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Touch and tactile neuropathic pain sensitivity are set by corticospinal projections

Author

Listed:
  • Yuanyuan Liu

    (Boston Children’s Hospital
    Harvard Medical School)

  • Alban Latremoliere

    (Boston Children’s Hospital
    Johns Hopkins School of Medicine)

  • Xinjian Li

    (Clinical and Translational Neuroscience Branch, National Institute of Mental Health, National Institutes of Health
    Zhejiang University School of Medicine)

  • Zicong Zhang

    (Boston Children’s Hospital
    Harvard Medical School)

  • Mengying Chen

    (Boston Children’s Hospital
    Children’s Hospital of Nanjing Medical University)

  • Xuhua Wang

    (Boston Children’s Hospital)

  • Chao Fang

    (Boston Children’s Hospital)

  • Junjie Zhu

    (Boston Children’s Hospital)

  • Chloe Alexandre

    (Johns Hopkins School of Medicine
    Beth Israel Deaconess Medical Center)

  • Zhongyang Gao

    (Boston Children’s Hospital)

  • Bo Chen

    (Boston Children’s Hospital
    Harvard Medical School)

  • Xin Ding

    (Boston Children’s Hospital)

  • Jin-Yong Zhou

    (Boston Children’s Hospital)

  • Yiming Zhang

    (Boston Children’s Hospital)

  • Chinfei Chen

    (Boston Children’s Hospital
    Harvard Medical School)

  • Kuan Hong Wang

    (Clinical and Translational Neuroscience Branch, National Institute of Mental Health, National Institutes of Health)

  • Clifford J. Woolf

    (Boston Children’s Hospital
    Harvard Medical School
    Harvard Medical School)

  • Zhigang He

    (Boston Children’s Hospital
    Harvard Medical School)

Abstract

Current models of somatosensory perception emphasize transmission from primary sensory neurons to the spinal cord and on to the brain1–4. Mental influence on perception is largely assumed to occur locally within the brain. Here we investigate whether sensory inflow through the spinal cord undergoes direct top-down control by the cortex. Although the corticospinal tract (CST) is traditionally viewed as a primary motor pathway5, a subset of corticospinal neurons (CSNs) originating in the primary and secondary somatosensory cortex directly innervate the spinal dorsal horn via CST axons. Either reduction in somatosensory CSN activity or transection of the CST in mice selectively impairs behavioural responses to light touch without altering responses to noxious stimuli. Moreover, such CSN manipulation greatly attenuates tactile allodynia in a model of peripheral neuropathic pain. Tactile stimulation activates somatosensory CSNs, and their corticospinal projections facilitate light-touch-evoked activity of cholecystokinin interneurons in the deep dorsal horn. This touch-driven feed-forward spinal–cortical–spinal sensitization loop is important for the recruitment of spinal nociceptive neurons under tactile allodynia. These results reveal direct cortical modulation of normal and pathological tactile sensory processing in the spinal cord and open up opportunities for new treatments for neuropathic pain.

Suggested Citation

  • Yuanyuan Liu & Alban Latremoliere & Xinjian Li & Zicong Zhang & Mengying Chen & Xuhua Wang & Chao Fang & Junjie Zhu & Chloe Alexandre & Zhongyang Gao & Bo Chen & Xin Ding & Jin-Yong Zhou & Yiming Zhan, 2018. "Touch and tactile neuropathic pain sensitivity are set by corticospinal projections," Nature, Nature, vol. 561(7724), pages 547-550, September.
  • Handle: RePEc:nat:nature:v:561:y:2018:i:7724:d:10.1038_s41586-018-0515-2
    DOI: 10.1038/s41586-018-0515-2
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    Citations

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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. Chao Chen & Linlin Sun & Avital Adler & Hang Zhou & Licheng Zhang & Lihai Zhang & Junhao Deng & Yang Bai & Jinhui Zhang & Guang Yang & Wen-Biao Gan & Peifu Tang, 2023. "Synchronized activity of sensory neurons initiates cortical synchrony in a model of neuropathic pain," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    3. Daniel G. Taub & Qiufen Jiang & Francesca Pietrafesa & Junfeng Su & Aloe Carroll & Caitlin Greene & Michael R. Blanchard & Aakanksha Jain & Mahmoud El-Rifai & Alexis Callen & Katherine Yager & Clara C, 2024. "The secondary somatosensory cortex gates mechanical and heat sensitivity," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    4. Hironobu Osaki & Moeko Kanaya & Yoshifumi Ueta & Mariko Miyata, 2022. "Distinct nociception processing in the dysgranular and barrel regions of the mouse somatosensory cortex," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    5. Saeka Tomatsu & GeeHee Kim & Shinji Kubota & Kazuhiko Seki, 2023. "Presynaptic gating of monkey proprioceptive signals for proper motor action," Nature Communications, Nature, vol. 14(1), pages 1-14, December.

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