Synaptic architecture of leg and wing premotor control networks in Drosophila
- Creators
- Lesser, Ellen
- Azevedo, Anthony W.
- Phelps, Jasper S.
- Elabbady, Leila
- Cook, Andrew
- Syed, Durafshan Sakeena
- Mark, Brandon
- Kuroda, Sumiya
- Sustar, Anne
- Moussa, Anthony
- Dallmann, Chris J.
- Agrawal, Sweta
- Lee, Su-Yee J.
- Pratt, Brandon
- Skutt-Kakaria, Kyobi
- Gerhard, Stephan
- Lu, Ran
- Kemnitz, Nico
- Lee, Kisuk
- Halageri, Akhilesh
- Castro, Manuel
- Ih, Dodam
- Gager, Jay
- Tammam, Marwan
- Dorkenwald, Sven
- Collman, Forrest
- Schneider-Mizell, Casey
- Brittain, Derrick
- Jordan, Chris S.
- Macrina, Thomas
- Dickinson, Michael1
- Lee, Wei-Chung Allen
- Tuthill, John C.
Abstract
Animal movement is controlled by motor neurons (MNs), which project out of the central nervous system to activate muscles1. MN activity is coordinated by complex premotor networks that facilitate the contribution of individual muscles to many different behaviours2,3,4,5,6. Here we use connectomics7 to analyse the wiring logic of premotor circuits controlling the Drosophila leg and wing. We find that both premotor networks cluster into modules that link MNs innervating muscles with related functions. Within most leg motor modules, the synaptic weights of each premotor neuron are proportional to the size of their target MNs, establishing a circuit basis for hierarchical MN recruitment. By contrast, wing premotor networks lack proportional synaptic connectivity, which may enable more flexible recruitment of wing steering muscles. Through comparison of the architecture of distinct motor control systems within the same animal, we identify common principles of premotor network organization and specializations that reflect the unique biomechanical constraints and evolutionary origins of leg and wing motor control.
Copyright and License
© The Author(s), under exclusive licence to Springer Nature Limited 2024.
Acknowledgement
This work was supported by a Searle Scholar Award, a Klingenstein-Simons Fellowship, a Pew Biomedical Scholar Award, a McKnight Scholar Award, a Sloan Research Fellowship, the New York Stem Cell Foundation and a UW Innovation Award to J.C.T.; a Genise Goldenson Award to W.-C.A.L.; NIH no. U19NS104655 to J.C.T. and M.D.; 1RF1NS128785-01 to J.C.T.; and NIH no. R01MH117808 to J.C.T. and W.-C.A.L. J.C.T. is a New York Stem Cell Foundation – Robertson Investigator. We thank J. Truman, D. Shepherd and E. Marin for assistance with hemilineage identification. We thank H. Lacin, L. Marin, G. Jefferis amd G. Card for helpful discussions, and for their laboratory’s contributions to proofreading in the FANC dataset, in particular K. Eichler, P. Brooks, T. Stürner, M. Costa and G. Jefferis for sharing comprehensive proofreading and annotation of neck connective neurons including descending and ascending neurons in the FANC dataset (supported by Wellcome award 221300/Z/20/Z). We thank members of the Tuthill and Dickinson Laboratories, S. Ahmed, B. Brunton and J. Truman for comments on the manuscript.
Contributions
These authors contributed equally: Ellen Lesser, Anthony W. Azevedo
E.L., A.W.A., W.-C.A.L. and J.C.T. conceived the project. W.-C.A.L. and J.C.T. acquired funding. R.L., N.K., K.L., A.H., M.C., D.I., J.G., M.T., C.S.J., S.G., S.K. and T.M. developed and deployed the software to support proofreading of segmented electron microscopy data. S.D., F.C., C.S.-M. and D.B. deployed and supported the annotation software CAVE. A.W.A., E.L., J.S.P., B.M., L.E., A.M., D.S.S., C.J.D., S.A., S.-Y.J.L., B.P., A.C. and K.S.-K. proofread neurons in FANC and edited the paper. A.S. designed and performed light-microscopy imaging. J.S.P. organized the community guidelines and efforts to proofread and annotate FANC. M.D. and W.-C.A.L. advised the project and edited the paper. A.W.A., E.L. and L.E. analysed data. A.W.A., E.L. and J.C.T. wrote the paper, with input from all other co-authors.
Data Availability
The data presented in the paper were analysed from CAVE materialization version 840 (v.840). Annotated connectivity matrices (Fig. 2) are available as Python Pandas data frames (https://pandas.pydata.org/) at GitHub (https://github.com/tuthill-lab/Lesser_Azevedo_2023). Links to public preMN and MN segmentations are available throughout the text, as well as in Supplementary Tables 1–3.
Extended Data Fig. 1 Detailed properties of individual leg and wing MNs.
Code Availability
Scripts to recreate the analyses and figures in the paper, as well as scripts to recreate the connectivity matrices, are available at GitHub (https://github.com/tuthill-lab/Lesser_Azevedo_2023) for users authorized to interact with the CAVEclient. All analysis was performed in Python 3.9 using custom code, making extensive use of CAVEclient (https://github.com/seung-lab/CAVEclient)65 and CloudVolume to interact with data infrastructure, and the libraries Matplotlib, Numpy, Pandas, Scikit-learn, Scipy, stats-models and VTK for general computation, machine learning and data visualization. Additional code is available at https://github.com/htem/FANC_auto_recon, providing additional tutorials, documentation for interaction with FANC and instructions for joining the FANC community.
Conflict of Interest
The authors declare no competing interests.
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Additional details
- ISSN
- 1476-4687
- URL
- https://rdcu.be/dL0Y8
- Chicago Community Trust
- Searle Scholar
- Esther A. & Joseph Klingenstein Fund
- Simons Foundation
- McKnight Brain Research Foundation
- Alfred P. Sloan Foundation
- New York Stem Cell Foundation
- University of Washington
- Harvard University
- Genise Goldenson Fund
- National Institutes of Health
- U19NS104655
- National Institutes of Health
- 1RF1NS128785
- National Institutes of Health
- R01MH117808
- Wellcome Trust
- 221300/Z/20/Z
- Caltech groups
- Division of Biology and Biological Engineering, GALCIT, Tianqiao and Chrissy Chen Institute for Neuroscience