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

Author

Listed:
  • Jingyuan Jiang

    (Peking University)

  • Yifan Su

    (Peking University)

  • Ruilin Zhang

    (Peking University
    Peking University)

  • Haiwen Li

    (Peking University)

  • Louis Tao

    (Peking University
    Peking University)

  • Qiang Liu

    (The Rockefeller University
    City University of Hong Kong)

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.

Suggested Citation

  • Jingyuan Jiang & Yifan Su & Ruilin Zhang & Haiwen Li & Louis Tao & Qiang Liu, 2022. "C. elegans enteric motor neurons fire synchronized action potentials underlying the defecation motor program," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-30452-y
    DOI: 10.1038/s41467-022-30452-y
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    References listed on IDEAS

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    1. Ping Liu & Bojun Chen & Zhao-Wen Wang, 2014. "SLO-2 potassium channel is an important regulator of neurotransmitter release in Caenorhabditis elegans," Nature Communications, Nature, vol. 5(1), pages 1-12, December.
    2. Theodore H. Lindsay & Tod R. Thiele & Shawn R. Lockery, 2011. "Optogenetic analysis of synaptic transmission in the central nervous system of the nematode Caenorhabditis elegans," Nature Communications, Nature, vol. 2(1), pages 1-9, September.
    3. Ping Liu & Bojun Chen & Roger Mailler & Zhao-Wen Wang, 2017. "Antidromic-rectifying gap junctions amplify chemical transmission at functionally mixed electrical-chemical synapses," Nature Communications, Nature, vol. 8(1), pages 1-16, April.
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    Cited by:

    1. Ukjin Choi & Mingxi Hu & Qixin Zhang & Derek Sieburth, 2023. "The head mesodermal cell couples FMRFamide neuropeptide signaling with rhythmic muscle contraction in C. elegans," Nature Communications, Nature, vol. 14(1), pages 1-16, December.

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