Journal Article

Synaptic architecture of leg and wing premotor control networks in Drosophila

Azevedo, Anthony W., Jordan, Chris S., Elabbady, Leila, Pratt, Brandon, Tuthill, John C., Lee, Kisuk, Gager, Jay, Syed, Durafshan Sakeena, Cook, Andrew, Kemnitz, Nico, Castro, Manuel, Phelps, Jasper S., Mark, Brandon, Dallmann, Chris J., Kuroda, Sumiya, Halageri, Akhilesh, Schneider-Mizell, Casey, Tammam, Marwan, Brittain, Derrick, Sustar, Anne, Skutt-Kakaria, Kyobi, Lee, Wei-Chung Allen, Macrina, Thomas, Gerhard, Stephan, Dorkenwald, Sven, Ih, Dodam, Moussa, Anthony, Lesser, Ellen, Lee, Su-Yee J., Lu, Ran, Dickinson, Michael, Agrawal, Sweta, Collman, Forrest

2024

Overview

Animal movement is controlled by motor neurons (MNs), which project out of the central nervous system to activate muscles 1 . MN activity is coordinated by complex premotor networks that facilitate the contribution of individual muscles to many different behaviours 2 – 6 . Here we use connectomics 7 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. We use connectomics to compare the wiring logic of premotor circuits controlling the Drosophila leg and wing, finding that both premotor networks cluster into modules that link motor neurons innervating muscles with related functions.

• Publisher: Nature Publishing Group UK,Nature Publishing Group
• Subject: 14 / 14/28 / 631/378/2632/1823 / 631/378/3920 / Animals / Biomechanical engineering / Biomechanics / Car pools / Central nervous system / Connectome / Control systems / Drosophila / Drosophila melanogaster - anatomy & histology / Drosophila melanogaster - cytology / Drosophila melanogaster - physiology / Extremities - innervation / Extremities - physiology / Female / Fruit flies / Humanities and Social Sciences / Insects / Leg / Male / Microscopy / Modules / Motor neurons / Motor Neurons - physiology / Motor task performance / Movement - physiology / multidisciplinary / Muscles / Muscles - innervation / Muscles - physiology / Nerve Net - anatomy & histology / Nerve Net - cytology / Nerve Net - physiology / Networks / Neural networks / Neural Pathways - anatomy & histology / Neural Pathways - cytology / Neural Pathways - physiology / Neurons / Recruitment / Science / Science (multidisciplinary) / Steering / Synapses - physiology / Synaptic strength / Thorax / Wings / Wings, Animal - innervation / Wings, Animal - physiology