Whole-brain annotation and multi-connectome cell typing of Drosophila

Philipp Schlegel, Yijie Yin, Alexander S. Bates, Sven Dorkenwald, Katharina Eichler, Paul Brooks, Daniel S. Han, Marina Gkantia, Marcia Santos, Eva J. Munnelly, Griffin Badalamente, Laia Serratosa Capdevila, Varun A. Sane, Alexandra M. C. Fragniere, Ladann Kiassat, Markus W. Pleijzier, Tomke Stürner, Imaan F. M. Tamimi, Christopher R. Dunne, Irene Salgarella, Alexandre Javier, Siqi Fang, Eric Perlman, Tom Kazimiers, Sridhar R. Jagannathan, Arie Matsliah, Amy R. Sterling, Szi-chieh Yu, Claire E. McKellar, Marta Costa, H. Sebastian Seung, Mala Murthy, Volker Hartenstein, Davi D. Bock () and Gregory S. X. E. Jefferis ()
Additional contact information
Philipp Schlegel: MRC Laboratory of Molecular Biology
Yijie Yin: University of Cambridge
Alexander S. Bates: MRC Laboratory of Molecular Biology
Sven Dorkenwald: Princeton University
Katharina Eichler: University of Cambridge
Paul Brooks: University of Cambridge
Daniel S. Han: MRC Laboratory of Molecular Biology
Marina Gkantia: University of Cambridge
Marcia Santos: University of Cambridge
Eva J. Munnelly: University of Cambridge
Griffin Badalamente: University of Cambridge
Laia Serratosa Capdevila: University of Cambridge
Varun A. Sane: University of Cambridge
Alexandra M. C. Fragniere: University of Cambridge
Ladann Kiassat: University of Cambridge
Markus W. Pleijzier: MRC Laboratory of Molecular Biology
Tomke Stürner: MRC Laboratory of Molecular Biology
Imaan F. M. Tamimi: University of Cambridge
Christopher R. Dunne: University of Cambridge
Irene Salgarella: University of Cambridge
Alexandre Javier: University of Cambridge
Siqi Fang: University of Cambridge
Eric Perlman: Yikes
Tom Kazimiers: kazmos
Sridhar R. Jagannathan: University of Cambridge
Arie Matsliah: Princeton University
Amy R. Sterling: Princeton University
Szi-chieh Yu: Princeton University
Claire E. McKellar: Princeton University
Marta Costa: University of Cambridge
H. Sebastian Seung: Princeton University
Mala Murthy: Princeton University
Volker Hartenstein: University of California Los Angeles
Davi D. Bock: University of Vermont
Gregory S. X. E. Jefferis: MRC Laboratory of Molecular Biology

Nature, 2024, vol. 634, issue 8032, 139-152

Abstract: Abstract The fruit fly Drosophila melanogaster has emerged as a key model organism in neuroscience, in large part due to the concentration of collaboratively generated molecular, genetic and digital resources available for it. Here we complement the approximately 140,000 neuron FlyWire whole-brain connectome1 with a systematic and hierarchical annotation of neuronal classes, cell types and developmental units (hemilineages). Of 8,453 annotated cell types, 3,643 were previously proposed in the partial hemibrain connectome2, and 4,581 are new types, mostly from brain regions outside the hemibrain subvolume. Although nearly all hemibrain neurons could be matched morphologically in FlyWire, about one-third of cell types proposed for the hemibrain could not be reliably reidentified. We therefore propose a new definition of cell type as groups of cells that are each quantitatively more similar to cells in a different brain than to any other cell in the same brain, and we validate this definition through joint analysis of FlyWire and hemibrain connectomes. Further analysis defined simple heuristics for the reliability of connections between brains, revealed broad stereotypy and occasional variability in neuron count and connectivity, and provided evidence for functional homeostasis in the mushroom body through adjustments of the absolute amount of excitatory input while maintaining the excitation/inhibition ratio. Our work defines a consensus cell type atlas for the fly brain and provides both an intellectual framework and open-source toolchain for brain-scale comparative connectomics.

Date: 2024
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DOI: 10.1038/s41586-024-07686-5

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