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C. elegans enteric motor neurons fire synchronized action potentials underlying the defecation motor program.

ABSTRACT: C. elegans neurons were thought to be non-spiking until our recent discovery of action potentials in the sensory neuron AWA; however, the extent to which the C. elegans nervous system relies on analog or digital coding is unclear. Here we show that the enteric motor neurons AVL and DVB fire synchronous all-or-none calcium-mediated action potentials following the intestinal pacemaker during the rhythmic C. elegans defecation behavior. AVL fires unusual compound action potentials with each depolarizing calcium spike mediated by UNC-2 followed by a hyperpolarizing potassium spike mediated by a repolarization-activated potassium channel EXP-2. Simultaneous behavior tracking and imaging in free-moving animals suggest that action potentials initiated in AVL propagate along its axon to activate precisely timed DVB action potentials through the INX-1 gap junction. This work identifies a novel circuit of spiking neurons in C. elegans that uses digital coding for long-distance communication and temporal synchronization underlying reliable behavioral rhythm.

SUBMITTER: Jiang J

PROVIDER: S-EPMC9120479 | biostudies-literature | 2022 May

REPOSITORIES: biostudies-literature

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C. elegans enteric motor neurons fire synchronized action potentials underlying the defecation motor program.

Jiang Jingyuan J Su Yifan Y Zhang Ruilin R Li Haiwen H Tao Louis L Liu Qiang Q

Nature communications 20220519 1

C. elegans neurons were thought to be non-spiking until our recent discovery of action potentials in the sensory neuron AWA; however, the extent to which the C. elegans nervous system relies on analog or digital coding is unclear. Here we show that the enteric motor neurons AVL and DVB fire synchronous all-or-none calcium-mediated action potentials following the intestinal pacemaker during the rhythmic C. elegans defecation behavior. AVL fires unusual compound action potentials with each depolar ...[more]

PMID: 35589790

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Project description:BackgroundPulmonary veins (PVs) and the coronary sinus (CS) play pivotal roles in triggering some episodes of atrial fibrillation. In isolated rabbit right or left atrial preparations, a 3-hour intermittent burst pacing protocol shortens action potential duration (APD) in CS and PV, but not in sinus node (SN) and left Bachmann bundle (BB) regions.ObjectiveThe purpose of this study was to use patch clamp techniques to study the rapidly inactivating (I(to)) and sustained (I(sus)) K(+) currents as well as Ca(2+) currents (I(Ca)) in cells dispersed from intermittent burst pacing and sham PV, BB, CS, and SN regions to determine whether changes in these currents contributed to APD shortening.MethodsReal-time polymerase chain reaction was performed for transient outward K(+) and Ca(2+) channel subunit mRNAs to determine if intermittent burst pacing affected expression levels.ResultsI(to) densities were unaffected by intermittent burst pacing in PV and Bachmann bundle cells. mRNA levels of K(V)4.3, K(V)4.2, K(V)1.4, and KChIP2 subunits of I(to) in both regions were stable. In CS cells, I(to) densities in intermittent burst pacing were greater than in sham (P <.05), but there were no parallel mRNA changes. I(Ca) density of PV cells was reduced from 14.27 +/- 2.08 pA/pF (at -5 mV) in sham to 7.52 +/- 1.65 pA/pF in intermittent burst pacing PV cells (P <.05) due to a significant shift in voltage dependence of activation. These results were seen in the absence of mRNA changes in alpha(1C) and alpha(1D) Ca(2+) channel subunits. In contrast, intermittent burst pacing had no effect on Ca(2+) current densities and kinetics of CS cells, but decreased alpha(1)C and alpha(1)D mRNA levels.ConclusionThere is region-specific remodeling of I(to) and I(Ca) by intermittent burst pacing protocols in rabbit atrium. Increased I(to) in CS cells could account for the APD shortening observed with intermittent burst pacing, whereas an intermittent burst pacing-induced shift in voltage dependence of activation may contribute to APD shortening in PV cells.

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C. elegans enteric motor neurons fire synchronized action potentials underlying the defecation motor program.

Publications

C. elegans enteric motor neurons fire synchronized action potentials underlying the defecation motor program.

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