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Reciprocal inhibition between sensory ASH and ASI neurons modulates nociception and avoidance in Caenorhabditis elegans

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  • Min Guo

    (Key Laboratory of Molecular Biophysics of Ministry of Education, Institute of Biophysics and Biochemistry, College of Life Science and Technology, Huazhong University of Science and Technology, 1037 Luoyu Road, Wuhan 430074, China)

  • Tai-Hong Wu

    (Key Laboratory of Molecular Biophysics of Ministry of Education, Institute of Biophysics and Biochemistry, College of Life Science and Technology, Huazhong University of Science and Technology, 1037 Luoyu Road, Wuhan 430074, China)

  • Yan-Xue Song

    (Key Laboratory of Molecular Biophysics of Ministry of Education, Institute of Biophysics and Biochemistry, College of Life Science and Technology, Huazhong University of Science and Technology, 1037 Luoyu Road, Wuhan 430074, China)

  • Ming-Hai Ge

    (Key Laboratory of Molecular Biophysics of Ministry of Education, Institute of Biophysics and Biochemistry, College of Life Science and Technology, Huazhong University of Science and Technology, 1037 Luoyu Road, Wuhan 430074, China)

  • Chun-Ming Su

    (Key Laboratory of Molecular Biophysics of Ministry of Education, Institute of Biophysics and Biochemistry, College of Life Science and Technology, Huazhong University of Science and Technology, 1037 Luoyu Road, Wuhan 430074, China)

  • Wei-Pin Niu

    (Key Laboratory of Molecular Biophysics of Ministry of Education, Institute of Biophysics and Biochemistry, College of Life Science and Technology, Huazhong University of Science and Technology, 1037 Luoyu Road, Wuhan 430074, China)

  • Lan-Lan Li

    (Key Laboratory of Molecular Biophysics of Ministry of Education, Institute of Biophysics and Biochemistry, College of Life Science and Technology, Huazhong University of Science and Technology, 1037 Luoyu Road, Wuhan 430074, China)

  • Zi-Jing Xu

    (Key Laboratory of Molecular Biophysics of Ministry of Education, Institute of Biophysics and Biochemistry, College of Life Science and Technology, Huazhong University of Science and Technology, 1037 Luoyu Road, Wuhan 430074, China)

  • Chang-Li Ge

    (Key Laboratory of Molecular Biophysics of Ministry of Education, Institute of Biophysics and Biochemistry, College of Life Science and Technology, Huazhong University of Science and Technology, 1037 Luoyu Road, Wuhan 430074, China)

  • Maha T. H. Al-Mhanawi

    (Key Laboratory of Molecular Biophysics of Ministry of Education, Institute of Biophysics and Biochemistry, College of Life Science and Technology, Huazhong University of Science and Technology, 1037 Luoyu Road, Wuhan 430074, China)

  • Shi-Ping Wu

    (School of Chemical Engineering and Pharmacy, Wuhan Institute of Technology)

  • Zheng-Xing Wu

    (Key Laboratory of Molecular Biophysics of Ministry of Education, Institute of Biophysics and Biochemistry, College of Life Science and Technology, Huazhong University of Science and Technology, 1037 Luoyu Road, Wuhan 430074, China)

Abstract

Sensory modulation is essential for animal sensations, behaviours and survival. Peripheral modulations of nociceptive sensations and aversive behaviours are poorly understood. Here we identify a biased cross-inhibitory neural circuit between ASH and ASI sensory neurons. This inhibition is essential to drive normal adaptive avoidance of a CuSO4 (Cu2+) challenge in Caenorhabditis elegans. In the circuit, ASHs respond to Cu2+ robustly and suppress ASIs via electro-synaptically exciting octopaminergic RIC interneurons, which release octopamine (OA), and neuroendocrinally inhibit ASI by acting on the SER-3 receptor. In addition, ASIs sense Cu2+ and permit a rapid onset of Cu2+-evoked responses in Cu2+-sensitive ADF neurons via neuropeptides possibly, to inhibit ASHs. ADFs function as interneurons to mediate ASI inhibition of ASHs by releasing serotonin (5-HT) that binds with the SER-5 receptor on ASHs. This elaborate modulation among sensory neurons via reciprocal inhibition fine-tunes the nociception and avoidance behaviour.

Suggested Citation

  • Min Guo & Tai-Hong Wu & Yan-Xue Song & Ming-Hai Ge & Chun-Ming Su & Wei-Pin Niu & Lan-Lan Li & Zi-Jing Xu & Chang-Li Ge & Maha T. H. Al-Mhanawi & Shi-Ping Wu & Zheng-Xing Wu, 2015. "Reciprocal inhibition between sensory ASH and ASI neurons modulates nociception and avoidance in Caenorhabditis elegans," Nature Communications, Nature, vol. 6(1), pages 1-13, May.
    • Handle: RePEc:nat:natcom:v:6:y:2015:i:1:d:10.1038_ncomms6655
    DOI: 10.1038/ncomms6655
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    Cited by:

    1. Chenxi Lin & Yuxin Shan & Zhongyi Wang & Hui Peng & Rong Li & Pingzhou Wang & Junyan He & Weiwei Shen & Zhengxing Wu & Min Guo, 2024. "Molecular and circuit mechanisms underlying avoidance of rapid cooling stimuli in C. elegans," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    2. Tobias Clark & Vera Hapiak & Mitchell Oakes & Holly Mills & Richard Komuniecki, 2018. "Monoamines differentially modulate neuropeptide release from distinct sites within a single neuron pair," PLOS ONE, Public Library of Science, vol. 13(5), pages 1-22, May.

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