Synaptic architecture of leg and wing premotor control networks in Drosophila

Ellen Lesser, Anthony W. Azevedo, Jasper S. Phelps, Leila Elabbady, Andrew Cook, Durafshan Sakeena Syed, Brandon Mark, Sumiya Kuroda, Anne Sustar, Anthony Moussa, Chris J. Dallmann, Sweta Agrawal, Su-Yee J. Lee, Brandon Pratt, Kyobi Skutt-Kakaria, Stephan Gerhard, Ran Lu, Nico Kemnitz, Kisuk Lee, Akhilesh Halageri, Manuel Castro, Dodam Ih, Jay Gager, Marwan Tammam, Sven Dorkenwald, Forrest Collman, Casey Schneider-Mizell, Derrick Brittain, Chris S. Jordan, Thomas Macrina, Michael Dickinson, Wei-Chung Allen Lee () and John C. Tuthill ()
Additional contact information
Ellen Lesser: University of Washington
Anthony W. Azevedo: University of Washington
Jasper S. Phelps: Harvard Medical School
Leila Elabbady: University of Washington
Andrew Cook: University of Washington
Durafshan Sakeena Syed: University of California
Brandon Mark: University of Washington
Sumiya Kuroda: Harvard Medical School
Anne Sustar: University of Washington
Anthony Moussa: University of Washington
Chris J. Dallmann: University of Washington
Sweta Agrawal: University of Washington
Su-Yee J. Lee: University of Washington
Brandon Pratt: University of Washington
Kyobi Skutt-Kakaria: California Institute of Technology
Stephan Gerhard: Harvard Medical School
Ran Lu: LLC
Nico Kemnitz: LLC
Kisuk Lee: LLC
Akhilesh Halageri: LLC
Manuel Castro: LLC
Dodam Ih: LLC
Jay Gager: LLC
Marwan Tammam: LLC
Sven Dorkenwald: Princeton University
Forrest Collman: Allen Institute for Brain Science
Casey Schneider-Mizell: Allen Institute for Brain Science
Derrick Brittain: Allen Institute for Brain Science
Chris S. Jordan: Princeton University
Thomas Macrina: LLC
Michael Dickinson: California Institute of Technology
Wei-Chung Allen Lee: Harvard Medical School
John C. Tuthill: University of Washington

Nature, 2024, vol. 631, issue 8020, 369-377

Abstract: 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 behaviours2–6. 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.

Date: 2024
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DOI: 10.1038/s41586-024-07600-z

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