Synaptic architecture of leg and wing motor control networks inDrosophila

Author:

Lesser EllenORCID,Azevedo Anthony W.ORCID,Phelps Jasper S.ORCID,Elabbady LeilaORCID,Cook AndrewORCID,Mark BrandonORCID,Kuroda SumiyaORCID,Sustar AnneORCID,Moussa AnthonyORCID,Dallmann Chris J.ORCID,Agrawal SwetaORCID,Lee Su-Yee J.,Pratt BrandonORCID,Skutt-Kakaria Kyobi,Gerhard StephanORCID,Lu RanORCID,Kemnitz NicoORCID,Lee Kisuk,Halageri AkhileshORCID,Castro Manuel,Ih DodamORCID,Gager Jay,Tammam MarwanORCID,Dorkenwald Sven,Collman ForrestORCID,Schneider-Mizell CaseyORCID,Brittain Derrick,Jordan Chris S.,Seung H. SebastianORCID,Macrina ThomasORCID,Dickinson Michael,Lee Wei-Chung AllenORCID,Tuthill John C.ORCID

Abstract

AbstractAnimal movement is controlled by motor neurons (MNs), which project out of the central nervous system to activate muscles. Because individual muscles may be used in many different behaviors, MN activity must be flexibly coordinated by dedicated premotor circuitry, the organization of which remains largely unknown. Here, we use comprehensive reconstruction of neuron anatomy and synaptic connectivity from volumetric electron microscopy (i.e., connectomics) to analyze the wiring logic of motor circuits controlling theDrosophilaleg and wing. We find that both leg and wing premotor networks are organized into modules that link MNs innervating muscles with related functions. However, the connectivity patterns within leg and wing motor modules are distinct. Leg premotor neurons exhibit proportional gradients of synaptic input onto MNs within each module, revealing a novel circuit basis for hierarchical MN recruitment. In comparison, wing premotor neurons lack proportional synaptic connectivity, which may allow muscles to be recruited in different combinations or with different relative timing. By comparing the architecture of distinct limb 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.

Publisher

Cold Spring Harbor Laboratory

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