Neural and genetic degeneracy underlies Caenorhabditis elegans feeding behavior

Nicholas F. Trojanowski, Olivia Padovan-Merhar, David M. Raizen, Christopher Fang-Yen

Research output: Contribution to journalArticle

23 Citations (Scopus)

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.

Original languageEnglish
Pages (from-to)951-961
Number of pages11
JournalJournal of Neurophysiology
Volume112
Issue number4
DOIs
Publication statusPublished - 2014 Aug 15

Fingerprint

Optogenetics
Caenorhabditis elegans
Nicotinic Receptors
Muscarinic Receptors
Feeding Behavior
Pharynx
Neurons
Inhibition (Psychology)

ASJC Scopus subject areas

  • Physiology
  • Neuroscience(all)

Cite this

Trojanowski, N. F., Padovan-Merhar, O., Raizen, D. M., & Fang-Yen, C. (2014). Neural and genetic degeneracy underlies Caenorhabditis elegans feeding behavior. Journal of Neurophysiology, 112(4), 951-961. https://doi.org/10.1152/jn.00150.2014

Neural and genetic degeneracy underlies Caenorhabditis elegans feeding behavior. / Trojanowski, Nicholas F.; Padovan-Merhar, Olivia; Raizen, David M.; Fang-Yen, Christopher.

In: Journal of Neurophysiology, Vol. 112, No. 4, 15.08.2014, p. 951-961.

Research output: Contribution to journalArticle

Trojanowski, NF, Padovan-Merhar, O, Raizen, DM & Fang-Yen, C 2014, 'Neural and genetic degeneracy underlies Caenorhabditis elegans feeding behavior', Journal of Neurophysiology, vol. 112, no. 4, pp. 951-961. https://doi.org/10.1152/jn.00150.2014
Trojanowski, Nicholas F. ; Padovan-Merhar, Olivia ; Raizen, David M. ; Fang-Yen, Christopher. / Neural and genetic degeneracy underlies Caenorhabditis elegans feeding behavior. In: Journal of Neurophysiology. 2014 ; Vol. 112, No. 4. pp. 951-961.
@article{b7a66a08c16840c89b8fb3c515e76628,
title = "Neural and genetic degeneracy underlies Caenorhabditis elegans feeding behavior",
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",
author = "Trojanowski, {Nicholas F.} and Olivia Padovan-Merhar and Raizen, {David M.} and Christopher Fang-Yen",
year = "2014",
month = "8",
day = "15",
doi = "10.1152/jn.00150.2014",
language = "English",
volume = "112",
pages = "951--961",
journal = "Journal of Neurophysiology",
issn = "0022-3077",
publisher = "American Physiological Society",
number = "4",

}

TY - JOUR

T1 - Neural and genetic degeneracy underlies Caenorhabditis elegans feeding behavior

AU - Trojanowski, Nicholas F.

AU - Padovan-Merhar, Olivia

AU - Raizen, David M.

AU - Fang-Yen, Christopher

PY - 2014/8/15

Y1 - 2014/8/15

N2 - 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.

AB - 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.

KW - Behavior

KW - Feeding

KW - Neural circuits

KW - Optogenetics

UR - http://www.scopus.com/inward/record.url?scp=84906091844&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84906091844&partnerID=8YFLogxK

U2 - 10.1152/jn.00150.2014

DO - 10.1152/jn.00150.2014

M3 - Article

C2 - 24872529

AN - SCOPUS:84906091844

VL - 112

SP - 951

EP - 961

JO - Journal of Neurophysiology

JF - Journal of Neurophysiology

SN - 0022-3077

IS - 4

ER -