Pharyngeal pumping in Caenorhabditis elegans depends on tonic and phasic signaling from the nervous system

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

Research output: Contribution to journalArticle

20 Citations (Scopus)

Abstract

Rhythmic movements are ubiquitous in animal locomotion, feeding, and circulatory systems. In some systems, the muscle itself generates rhythmic contractions. In others, rhythms are generated by the nervous system or by interactions between the nervous system and muscles. In the nematode Caenorhabditis elegans, feeding occurs via rhythmic contractions (pumping) of the pharynx, a neuromuscular feeding organ. Here, we use pharmacology, optogenetics, genetics, and electrophysiology to investigate the roles of the nervous system and muscle in generating pharyngeal pumping. Hyperpolarization of the nervous system using a histamine-gated chloride channel abolishes pumping, and optogenetic stimulation of pharyngeal muscle in these animals causes abnormal contractions, demonstrating that normal pumping requires nervous system function. In mutants that pump slowly due to defective nervous system function, tonic muscle stimulation causes rapid pumping, suggesting tonic neurotransmitter release may regulate pumping. However, tonic cholinergic motor neuron stimulation, but not tonic muscle stimulation, triggers pumps that electrophysiologically resemble typical rapid pumps. This suggests that pharyngeal cholinergic motor neurons are normally rhythmically, and not tonically active. These results demonstrate that the pharynx generates a myogenic rhythm in the presence of tonically released acetylcholine, and suggest that the pharyngeal nervous system entrains contraction rate and timing through phasic neurotransmitter release.

Original languageEnglish
Article number22940
JournalScientific Reports
Volume6
DOIs
Publication statusPublished - 2016 Mar 15
Externally publishedYes

Fingerprint

Caenorhabditis elegans
Nervous System
Muscles
Optogenetics
Cholinergic Neurons
Motor Neurons
Pharynx
Neurotransmitter Agents
Pharyngeal Muscles
Chloride Channels
Electrophysiology
Locomotion
Cardiovascular System
Histamine
Acetylcholine
Pharmacology

ASJC Scopus subject areas

  • General

Cite this

Pharyngeal pumping in Caenorhabditis elegans depends on tonic and phasic signaling from the nervous system. / Trojanowski, Nicholas F.; Raizen, David M.; Fang-Yen, Christopher.

In: Scientific Reports, Vol. 6, 22940, 15.03.2016.

Research output: Contribution to journalArticle

Trojanowski, Nicholas F. ; Raizen, David M. ; Fang-Yen, Christopher. / Pharyngeal pumping in Caenorhabditis elegans depends on tonic and phasic signaling from the nervous system. In: Scientific Reports. 2016 ; Vol. 6.
@article{26a68a73dd104255a459e34a828ed5ed,
title = "Pharyngeal pumping in Caenorhabditis elegans depends on tonic and phasic signaling from the nervous system",
abstract = "Rhythmic movements are ubiquitous in animal locomotion, feeding, and circulatory systems. In some systems, the muscle itself generates rhythmic contractions. In others, rhythms are generated by the nervous system or by interactions between the nervous system and muscles. In the nematode Caenorhabditis elegans, feeding occurs via rhythmic contractions (pumping) of the pharynx, a neuromuscular feeding organ. Here, we use pharmacology, optogenetics, genetics, and electrophysiology to investigate the roles of the nervous system and muscle in generating pharyngeal pumping. Hyperpolarization of the nervous system using a histamine-gated chloride channel abolishes pumping, and optogenetic stimulation of pharyngeal muscle in these animals causes abnormal contractions, demonstrating that normal pumping requires nervous system function. In mutants that pump slowly due to defective nervous system function, tonic muscle stimulation causes rapid pumping, suggesting tonic neurotransmitter release may regulate pumping. However, tonic cholinergic motor neuron stimulation, but not tonic muscle stimulation, triggers pumps that electrophysiologically resemble typical rapid pumps. This suggests that pharyngeal cholinergic motor neurons are normally rhythmically, and not tonically active. These results demonstrate that the pharynx generates a myogenic rhythm in the presence of tonically released acetylcholine, and suggest that the pharyngeal nervous system entrains contraction rate and timing through phasic neurotransmitter release.",
author = "Trojanowski, {Nicholas F.} and Raizen, {David M.} and Christopher Fang-Yen",
year = "2016",
month = "3",
day = "15",
doi = "10.1038/srep22940",
language = "English",
volume = "6",
journal = "Scientific Reports",
issn = "2045-2322",
publisher = "Nature Publishing Group",

