Decoding a neural circuit controlling global animal state in C. elegans

Elife. 2015 Mar 11;4:e04241. doi: 10.7554/eLife.04241.

Abstract

Brains organize behavior and physiology to optimize the response to threats or opportunities. We dissect how 21% O2, an indicator of surface exposure, reprograms C. elegans' global state, inducing sustained locomotory arousal and altering expression of neuropeptides, metabolic enzymes, and other non-neural genes. The URX O2-sensing neurons drive arousal at 21% O2 by tonically activating the RMG interneurons. Stimulating RMG is sufficient to switch behavioral state. Ablating the ASH, ADL, or ASK sensory neurons connected to RMG by gap junctions does not disrupt arousal. However, disrupting cation currents in these neurons curtails RMG neurosecretion and arousal. RMG signals high O2 by peptidergic secretion. Neuropeptide reporters reveal neural circuit state, as neurosecretion stimulates neuropeptide expression. Neural imaging in unrestrained animals shows that URX and RMG encode O2 concentration rather than behavior, while the activity of downstream interneurons such as AVB and AIY reflect both O2 levels and the behavior being executed.

Keywords: C. elegans; TRPV; caenorhabditis; gap junctions; neural circuit; neuroscience; optogenetics.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Animals, Genetically Modified
  • Arousal / genetics
  • Behavior, Animal
  • Caenorhabditis elegans / cytology
  • Caenorhabditis elegans / drug effects*
  • Caenorhabditis elegans / genetics
  • Caenorhabditis elegans / metabolism
  • Caenorhabditis elegans Proteins / genetics
  • Caenorhabditis elegans Proteins / metabolism
  • Calcium / metabolism
  • Gap Junctions / drug effects
  • Gap Junctions / metabolism
  • Gene Expression Regulation
  • Interneurons / cytology
  • Interneurons / drug effects*
  • Interneurons / metabolism
  • Ion Transport
  • Locomotion / genetics
  • Nerve Net / drug effects*
  • Nerve Net / metabolism
  • Nerve Tissue Proteins / genetics
  • Nerve Tissue Proteins / metabolism
  • Neuropeptides / genetics
  • Neuropeptides / metabolism
  • Oxygen / pharmacology*
  • Potassium Channels / genetics
  • Potassium Channels / metabolism
  • Receptors, Neuropeptide Y / genetics
  • Receptors, Neuropeptide Y / metabolism
  • Sensory Receptor Cells / cytology
  • Sensory Receptor Cells / drug effects*
  • Sensory Receptor Cells / metabolism
  • Signal Transduction
  • TRPV Cation Channels / genetics
  • TRPV Cation Channels / metabolism

Substances

  • Caenorhabditis elegans Proteins
  • Flp-2 protein, C elegans
  • NPR-1 protein, C elegans
  • Nerve Tissue Proteins
  • Neuropeptides
  • OCR-2 protein, C elegans
  • Potassium Channels
  • Receptors, Neuropeptide Y
  • TRPV Cation Channels
  • Oxygen
  • Calcium