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

Min Guo,Ming-Hai Ge,Maha T H Al-Mhanawi,Yan-Xue Song,Zi-Jing Xu,Wei-Pin Niu,Zheng-Xing Wu,Chun-Ming Su,Chang-Li Ge,Shi-Ping Wu,Tai-Hong Wu,Lan-Lan Li

doi:10.1038/ncomms6655

Min Guo, Ming-Hai Ge + Show 10 more

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https://doi.org/10.1038/ncomms6655

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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 (Cu(2+)) challenge in Caenorhabditis elegans. In the circuit, ASHs respond to Cu(2+) 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 Cu(2+) and permit a rapid onset of Cu(2+)-evoked responses in Cu(2+)-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.

Highlights

Sensory neurons transform various stimuli from the external and internal environment into sensory information that is primarily integrated in the central nervous system to form sensation and perception, drive adaptive behaviours and maintain physiological homeostasis
The polymodal ASH sensory neurons in C. elegans sense a variety of aversive stimuli and mediate avoidance of high osmotic, mechanical and chemical stimuli[8,9,10,11]
We examined the impact of silencing ASIs on the kinematics of a Cu2 þ -evoked reversal

Summary

Introduction

Sensory neurons transform various stimuli from the external and internal environment into sensory information that is primarily integrated in the central nervous system to form sensation and perception, drive adaptive behaviours and maintain physiological homeostasis. ASI sensory neurons are reported to mediate dauer formation[16], enable worms to learn to avoid the smell of pathogenic bacteria after ingestion via INS-6 signalling[17], suppress male-specific sexual attraction behaviour[18], respond to temperature stimuli to negatively modulate thermotaxis behaviour[19], mediate diet-restriction-induced longevity[20], modulate satiety quiescence[21], regulate acute CO2 avoidance[22], repress exploratory behaviours that comprise spontaneous reversals and omega turns[5], and inhibit ASH-mediated aversive responses to 100% 1-octanol[23] These studies support the hypothesis that ASIs are important polymodal sensory neurons mediating or modulating worm behaviours and development. The elaborate modulation of Cu2 þ sensation through the reciprocal inhibitory neuron circuit fine-tunes the worm nociception and avoidance behaviour

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