Cutaneous Hypersensitivity as an Indicator of Visceral Inflammation via C-Nociceptor Axon Bifurcation
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ORIGINAL ARTICLE
Cutaneous Hypersensitivity as an Indicator of Visceral Inflammation via C-Nociceptor Axon Bifurcation Yehong Fang1,3 • Shu Han2 • Xiaoxue Li2 • Yikuan Xie1,3 • Bing Zhu2 Xinyan Gao2 • Chao Ma1,3
•
Received: 5 January 2020 / Accepted: 19 May 2020 Ó The Author(s) 2020
Abstract Pain on the body surface can accompany disorders in the deep tissue or internal organs. However, the anatomical and physiological mechanisms are obscure. Here, we provided direct evidence of axon bifurcation in primary C-nociceptive neurons that innervate both the skin and a visceral organ. Double-labeled dorsal root ganglion (DRG) neurons and Evans blue extravasation were observed in 3 types of chemically-induced visceral inflammation (colitis, urocystitis, and acute gastritis) rat models. In the colitis model, mechanical hypersensitivity and spontaneous activity were recorded in vivo from doublelabeled C-nociceptive neurons in S1 or L6 DRGs. These neurons showed significantly enhanced responses to both somatic stimulation and colorectal distension. Our findings suggest that the branching of C-nociceptor axons contribute to cutaneous hypersensitivity in visceral inflammation. Cutaneous hypersensitivity on certain locations of the
Yehong Fang, Shu Han and Xiaoxue Li have contributed equally to this work. & Xinyan Gao [email protected] & Chao Ma [email protected] 1
Institute of Basic Medical Sciences, Department of Human Anatomy, Histology and Embryology, Neuroscience Center, Chinese Academy of Medical Sciences, School of Basic Medicine, Peking Union Medical College, Beijing 100005, China
2
Department of Physiology, Institute of Acupuncture and Moxibustion, China Academy of Chinese Medical Sciences, Beijing 100700, China
3
Joint Laboratory of Anesthesia and Pain, Peking Union Medical College, Beijing 100730, China
body surface might serve as an indicator of pathological conditions in the corresponding visceral organ. Keywords Visceral inflammation Cutaneous hypersensitivity Axon bifurcation C-nociceptor
Introduction Visceral pain, involving thoracic, abdominal, and pelvic organs, is the most common type of chronic pain nowadays [1–3]. However, the poor understanding of its pathogenesis makes it difficult to manage. It is well recognized that visceral innervation is complex. Organs in the thoracic and abdominal cavities may be innervated by both the vagal and spinal nerves with central terminals in the brainstem and spinal cord, respectively. Meanwhile, some pelvic organs are innervated by the pelvic nerves, which terminate in the lumbosacral spinal cord [4, 5]. Unlike cutaneous pain that is well localized, visceral pain is diffuse and often referred to a distal superficial location [4, 6]. Therefore, it is necessary to find an indicator to help detect and locate visceral pain in order to treat visceral diseases better. Previous studies indicated that virtually all second-order spinal dorsal horn neurons, like wide dynamic range neurons, receive both visceral and c
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