Sensory Glia Detect Repulsive Odorants and Drive Olfactory Adaptation

  • Neuron. 2020 Nov 25;108(4):707-721.e8. doi: 10.1016/j.neuron.2020.08.026.
Duo Duan  1 ,  Hu Zhang  2 ,  Xiaomin Yue  2 ,  Yuedan Fan  2 ,  Yadan Xue  3 ,  Jiajie Shao  3 ,  Gang Ding  3 ,  Du Chen  3 ,  Shitian Li  3 ,  Hankui Cheng  3 ,  Xiaoyan Zhang  3 ,  Wenjuan Zou  3 ,  Jia Liu  3 ,  Jian Zhao  3 ,  Linmei Wang  3 ,  Bingzhen Zhao  4 ,  Zhiping Wang  3 ,  Suhong Xu  5 ,  Quan Wen  4 ,  Jie Liu  6 ,  Shumin Duan  7 ,  Lijun Kang  8
Affiliations
  • 1. Department of Neurobiology and Department of Neurosurgery of the First Affiliated Hospital, Zhejiang University School of Medicine, Zhejiang 310053, China; NHC and CAMS Key Laboratory of Medical Neurobiology, MOE Frontier Science Center for Brain Research and Brain-Machine Integration, School of Brain Science and Brain Medicine, Zhejiang University, Hangzhou, Zhejiang 310053, China; Department of Neurology of Second Affiliated Hospital, Zhejiang University School of Medicine, Zhejiang 310053, China.
  • 2. Department of Neurobiology and Department of Neurosurgery of the First Affiliated Hospital, Zhejiang University School of Medicine, Zhejiang 310053, China; NHC and CAMS Key Laboratory of Medical Neurobiology, MOE Frontier Science Center for Brain Research and Brain-Machine Integration, School of Brain Science and Brain Medicine, Zhejiang University, Hangzhou, Zhejiang 310053, China.
  • 3. Department of Neurobiology and Department of Neurosurgery of the First Affiliated Hospital, Zhejiang University School of Medicine, Zhejiang 310053, China.
  • 4. Chinese Academy of Sciences Key Laboratory of Brain Function and Disease, School of Life Sciences, University of Science and Technology of China, Hefei, Anhui 230026, China.
  • 5. Center for Stem Cell and Regenerative Medicine, Zhejiang University School of Medicine, Hangzhou, Zhejiang 310058, China.
  • 6. Monash Biomedicine Discovery Institute, Department of Anatomy and Developmental Biology, Monash University, Clayton, VIC 3800, Australia.
  • 7. NHC and CAMS Key Laboratory of Medical Neurobiology, MOE Frontier Science Center for Brain Research and Brain-Machine Integration, School of Brain Science and Brain Medicine, Zhejiang University, Hangzhou, Zhejiang 310053, China; Department of Neurology of Second Affiliated Hospital, Zhejiang University School of Medicine, Zhejiang 310053, China. Electronic address: [email protected].
  • 8. Department of Neurobiology and Department of Neurosurgery of the First Affiliated Hospital, Zhejiang University School of Medicine, Zhejiang 310053, China; NHC and CAMS Key Laboratory of Medical Neurobiology, MOE Frontier Science Center for Brain Research and Brain-Machine Integration, School of Brain Science and Brain Medicine, Zhejiang University, Hangzhou, Zhejiang 310053, China. Electronic address: [email protected].
PMID: 32970991 DOI: 10.1016/j.neuron.2020.08.026
Abstract

Glia are typically considered as supporting cells for neural development and synaptic transmission. Here, we report an active role of a glia in olfactory transduction. As a polymodal sensory neuron in C. elegans, the ASH neuron is previously known to detect multiple aversive odorants. We reveal that the AMsh glia, a sheath for multiple sensory neurons including ASH, cell-autonomously respond to aversive odorants via G-protein-coupled receptors (GPCRs) distinct from those in ASH. Upon activation, the AMsh glia suppress aversive odorant-triggered avoidance and promote olfactory adaptation by inhibiting the ASH neuron via GABA signaling. Thus, we propose a novel two-receptor model where the glia and sensory neuron jointly mediate adaptive olfaction. Our study reveals a non-canonical function of glial cells in olfactory transduction, which may provide new insights into the glia-like supporting cells in mammalian sensory procession.

Keywords
C. elegans; GABAergic inhibition; glia; olfactory adaptation; olfactory transduction.
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