Regulation of forward and backward locomotion through intersegmental feedback circuits in Drosophila larvae

Hiroshi Kohsaka (), Maarten F. Zwart, Akira Fushiki, Richard D. Fetter, James W. Truman, Albert Cardona and Akinao Nose ()
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Hiroshi Kohsaka: the University of Tokyo
Maarten F. Zwart: HHMI Janelia Research Campus
Akira Fushiki: HHMI Janelia Research Campus
Richard D. Fetter: HHMI Janelia Research Campus
James W. Truman: HHMI Janelia Research Campus
Albert Cardona: HHMI Janelia Research Campus
Akinao Nose: the University of Tokyo

Nature Communications, 2019, vol. 10, issue 1, 1-11

Abstract: Abstract Animal locomotion requires spatiotemporally coordinated contraction of muscles throughout the body. Here, we investigate how contractions of antagonistic groups of muscles are intersegmentally coordinated during bidirectional crawling of Drosophila larvae. We identify two pairs of higher-order premotor excitatory interneurons present in each abdominal neuromere that intersegmentally provide feedback to the adjacent neuromere during motor propagation. The two feedback neuron pairs are differentially active during either forward or backward locomotion but commonly target a group of premotor interneurons that together provide excitatory inputs to transverse muscles and inhibitory inputs to the antagonistic longitudinal muscles. Inhibition of either feedback neuron pair compromises contraction of transverse muscles in a direction-specific manner. Our results suggest that the intersegmental feedback neurons coordinate contraction of synergistic muscles by acting as delay circuits representing the phase lag between segments. The identified circuit architecture also shows how bidirectional motor networks could be economically embedded in the nervous system.

Date: 2019
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DOI: 10.1038/s41467-019-10695-y

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