Literature DB >> 24872529

Neural and genetic degeneracy underlies Caenorhabditis elegans feeding behavior.

Nicholas F Trojanowski1, Olivia Padovan-Merhar2, David M Raizen3, Christopher Fang-Yen4.   

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.
Copyright © 2014 the American Physiological Society.

Entities:  

Keywords:  behavior; feeding; neural circuits; optogenetics

Mesh:

Substances:

Year:  2014        PMID: 24872529      PMCID: PMC4122747          DOI: 10.1152/jn.00150.2014

Source DB:  PubMed          Journal:  J Neurophysiol        ISSN: 0022-3077            Impact factor:   2.974


  71 in total

1.  Measures of degeneracy and redundancy in biological networks.

Authors:  G Tononi; O Sporns; G M Edelman
Journal:  Proc Natl Acad Sci U S A       Date:  1999-03-16       Impact factor: 11.205

2.  Multiple models to capture the variability in biological neurons and networks.

Authors:  Eve Marder; Adam L Taylor
Journal:  Nat Neurosci       Date:  2011-02       Impact factor: 24.884

3.  The dauerlarva, a post-embryonic developmental variant of the nematode Caenorhabditis elegans.

Authors:  R C Cassada; R L Russell
Journal:  Dev Biol       Date:  1975-10       Impact factor: 3.582

4.  Cloning and functional characterization of a Caenorhabditis elegans muscarinic acetylcholine receptor.

Authors:  J M Hwang; D J Chang; U S Kim; Y S Lee; Y S Park; B K Kaang; N J Cho
Journal:  Receptors Channels       Date:  1999

5.  Light activation of channelrhodopsin-2 in excitable cells of Caenorhabditis elegans triggers rapid behavioral responses.

Authors:  Georg Nagel; Martin Brauner; Jana F Liewald; Nona Adeishvili; Ernst Bamberg; Alexander Gottschalk
Journal:  Curr Biol       Date:  2005-12-20       Impact factor: 10.834

Review 6.  C. elegans feeding.

Authors:  Leon Avery; Young-Jai You
Journal:  WormBook       Date:  2012-05-21

7.  A cell that dies during wild-type C. elegans development can function as a neuron in a ced-3 mutant.

Authors:  L Avery; H R Horvitz
Journal:  Cell       Date:  1987-12-24       Impact factor: 41.582

8.  The genetics of feeding in Caenorhabditis elegans.

Authors:  L Avery
Journal:  Genetics       Date:  1993-04       Impact factor: 4.562

9.  The C. elegans T-type calcium channel CCA-1 boosts neuromuscular transmission.

Authors:  Katherine A Steger; Boris B Shtonda; Colin Thacker; Terrance P Snutch; Leon Avery
Journal:  J Exp Biol       Date:  2005-06       Impact factor: 3.312

10.  Microbial light-activatable proton pumps as neuronal inhibitors to functionally dissect neuronal networks in C. elegans.

Authors:  Steven J Husson; Jana F Liewald; Christian Schultheis; Jeffrey N Stirman; Hang Lu; Alexander Gottschalk
Journal:  PLoS One       Date:  2012-07-16       Impact factor: 3.240

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  26 in total

1.  Stochastic feeding dynamics arise from the need for information and energy.

Authors:  Monika Scholz; Aaron R Dinner; Erel Levine; David Biron
Journal:  Proc Natl Acad Sci U S A       Date:  2017-08-11       Impact factor: 11.205

Review 2.  Micro-connectomics: probing the organization of neuronal networks at the cellular scale.

Authors:  Manuel Schröter; Ole Paulsen; Edward T Bullmore
Journal:  Nat Rev Neurosci       Date:  2017-02-02       Impact factor: 34.870

3.  Distinct Mechanisms Underlie Quiescence during Two Caenorhabditis elegans Sleep-Like States.

Authors:  Nicholas F Trojanowski; Matthew D Nelson; Steven W Flavell; Christopher Fang-Yen; David M Raizen
Journal:  J Neurosci       Date:  2015-10-28       Impact factor: 6.167

Review 4.  Consequences of degeneracy in network function.

Authors:  Elizabeth C Cropper; Andrew M Dacks; Klaudiusz R Weiss
Journal:  Curr Opin Neurobiol       Date:  2016-08-31       Impact factor: 6.627

5.  Network Degeneracy and the Dynamics of Task Switching in the Feeding Circuit in Aplysia.

Authors:  Yanqing Wang; Klaudiusz R Weiss; Elizabeth C Cropper
Journal:  J Neurosci       Date:  2019-09-23       Impact factor: 6.167

6.  Modular Organization of Cis-regulatory Control Information of Neurotransmitter Pathway Genes in Caenorhabditis elegans.

Authors:  Esther Serrano-Saiz; Burcu Gulez; Laura Pereira; Marie Gendrel; Sze Yen Kerk; Berta Vidal; Weidong Feng; Chen Wang; Paschalis Kratsios; James B Rand; Oliver Hobert
Journal:  Genetics       Date:  2020-05-22       Impact factor: 4.562

7.  Simultaneous Optogenetic Stimulation of Individual Pharyngeal Neurons and Monitoring of Feeding Behavior in Intact C. elegans.

Authors:  Nicholas F Trojanowski; Christopher Fang-Yen
Journal:  Methods Mol Biol       Date:  2015

Review 8.  Call it Worm Sleep.

Authors:  Nicholas F Trojanowski; David M Raizen
Journal:  Trends Neurosci       Date:  2015-12-30       Impact factor: 13.837

9.  Distinct Neural Circuits Control Rhythm Inhibition and Spitting by the Myogenic Pharynx of C. elegans.

Authors:  Nikhil Bhatla; Rita Droste; Steven R Sando; Anne Huang; H Robert Horvitz
Journal:  Curr Biol       Date:  2015-07-23       Impact factor: 10.834

Review 10.  Illuminating neural circuits and behaviour in Caenorhabditis elegans with optogenetics.

Authors:  Christopher Fang-Yen; Mark J Alkema; Aravinthan D T Samuel
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2015-09-19       Impact factor: 6.237

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