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.

p‐Coumaric acid improves oxidative and osmosis stress responses in Caenorhabditis elegans

“…Although it is well established that decreased food intake can increase the lifespan of C. elegans , there is no report of a small increase in food intake shortening longevity. It is not clear how p ‐coumaric acid increased pumping rate in the current study; however, based on previous reports that pumping behavior is regulated by the nervous system, we speculate that alteration of pumping rate by p ‐coumaric suggests a potential role of p ‐coumaric acid in the nervous system . Alternatively, the pumping rate is used as an age‐related behavioral marker in C. elegans , as it significantly declines with aging .…”

“…It is not clear how p-coumaric acid increased pumping rate in the current study; however, based on previous reports that pumping behavior is regulated by the nervous system, we speculate that alteration of pumping rate by p-coumaric suggests a potential role of p-coumaric acid in the nervous system. 39 Alternatively, the pumping rate is used as an age-related behavioral marker in C. elegans, as it significantly declines with aging. 40 Even though we did not observe the significant influence of p-coumaric acid on aging in the current study, it is possible that the improvement of oxidative stress by p-coumaric acid may have prevented the decline in the pumping rate in these worms.…”

Consequences of degeneracy in network function

“…C. elegans feed on bacteria via rhythmic contractions and relaxations of the pharynx (i.e., pharyngeal pumping) [29]. The pharynx is innervated by a well-mapped nervous system that can be optogenetically manipulated during behavior [30].…”

Microfluidic platform for electrophysiological recordings from host-stage hookworm and Ascaris suum larvae: A new tool for anthelmintic research

“…In C. elegans , 5HT influences pharyngeal behavior via multiple neural pathways and 5HT receptor subtypes (Song and Avery, 2012, Trojanowski et al., 2016). Comparable information is not available for hookworms.…”

“…Our device records electropharyngeograms (EPGs) from eight worms simultaneously during exposure to control or test substances. EPG recordings reveal electrical activity of muscles and neurons of the pharynx (sometimes termed the esophagus), the muscular pump used for feeding (Raizen and Avery, 1994, Trojanowski et al., 2016). In C. elegans , pharyngeal pumping draws bacteria into the digestive tract, whereas intestinal parasites ingest host digesta, blood and/or tissue (Wells, 1931, Kalkofen, 1970, Khuroo, 1996, Avery and You, 2012).…”