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An Hourglass Circuit Motif Transforms a Motor Program via Subcellularly Localized Muscle Calcium Signaling and Contraction

View ORCID ProfileSteven R. Sando, Nikhil Bhatla, View ORCID ProfileEugene L. Q. Lee, View ORCID ProfileH. Robert Horvitz
doi: https://doi.org/10.1101/2020.06.02.129825
Steven R. Sando
1Howard Hughes Medical Institute, Department of Biology, McGovern Institute for Brain Research, Massachusetts Institute of Technology, Cambridge, MA, 02139, USA
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  • ORCID record for Steven R. Sando
Nikhil Bhatla
1Howard Hughes Medical Institute, Department of Biology, McGovern Institute for Brain Research, Massachusetts Institute of Technology, Cambridge, MA, 02139, USA
2Miller Institute, Helen Wills Neuroscience Institute, Department of Molecular and Cellular Biology, University of California, Berkeley, Berkeley, 94720, USA
3Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, MA, 02139, USA
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Eugene L. Q. Lee
1Howard Hughes Medical Institute, Department of Biology, McGovern Institute for Brain Research, Massachusetts Institute of Technology, Cambridge, MA, 02139, USA
3Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, MA, 02139, USA
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H. Robert Horvitz
1Howard Hughes Medical Institute, Department of Biology, McGovern Institute for Brain Research, Massachusetts Institute of Technology, Cambridge, MA, 02139, USA
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  • For correspondence: horvitz@mit.edu
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Abstract

Neural control of muscle function is fundamental to animal behavior. Many muscles can generate multiple distinct behaviors. Nonetheless, individual muscle cells are generally regarded as the smallest units of motor control. We report that muscle cells can alter behavior by contracting subcellularly. We previously discovered that noxious tastes reverse the net flow of particles through the C. elegans pharynx, a neuromuscular pump, resulting in spitting. We now show that spitting results from the subcellular contraction of the anterior region of the pm3 muscle cell. Subcellularly localized calcium increases accompany this contraction. Spitting is controlled by an “hourglass” circuit motif: parallel neural pathways converge onto a single motor neuron that differentially controls multiple muscles and the critical subcellular muscle compartment. We conclude that subcellular muscle units enable modulatory motor control and propose that subcellular muscle contraction is a fundamental mechanism by which neurons can reshape behavior.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • This version of the manuscript has been revised in response to comments from our eLife reviewers given on July 6th 2020 (eLife review letter viewable at https://tinyurl.com/y49zqeho).

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted June 09, 2021.
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An Hourglass Circuit Motif Transforms a Motor Program via Subcellularly Localized Muscle Calcium Signaling and Contraction
Steven R. Sando, Nikhil Bhatla, Eugene L. Q. Lee, H. Robert Horvitz
bioRxiv 2020.06.02.129825; doi: https://doi.org/10.1101/2020.06.02.129825
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An Hourglass Circuit Motif Transforms a Motor Program via Subcellularly Localized Muscle Calcium Signaling and Contraction
Steven R. Sando, Nikhil Bhatla, Eugene L. Q. Lee, H. Robert Horvitz
bioRxiv 2020.06.02.129825; doi: https://doi.org/10.1101/2020.06.02.129825

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