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.
Highlights
Rhythmic muscle contractions are required for many aspects of physiology and behavior, from circulation to locomotion[1]
Our results demonstrate that the pharyngeal muscle generates a myogenic rhythm only in the presence of tonically released ACh, and suggest that the MC neurons stimulate pumping by rhythmically exciting and entraining the pharyngeal muscle rhythm in a manner similar to that by which the leech heartbeat is controlled by heart motor neurons
When we stimulated the pharyngeal muscle in worms in which the nervous system was silenced via the histamine-gated chloride channel (HisCl) channel, we found that pharyngeal muscle action potential duration, measured as the time between the E2 and R1 spikes, was dramatically increased (Fig. 2a,c), suggesting that increased pump duration is due to either decreased M3 activity or altered pharyngeal excitability
Summary
Rhythmic muscle contractions are required for many aspects of physiology and behavior, from circulation to locomotion[1] These rhythms can be described as myogenic, if intrinsic oscillations of membrane currents in the muscles drive contractions, or neurogenic, if a network of neurons acts as a central pattern generator (CPG) to drive muscle contraction. The development of optical[14,15] and electrophysiological[16] methods for manipulating and monitoring neural activity has begun to enable analysis of the physiology and functional connectivity of C. elegans neural circuits. Such investigations apply a conceptual approach similar to that developed in leeches, crustaceans, and gastropods while leveraging the extensive genetic toolkit available in worms. C. elegans is well suited to provide insights into mechanisms that underlie rhythmic behaviors
Sign-in/Register to view highlights & summary Sign-in/Register to access full text options 
Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have
Schedule a callDisclaimer: All third-party content on this website/platform is and will remain the property of their respective owners and is provided on "as is" basis without any warranties, express or implied. Use of third-party content does not indicate any affiliation, sponsorship with or endorsement by them. Any references to third-party content is to identify the corresponding services and shall be considered fair use under The CopyrightLaw.
