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Injury of Muscular but not Cutaneous Nerve Drives Acute Neuropathic Pain in Rats

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Abstract

Acute pain is a common complication after injury of a peripheral nerve but the underlying mechanism is obscure. We established a model of acute neuropathic pain via pulling a pre-implanted suture loop to transect a peripheral nerve in awake rats. The tibial (both muscular and cutaneous), gastrocnemius–soleus (muscular only), and sural nerves (cutaneous only) were each transected. Transection of the tibial and gastrocnemius–soleus nerves, but not the sural nerve immediately evoked spontaneous pain and mechanical allodynia in the skin territories innervated by the adjacent intact nerves. Evans blue extravasation and cutaneous temperature of the intact skin territory were also significantly increased. In vivo electrophysiological recordings revealed that injury of a muscular nerve induced mechanical hypersensitivity and spontaneous activity in the nociceptive C-neurons in adjacent intact nerves. Our results indicate that injury of a muscular nerve, but not a cutaneous nerve, drives acute neuropathic pain.

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Acknowledgements

We thank Bo Yuan, B.S., Tao Wang, Ph.D. and Jin Tao, M.S. from the Institute of Basic Medical Sciences, Chinese Academy of Medical Sciences, Beijing, China, for technical assistance. This work was supported by grants from the National Natural Science Foundation of China (NSFC; 81271239 and 91632113 to CM, and NSFC for Young Scientists 81600956 to WD), and the Chinese Academy of Medical Sciences Innovation Fund for Medical Sciences (2017-I2M-3-008 to CM).

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Author notes

  1. Jie Zhu, Zhiyong Chen, and Yehong Fang have contributed equally to this work.

Authors and Affiliations

  1. Department of Human Anatomy, Histology and Embryology, Institute of Basic Medical Sciences, Neuroscience Center, Chinese Academy of Medical Sciences, School of Basic Medicine, Peking Union Medical College, Beijing, 100005, China

    Jie Zhu, Zhiyong Chen, Yehong Fang, Yikuan Xie & Chao Ma

  2. Department of Radiation Oncology, Sichuan Cancer Hospital and Institute, Sichuan Cancer Center, School of Medicine, University of Electronic Science and Technology of China, Chengdu, 610054, China

    Jie Zhu

  3. Joint Laboratory of Anesthesia and Pain, Peking Union Medical College, Beijing, 100730, China

    Zhiyong Chen, Yehong Fang & Chao Ma

  4. Department of Anesthesiology and Critical Care Medicine, Johns Hopkins University, School of Medicine, Baltimore, MD, 21205, USA

    Zhiyong Chen

  5. Department of Neurosurgery, Xuanwu Hospital, Capital Medical University, Beijing, 100053, China

    Wanru Duan

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  1. Jie Zhu
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Correspondence to Chao Ma.

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Zhu, J., Chen, Z., Fang, Y. et al. Injury of Muscular but not Cutaneous Nerve Drives Acute Neuropathic Pain in Rats. Neurosci. Bull. 36, 453–462 (2020). https://doi.org/10.1007/s12264-019-00462-w

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  • DOI: https://doi.org/10.1007/s12264-019-00462-w

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