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Molecular encoding and synaptic decoding of context during salt chemotaxis in C. elegans

Author

Listed:
  • Shingo Hiroki

    (The University of Tokyo)

  • Hikari Yoshitane

    (The University of Tokyo
    Tokyo Metropolitan Institute of Medical Science)

  • Hinako Mitsui

    (The University of Tokyo)

  • Hirofumi Sato

    (The University of Tokyo)

  • Chie Umatani

    (The University of Tokyo)

  • Shinji Kanda

    (The University of Tokyo)

  • Yoshitaka Fukada

    (The University of Tokyo
    Tokyo Metropolitan Institute of Medical Science
    The University of Tokyo)

  • Yuichi Iino

    (The University of Tokyo)

Abstract

Animals navigate toward favorable locations using various environmental cues. However, the mechanism of how the goal information is encoded and decoded to generate migration toward the appropriate direction has not been clarified. Here, we describe the mechanism of migration towards a learned concentration of NaCl in Caenorhabditis elegans. In the salt-sensing neuron ASER, the difference between the experienced and currently perceived NaCl concentration is encoded as phosphorylation at Ser65 of UNC-64/Syntaxin 1 A through the protein kinase C(PKC-1) signaling pathway. The phosphorylation affects basal glutamate transmission from ASER, inducing the reversal of the postsynaptic response of reorientation-initiating neurons (i.e., from inhibitory to excitatory), guiding the animals toward the experienced concentration. This process, the decoding of the context, is achieved through the differential sensitivity of postsynaptic excitatory and inhibitory receptors. Our results reveal the mechanism of migration based on the synaptic plasticity that conceptually differs from the classical ones.

Suggested Citation

  • Shingo Hiroki & Hikari Yoshitane & Hinako Mitsui & Hirofumi Sato & Chie Umatani & Shinji Kanda & Yoshitaka Fukada & Yuichi Iino, 2022. "Molecular encoding and synaptic decoding of context during salt chemotaxis in C. elegans," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-30279-7
    DOI: 10.1038/s41467-022-30279-7
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    References listed on IDEAS

    as
    1. Hirofumi Kunitomo & Hirofumi Sato & Ryo Iwata & Yohsuke Satoh & Hayao Ohno & Koji Yamada & Yuichi Iino, 2013. "Concentration memory-dependent synaptic plasticity of a taste circuit regulates salt concentration chemotaxis in Caenorhabditis elegans," Nature Communications, Nature, vol. 4(1), pages 1-11, October.
    2. Chi-Wei Tien & Bin Yu & Mengjia Huang & Karolina P. Stepien & Kyoko Sugita & Xiaoyu Xie & Liping Han & Philippe P. Monnier & Mei Zhen & Josep Rizo & Shangbang Gao & Shuzo Sugita, 2020. "Open syntaxin overcomes exocytosis defects of diverse mutants in C. elegans," Nature Communications, Nature, vol. 11(1), pages 1-18, December.
    3. 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.
    4. Thorsten Althoff & Ryan E. Hibbs & Surajit Banerjee & Eric Gouaux, 2014. "X-ray structures of GluCl in apo states reveal a gating mechanism of Cys-loop receptors," Nature, Nature, vol. 512(7514), pages 333-337, August.
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