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The connectome of an insect brain

View ORCID ProfileMichael Winding, View ORCID ProfileBenjamin D. Pedigo, View ORCID ProfileChristopher L. Barnes, View ORCID ProfileHeather G. Patsolic, View ORCID ProfileYoungser Park, View ORCID ProfileTom Kazimiers, View ORCID ProfileAkira Fushiki, Ingrid V. Andrade, View ORCID ProfileAvinash Khandelwal, View ORCID ProfileJavier Valdes-Aleman, Feng Li, View ORCID ProfileNadine Randel, View ORCID ProfileElizabeth Barsotti, View ORCID ProfileAna Correia, View ORCID ProfileRichard D. Fetter, View ORCID ProfileVolker Hartenstein, Carey E. Priebe, View ORCID ProfileJoshua T. Vogelstein, View ORCID ProfileAlbert Cardona, View ORCID ProfileMarta Zlatic
doi: https://doi.org/10.1101/2022.11.28.516756
Michael Winding
1University of Cambridge, Department of Zoology; Cambridge, UK
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  • For correspondence: mjw226@cam.ac.uk jovo@jhu.edu mz209@cam.ac.uk ac2040@cam.ac.uk
Benjamin D. Pedigo
2Johns Hopkins University, Department of Biomedical Engineering; Baltimore, MD, USA
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  • ORCID record for Benjamin D. Pedigo
Christopher L. Barnes
3University of Cambridge, Department of Physiology, Development, and Neuroscience; Cambridge, UK
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Heather G. Patsolic
4Johns Hopkins University, Department of Applied Mathematics and Statistics; Baltimore, MD, USA
5Accenture; Arlington, VA, USA
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Youngser Park
6Johns Hopkins University, Center for Imaging Science; Baltimore, MD, USA
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Tom Kazimiers
7Janelia Research Campus, Howard Hughes Medical Institute; Ashburn, VA, USA
8kazmos GmbH; Dresden, Germany
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Akira Fushiki
7Janelia Research Campus, Howard Hughes Medical Institute; Ashburn, VA, USA
9Zuckerman Mind Brain Behavior Institute, Columbia University; New York, NY, USA
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Ingrid V. Andrade
10University of California Los Angeles, Department of Molecular, Cell and Developmental Biology; Los Angeles, CA, USA
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Avinash Khandelwal
7Janelia Research Campus, Howard Hughes Medical Institute; Ashburn, VA, USA
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  • ORCID record for Avinash Khandelwal
Javier Valdes-Aleman
1University of Cambridge, Department of Zoology; Cambridge, UK
7Janelia Research Campus, Howard Hughes Medical Institute; Ashburn, VA, USA
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Feng Li
7Janelia Research Campus, Howard Hughes Medical Institute; Ashburn, VA, USA
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Nadine Randel
1University of Cambridge, Department of Zoology; Cambridge, UK
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Elizabeth Barsotti
3University of Cambridge, Department of Physiology, Development, and Neuroscience; Cambridge, UK
11MRC Laboratory of Molecular Biology, Neurobiology Division; Cambridge, UK
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Ana Correia
3University of Cambridge, Department of Physiology, Development, and Neuroscience; Cambridge, UK
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Richard D. Fetter
7Janelia Research Campus, Howard Hughes Medical Institute; Ashburn, VA, USA
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Volker Hartenstein
10University of California Los Angeles, Department of Molecular, Cell and Developmental Biology; Los Angeles, CA, USA
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Carey E. Priebe
4Johns Hopkins University, Department of Applied Mathematics and Statistics; Baltimore, MD, USA
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Joshua T. Vogelstein
2Johns Hopkins University, Department of Biomedical Engineering; Baltimore, MD, USA
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  • For correspondence: mjw226@cam.ac.uk jovo@jhu.edu mz209@cam.ac.uk ac2040@cam.ac.uk
Albert Cardona
3University of Cambridge, Department of Physiology, Development, and Neuroscience; Cambridge, UK
7Janelia Research Campus, Howard Hughes Medical Institute; Ashburn, VA, USA
11MRC Laboratory of Molecular Biology, Neurobiology Division; Cambridge, UK
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  • For correspondence: mjw226@cam.ac.uk jovo@jhu.edu mz209@cam.ac.uk ac2040@cam.ac.uk
Marta Zlatic
1University of Cambridge, Department of Zoology; Cambridge, UK
7Janelia Research Campus, Howard Hughes Medical Institute; Ashburn, VA, USA
11MRC Laboratory of Molecular Biology, Neurobiology Division; Cambridge, UK
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  • For correspondence: mjw226@cam.ac.uk jovo@jhu.edu mz209@cam.ac.uk ac2040@cam.ac.uk
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Abstract

Brains contain networks of interconnected neurons, so knowing the network architecture is essential for understanding brain function. We therefore mapped the synaptic-resolution connectome of an insect brain (Drosophila larva) with rich behavior, including learning, value-computation, and action-selection, comprising 3,013 neurons and 544,000 synapses. We characterized neuron-types, hubs, feedforward and feedback pathways, and cross-hemisphere and brain-nerve cord interactions. We found pervasive multisensory and interhemispheric integration, highly recurrent architecture, abundant feedback from descending neurons, and multiple novel circuit motifs. The brain’s most recurrent circuits comprised the input and output neurons of the learning center. Some structural features, including multilayer shortcuts and nested recurrent loops, resembled powerful machine learning architectures. The identified brain architecture provides a basis for future experimental and theoretical studies of neural circuits.

One-Sentence Summary We generated a synaptic-resolution brain connectome and characterized its connection types, neuron types, and circuit motifs.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • ↵† co-first authors

  • ‡ joint supervision

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 November 28, 2022.
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The connectome of an insect brain
Michael Winding, Benjamin D. Pedigo, Christopher L. Barnes, Heather G. Patsolic, Youngser Park, Tom Kazimiers, Akira Fushiki, Ingrid V. Andrade, Avinash Khandelwal, Javier Valdes-Aleman, Feng Li, Nadine Randel, Elizabeth Barsotti, Ana Correia, Richard D. Fetter, Volker Hartenstein, Carey E. Priebe, Joshua T. Vogelstein, Albert Cardona, Marta Zlatic
bioRxiv 2022.11.28.516756; doi: https://doi.org/10.1101/2022.11.28.516756
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The connectome of an insect brain
Michael Winding, Benjamin D. Pedigo, Christopher L. Barnes, Heather G. Patsolic, Youngser Park, Tom Kazimiers, Akira Fushiki, Ingrid V. Andrade, Avinash Khandelwal, Javier Valdes-Aleman, Feng Li, Nadine Randel, Elizabeth Barsotti, Ana Correia, Richard D. Fetter, Volker Hartenstein, Carey E. Priebe, Joshua T. Vogelstein, Albert Cardona, Marta Zlatic
bioRxiv 2022.11.28.516756; doi: https://doi.org/10.1101/2022.11.28.516756

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