An hourglass circuit motif transforms a motor program via subcellularly localized muscle calcium signaling and contraction

Elife. 2021 Jul 2;10:e59341. doi: 10.7554/eLife.59341.

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.

Keywords: C. elegans; behavior; hourglass circuit motif; motor control; neural circuitry; neuroscience; subcellular muscle contraction; subcellularly localized calcium transients.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Biochemical Phenomena
  • Caenorhabditis elegans
  • Calcium / metabolism
  • Calcium Signaling / physiology*
  • Light
  • Motor Neurons / physiology
  • Muscle Cells / physiology*
  • Muscle Contraction / physiology*
  • Neural Pathways
  • Pharynx

Substances

  • Calcium

Associated data

  • figshare/10.6084/m9.figshare.c.5521161.v1