A circuit mechanism for the propagation of waves of muscle contraction in Drosophila

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Abstract

Animals move by adaptively coordinating the sequential activation of muscles. The circuit mechanisms underlying coordinated locomotion are poorly understood. Here, we report on a novel circuit for propagation of waves of muscle contraction, using the peristaltic locomotion of Drosophila larvae as a model system. We found an intersegmental chain of synaptically connected neurons, alternating excitatory and inhibitory, necessary for wave propagation and active in phase with the wave. The excitatory neurons (A27h) are premotor and necessary only for forward locomotion, and are modulated by stretch receptors and descending inputs. The inhibitory neurons (GDL) are necessary for both forward and backward locomotion, suggestive of different yet coupled central pattern generators, and its inhibition is necessary for wave propagation. The circuit structure and functional imaging indicated that the commands to contract one segment promote the relaxation of the next segment, revealing a mechanism for wave propagation in peristaltic locomotion.

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Akira Fushiki

Department of Complexity Science and Engineering, Graduate School of Frontier Sciences, University of Tokyo, Tokyo, Japan

Competing interests
The authors declare that no competing interests exist.
Maarten F Zwart

Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States

Competing interests
The authors declare that no competing interests exist.
Hiroshi Kohsaka

Department of Complexity Science and Engineering, University of Tokyo, Kashiwa, Chiba, Japan

Competing interests
The authors declare that no competing interests exist.
Richard D Fetter

Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States

Competing interests
The authors declare that no competing interests exist.
Albert Cardona

Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States

Competing interests
The authors declare that no competing interests exist.
Akinao Nose

Department of Complexity Science and Engineering, Graduate School of Frontier Sciences, University of Tokyo, Tokyo, Japan

For correspondence
nose@k.u-tokyo.ac.jp

Competing interests
The authors declare that no competing interests exist.

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