ProfileSiqi Fang, View ORCID ProfileSung Soo Moon, View ORCID ProfileHan S. J. Cheong, View ORCID ProfileFeng Li, View ORCID ProfilePhilipp Schlegel, Sebastian E. Ahnert, View ORCID ProfileStuart Berg, Janelia FlyEM Project Team, View ORCID ProfileGwyneth M. Card, View ORCID ProfileMarta Costa, View ORCID ProfileDavid Shepherd, View ORCID ProfileGregory S.X.E. Jefferis
doi: https://doi.org/10.1101/2023.06.05.543407
Elizabeth C. Marin
1Drosophila Connectomics Group, Department of Zoology, University of Cambridge, Downing Street, Cambridge, UK
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  • For correspondence: [email protected] [email protected]
Billy J. Morris
1Drosophila Connectomics Group, Department of Zoology, University of Cambridge, Downing Street, Cambridge, UK
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Tomke Stürner
2Neurobiology Division, MRC Laboratory of Molecular Biology, Cambridge, UK
1Drosophila Connectomics Group, Department of Zoology, University of Cambridge, Downing Street, Cambridge, UK
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Andrew S. Champion
1Drosophila Connectomics Group, Department of Zoology, University of Cambridge, Downing Street, Cambridge, UK
2Neurobiology Division, MRC Laboratory of Molecular Biology, Cambridge, UK
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Dominik Krzeminski
1Drosophila Connectomics Group, Department of Zoology, University of Cambridge, Downing Street, Cambridge, UK
2Neurobiology Division, MRC Laboratory of Molecular Biology, Cambridge, UK
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Griffin Badalamente
1Drosophila Connectomics Group, Department of Zoology, University of Cambridge, Downing Street, Cambridge, UK
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  • ORCID record for Griffin Badalamente
Marina Gkantia
1Drosophila Connectomics Group, Department of Zoology, University of Cambridge, Downing Street, Cambridge, UK
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  • ORCID record for Marina Gkantia
Christopher R. Dunne
1Drosophila Connectomics Group, Department of Zoology, University of Cambridge, Downing Street, Cambridge, UK
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Katharina Eichler
1Drosophila Connectomics Group, Department of Zoology, University of Cambridge, Downing Street, Cambridge, UK
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Shin-ya Takemura
4Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, USA
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Imaan F. M. Tamimi
1Drosophila Connectomics Group, Department of Zoology, University of Cambridge, Downing Street, Cambridge, UK
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Siqi Fang
1Drosophila Connectomics Group, Department of Zoology, University of Cambridge, Downing Street, Cambridge, UK
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Sung Soo Moon
3Department of Chemical Engineering and Biotechnology, University of Cambridge, Philippa Fawcett Drive, Cambridge, UK
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Han S. J. Cheong
4Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, USA
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Feng Li
4Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, USA
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Philipp Schlegel
1Drosophila Connectomics Group, Department of Zoology, University of Cambridge, Downing Street, Cambridge, UK
2Neurobiology Division, MRC Laboratory of Molecular Biology, Cambridge, UK
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Sebastian E. Ahnert
3Department of Chemical Engineering and Biotechnology, University of Cambridge, Philippa Fawcett Drive, Cambridge, UK
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Stuart Berg
4Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, USA
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4Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, USA
Gwyneth M. Card
4Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, USA
5Zuckerman Institute, Columbia University, New York, USA
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Marta Costa
1Drosophila Connectomics Group, Department of Zoology, University of Cambridge, Downing Street, Cambridge, UK
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David Shepherd
6School of Biological Sciences, University of Southampton, Southampton, UK
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Gregory S.X.E. Jefferis
2Neurobiology Division, MRC Laboratory of Molecular Biology, Cambridge, UK
1Drosophila Connectomics Group, Department of Zoology, University of Cambridge, Downing Street, Cambridge, UK
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  • For correspondence: [email protected] [email protected]
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Summary

Nervous systems function as ensembles of neurons communicating via synaptic connections, and a functional understanding of nervous systems requires extensive knowledge of their connectomes. In a companion paper (Takemura et al., 2023), we describe the acquisition of a complete fruit fly nerve cord connectome, the first for an animal that can walk or fly. Here, to efficiently navigate and to appreciate the biological significance of this connectome, we categorise and name nearly all neurons systematically and link them to the experimental literature. We employ a system of hierarchical coarse annotations and group similar neurons across the midline and across segments, then define systematic cell types for sensory neurons, intrinsic neurons, ascending neurons, and non-motor efferent neurons. Stereotyped arrays of neuroblasts generate related neuron populations called hemilineages that repeat across the segments of the nerve cord. We confirm that larval-born neurons from a given hemilineage generally express the same neurotransmitter but find that earlier born neurons often express a different one. We match over 35% of intrinsic, ascending, and non-motor efferent neurons across segments, defining serial sets which were crucial for systematic typing of motor neurons and sensory neurons. We assign a sensory modality to over 5000 sensory neurons, cluster them by connectivity, and identify serially homologous cell types and a layered organisation likely corresponding to peripheral topography. Finally, we present selected examples of sensory circuits predicated on programmatic analysis of a complete VNC connectome. Our annotations are critical for analysing the structure of descending input to the nerve cord and of motor output, both described in a third companion paper (Cheong et al., 2023). These annotations are being released as part of the neuprint.janelia.org and clio.janelia.org web applications and also serve as the basis for programmatic analysis of the connectome through dedicated tools that we describe in this paper.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • This version incorporates substantial revisions in response to comments from colleagues in the field. It accompanies a new release of Neuprint and Clio Neuroglancer with revised annotations including cell type information.

  • https://neuprint.janelia.org/

  • https://clio.janelia.org/

  • https://github.com/natverse/malevnc

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 March 11, 2024.
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Systematic annotation of a complete adult male Drosophila nerve cord connectome reveals principles of functional organisation
Elizabeth C. Marin, Billy J. Morris, Tomke Stürner, Andrew S. Champion, Dominik Krzeminski, Griffin Badalamente, Marina Gkantia, Christopher R. Dunne, Katharina Eichler, Shin-ya Takemura, Imaan F. M. Tamimi, Siqi Fang, Sung Soo Moon, Han S. J. Cheong, Feng Li, Philipp Schlegel, Sebastian E. Ahnert, Stuart Berg, Janelia FlyEM Project Team, Gwyneth M. Card, Marta Costa, David Shepherd, Gregory S.X.E. Jefferis
bioRxiv 2023.06.05.543407; doi: https://doi.org/10.1101/2023.06.05.543407
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Systematic annotation of a complete adult male Drosophila nerve cord connectome reveals principles of functional organisation
Elizabeth C. Marin, Billy J. Morris, Tomke Stürner, Andrew S. Champion, Dominik Krzeminski, Griffin Badalamente, Marina Gkantia, Christopher R. Dunne, Katharina Eichler, Shin-ya Takemura, Imaan F. M. Tamimi, Siqi Fang, Sung Soo Moon, Han S. J. Cheong, Feng Li, Philipp Schlegel, Sebastian E. Ahnert, Stuart Berg, Janelia FlyEM Project Team, Gwyneth M. Card, Marta Costa, David Shepherd, Gregory S.X.E. Jefferis
bioRxiv 2023.06.05.543407; doi: https://doi.org/10.1101/2023.06.05.543407

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