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

Patrick Laurent1, Zoltan Soltesz1, Geoffrey M Nelson2

  • 1Laboratory of Molecular Biology, Cambridge, United Kingdom.

Elife
|March 12, 2015
PubMed
Summary

High oxygen levels reprogram C. elegans behavior by activating specific oxygen-sensing neurons (URX) that signal through interneurons (RMG) to induce arousal and alter gene expression.

Keywords:
C. elegansTRPVcaenorhabditisgap junctionsneural circuitneuroscienceoptogenetics

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Area of Science:

  • Neuroscience
  • Animal Behavior
  • Molecular Biology

Background:

  • Organisms adapt behavior and physiology to environmental cues like oxygen levels.
  • C. elegans' response to oxygen (O2) involves changes in locomotion and gene expression.

Purpose of the Study:

  • To investigate how high oxygen (21% O2) reprograms the global state of C. elegans.
  • To identify the neural circuits and molecular mechanisms underlying oxygen-induced behavioral changes.

Main Methods:

  • Neural circuit analysis in C. elegans, including ablation and stimulation of specific neurons (URX, RMG, ASH, ADL, ASK).
  • Monitoring of cation currents and neurosecretion.
  • Neuropeptide reporter assays to track neural circuit states.
  • In vivo neural imaging in unrestrained animals to correlate neural activity with O2 levels and behavior.

Main Results:

  • 21% O2 induces sustained locomotory arousal and alters expression of neuropeptides and metabolic genes.
  • URX oxygen-sensing neurons tonically activate RMG interneurons, driving arousal.
  • RMG signals high O2 via peptidergic secretion, influencing neuropeptide expression.
  • Neural imaging reveals URX and RMG encode O2 concentration, while downstream neurons (AVB, AIY) reflect both O2 and behavior.

Conclusions:

  • The URX-RMG neural circuit is critical for mediating behavioral and physiological responses to high oxygen levels in C. elegans.
  • Oxygen concentration, not behavior, is directly encoded by URX and RMG neurons.
  • This study elucidates a fundamental mechanism of environmental sensing and behavioral adaptation.