}

TY - JOUR

T1 - Pharyngeal pumping in Caenorhabditis elegans depends on tonic and phasic signaling from the nervous system

AU - Trojanowski, Nicholas F.

AU - Raizen, David M.

AU - Fang-Yen, Christopher

PY - 2016/3/15

Y1 - 2016/3/15

N2 - Rhythmic movements are ubiquitous in animal locomotion, feeding, and circulatory systems. In some systems, the muscle itself generates rhythmic contractions. In others, rhythms are generated by the nervous system or by interactions between the nervous system and muscles. In the nematode Caenorhabditis elegans, feeding occurs via rhythmic contractions (pumping) of the pharynx, a neuromuscular feeding organ. Here, we use pharmacology, optogenetics, genetics, and electrophysiology to investigate the roles of the nervous system and muscle in generating pharyngeal pumping. Hyperpolarization of the nervous system using a histamine-gated chloride channel abolishes pumping, and optogenetic stimulation of pharyngeal muscle in these animals causes abnormal contractions, demonstrating that normal pumping requires nervous system function. In mutants that pump slowly due to defective nervous system function, tonic muscle stimulation causes rapid pumping, suggesting tonic neurotransmitter release may regulate pumping. However, tonic cholinergic motor neuron stimulation, but not tonic muscle stimulation, triggers pumps that electrophysiologically resemble typical rapid pumps. This suggests that pharyngeal cholinergic motor neurons are normally rhythmically, and not tonically active. These results demonstrate that the pharynx generates a myogenic rhythm in the presence of tonically released acetylcholine, and suggest that the pharyngeal nervous system entrains contraction rate and timing through phasic neurotransmitter release.

AB - Rhythmic movements are ubiquitous in animal locomotion, feeding, and circulatory systems. In some systems, the muscle itself generates rhythmic contractions. In others, rhythms are generated by the nervous system or by interactions between the nervous system and muscles. In the nematode Caenorhabditis elegans, feeding occurs via rhythmic contractions (pumping) of the pharynx, a neuromuscular feeding organ. Here, we use pharmacology, optogenetics, genetics, and electrophysiology to investigate the roles of the nervous system and muscle in generating pharyngeal pumping. Hyperpolarization of the nervous system using a histamine-gated chloride channel abolishes pumping, and optogenetic stimulation of pharyngeal muscle in these animals causes abnormal contractions, demonstrating that normal pumping requires nervous system function. In mutants that pump slowly due to defective nervous system function, tonic muscle stimulation causes rapid pumping, suggesting tonic neurotransmitter release may regulate pumping. However, tonic cholinergic motor neuron stimulation, but not tonic muscle stimulation, triggers pumps that electrophysiologically resemble typical rapid pumps. This suggests that pharyngeal cholinergic motor neurons are normally rhythmically, and not tonically active. These results demonstrate that the pharynx generates a myogenic rhythm in the presence of tonically released acetylcholine, and suggest that the pharyngeal nervous system entrains contraction rate and timing through phasic neurotransmitter release.

UR - http://www.scopus.com/inward/record.url?scp=84961123903&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84961123903&partnerID=8YFLogxK

U2 - 10.1038/srep22940

DO - 10.1038/srep22940

M3 - Article

C2 - 26976078

AN - SCOPUS:84961123903

VL - 6

JO - Scientific Reports

JF - Scientific Reports

SN - 2045-2322

M1 - 22940

ER -