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Parallel ascending spinal pathways for affective touch and pain

Author

Listed:
  • Seungwon Choi

    (Howard Hughes Medical Institute, Harvard Medical School)

  • Junichi Hachisuka

    (University of Pittsburgh
    University of Pittsburgh
    University of Glasgow)

  • Matthew A. Brett

    (Howard Hughes Medical Institute, Harvard Medical School)

  • Alexandra R. Magee

    (Howard Hughes Medical Institute, Harvard Medical School)

  • Yu Omori

    (University of Pittsburgh
    University of Pittsburgh
    Toray Industries, Inc., Pharmaceutical Research Laboratories)

  • Noor-ul-Aine Iqbal

    (Howard Hughes Medical Institute, Harvard Medical School)

  • Dawei Zhang

    (Howard Hughes Medical Institute, Harvard Medical School)

  • Michelle M. DeLisle

    (Howard Hughes Medical Institute, Harvard Medical School)

  • Rachel L. Wolfson

    (Howard Hughes Medical Institute, Harvard Medical School)

  • Ling Bai

    (Howard Hughes Medical Institute, Harvard Medical School)

  • Celine Santiago

    (Howard Hughes Medical Institute, Harvard Medical School)

  • Shiaoching Gong

    (The Rockefeller University)

  • Martyn Goulding

    (The Salk Institute for Biological Studies)

  • Nathaniel Heintz

    (The Rockefeller University)

  • H. Richard Koerber

    (University of Pittsburgh
    University of Pittsburgh)

  • Sarah E. Ross

    (University of Pittsburgh
    University of Pittsburgh)

  • David D. Ginty

    (Howard Hughes Medical Institute, Harvard Medical School)

Abstract

The anterolateral pathway consists of ascending spinal tracts that convey pain, temperature and touch information from the spinal cord to the brain1–4. Projection neurons of the anterolateral pathway are attractive therapeutic targets for pain treatment because nociceptive signals emanating from the periphery are channelled through these spinal projection neurons en route to the brain. However, the organizational logic of the anterolateral pathway remains poorly understood. Here we show that two populations of projection neurons that express the structurally related G-protein-coupled receptors (GPCRs) TACR1 and GPR83 form parallel ascending circuit modules that cooperate to convey thermal, tactile and noxious cutaneous signals from the spinal cord to the lateral parabrachial nucleus of the pons. Within this nucleus, axons of spinoparabrachial (SPB) neurons that express Tacr1 or Gpr83 innervate distinct sets of subnuclei, and strong optogenetic stimulation of the axon terminals induces distinct escape behaviours and autonomic responses. Moreover, SPB neurons that express Gpr83 are highly sensitive to cutaneous mechanical stimuli and receive strong synaptic inputs from both high- and low-threshold primary mechanosensory neurons. Notably, the valence associated with activation of SPB neurons that express Gpr83 can be either positive or negative, depending on stimulus intensity. These findings reveal anatomically, physiologically and functionally distinct subdivisions of the SPB tract that underlie affective aspects of touch and pain.

Suggested Citation

  • Seungwon Choi & Junichi Hachisuka & Matthew A. Brett & Alexandra R. Magee & Yu Omori & Noor-ul-Aine Iqbal & Dawei Zhang & Michelle M. DeLisle & Rachel L. Wolfson & Ling Bai & Celine Santiago & Shiaoch, 2020. "Parallel ascending spinal pathways for affective touch and pain," Nature, Nature, vol. 587(7833), pages 258-263, November.
  • Handle: RePEc:nat:nature:v:587:y:2020:i:7833:d:10.1038_s41586-020-2860-1
    DOI: 10.1038/s41586-020-2860-1
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    Cited by:

    1. Mayank Gautam & Akihiro Yamada & Ayaka I. Yamada & Qinxue Wu & Kim Kridsada & Jennifer Ling & Huasheng Yu & Peter Dong & Minghong Ma & Jianguo Gu & Wenqin Luo, 2024. "Distinct local and global functions of mouse Aβ low-threshold mechanoreceptors in mechanical nociception," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    2. Fu-Chao Zhang & Rui-Xia Weng & Di Li & Yong-Chang Li & Xiao-Xuan Dai & Shufen Hu & Qian Sun & Rui Li & Guang-Yin Xu, 2024. "A vagus nerve dominant tetra-synaptic ascending pathway for gastric pain processing," Nature Communications, Nature, vol. 15(1), pages 1-16, December.

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