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

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 and Zheng-Xing Wu ()
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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

Nature Communications, 2015, vol. 6, issue 1, 1-13

Abstract: 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.

Date: 2015
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DOI: 10.1038/ncomms6655

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