An hourglass circuit motif transforms a motor program via subcellularly localized muscle calcium signaling and contraction
- Massachusetts Institute of Technology, United States
- Miller Institute, Helen Wills Neuroscience Institute, University of California, Berkeley, United States
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.
Data availability
All numerical data and analyses generated during this study are included in the manuscript and supporting files. Each figure and figure supplement is accompanied by a source data file that includes all numerical data used to generate that figure. This includes all excel files, all matlab data files and figures, all statistical analyses, and the .svg (scalable vector graphic) file used to generate each figure.All custom Matlab scripts used in data analysis and the sequences of all plasmids generated in this study are also included in separate source data files.In addition, all raw imaging data (i.e., confocal micrographs, calcium imaging videos, and all high-speed behavioral videos) are available for download on FigShare (doi: 10.6084/m9.figshare.c.5485554).
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Sando et al eLife (2021) - source dataFigShare, doi:10.6084/m9.figshare.c.5485554.
Article and author information
Author details
Funding
National Institutes of Health (T32GM007287)
- Steven R Sando
National Institutes of Health (GM024663)
- Steven R Sando
- Nikhil Bhatla
- H Robert Horvitz
McGovern Institute (Friends of the McGovern Institute Fellowship)
- Steven R Sando
- Eugene L Q Lee
Lord Foundation (Lord Foundation Fellowship)
- Steven R Sando
National Science Foundation (Graduate Research Fellowship)
- Nikhil Bhatla
Agency for Science, Technology and Research (National Science Scholarship)
- Eugene L Q Lee
Howard Hughes Medical Institute
- H Robert Horvitz
Miller Institute (Miller Institute Research Fellowship)
- Nikhil Bhatla
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Copyright
© 2021, Sando et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Further reading
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- Neuroscience
- Physics of Living Systems
Neurons generate and propagate electrical pulses called action potentials which annihilate on arrival at the axon terminal. We measure the extracellular electric field generated by propagating and annihilating action potentials and find that on annihilation, action potentials expel a local discharge. The discharge at the axon terminal generates an inhomogeneous electric field that immediately influences target neurons and thus provokes ephaptic coupling. Our measurements are quantitatively verified by a powerful analytical model which reveals excitation and inhibition in target neurons, depending on position and morphology of the source-target arrangement. Our model is in full agreement with experimental findings on ephaptic coupling at the well-studied Basket cell-Purkinje cell synapse. It is able to predict ephaptic coupling for any other synaptic geometry as illustrated by a few examples.
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