Neural and genetic degeneracy underlies Caenorhabditis elegans feeding behavior

J Neurophysiol. 2014 Aug 15;112(4):951-61. doi: 10.1152/jn.00150.2014. Epub 2014 May 28.

Abstract

Degenerate networks, in which structurally distinct elements can perform the same function or yield the same output, are ubiquitous in biology. Degeneracy contributes to the robustness and adaptability of networks in varied environmental and evolutionary contexts. However, how degenerate neural networks regulate behavior in vivo is poorly understood, especially at the genetic level. Here, we identify degenerate neural and genetic mechanisms that underlie excitation of the pharynx (feeding organ) in the nematode Caenorhabditis elegans using cell-specific optogenetic excitation and inhibition. We show that the pharyngeal neurons MC, M2, M4, and I1 form multiple direct and indirect excitatory pathways in a robust network for control of pharyngeal pumping. I1 excites pumping via MC and M2 in a state-dependent manner. We identify nicotinic and muscarinic receptors through which the pharyngeal network regulates feeding rate. These results identify two different mechanisms by which degeneracy is manifest in a neural circuit in vivo.

Keywords: behavior; feeding; neural circuits; optogenetics.

Publication types

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

MeSH terms

  • Animals
  • Caenorhabditis elegans / genetics
  • Caenorhabditis elegans / metabolism
  • Caenorhabditis elegans / physiology*
  • Feeding Behavior*
  • Ganglia, Invertebrate / cytology
  • Ganglia, Invertebrate / physiology
  • Nerve Net / cytology*
  • Nerve Net / physiology
  • Neurons / metabolism
  • Neurons / physiology*
  • Optogenetics
  • Pharynx / innervation
  • Pharynx / physiology
  • Receptors, Muscarinic / metabolism
  • Receptors, Nicotinic / metabolism

Substances

  • Receptors, Muscarinic
  • Receptors, Nicotinic