Acute pressure on the sciatic nerve results in rapid inhibition of the wide dynamic range neuronal response

BMC Neuroscience

Jiman He⁴  Jun Chen¹  Buling Wu²  Wangyeng Zhao²  Qun Wang²  Yaoqing Yu¹  Jianhua Lin²  Danping Luo²  Wei Tan²  Wenxue Wang³ 

[1] Institute for Biomedical Sciences of Pain and Institute for Functional Brain Disorders, Tangdu Hospital, Fourth Military Medical University, Xi’an, 710032, China;Pain Medicine Program, IDD, Nanfang Hospital, Southern Medical University, Guangzhou, 510515, China;Department of Physiology, School of Life Science, Kuning, 605000, China;Rhode Island Hospital, Brown University, Providence, 02903, USA

关键词: Acute pressure;    Pain;    WDR;    Sciatic nerve;   

Others  :  1140698
DOI  :  10.1186/1471-2202-13-147

 received in 2012-02-15, accepted in 2012-11-29,  发布年份 2012

【 摘 要 】

Background

Acute pressure on the sciatic nerve has recently been reported to provide rapid short-term relief of pain in patients with various pathologies. Wide dynamic range (WDR) neurons transmit nociceptive information from the dorsal horn to higher brain centers. In the present study, we examined the effect of a 2-min application of sciatic nerve pressure on WDR neuronal activity in anesthetized male Sprague–Dawley rats.

Results

Experiments were carried out on 41 male Sprague–Dawley albino rats weighing 160–280 grams. Dorsal horn WDR neurons were identified on the basis of characteristic responses to mechanical stimuli applied to the cutaneous receptive field. Acute pressure was applied for 2 min to the sciatic nerve using a small vascular clip. The responses of WDR neurons to three mechanical stimuli applied to the cutaneous receptive field were recorded before, and 2, 5 and 20 min after cessation of the 2-min pressure application on the sciatic nerve. Two-min pressure applied to the sciatic nerve caused rapid attenuation of the WDR response to pinching, pressure and brushing stimuli applied to the cutaneous receptive field. Maximal attenuation of the WDR response to pinching and pressure was noted 5 min after release of the 2-min pressure on the sciatic nerve. The mean firing rate decreased from 31.7±1.7 Hz to 13±1.4 Hz upon pinching (p < 0.001), from 31.2±2.3 Hz to 10.9±1.4 Hz (p < 0.001) when pressure was applied, and from 18.9±1.2 Hz to 7.6±1.1 Hz (p < 0.001) upon brushing. Thereafter, the mean firing rates gradually recovered.

Conclusions

Our results indicate that acute pressure applied to the sciatic nerve exerts a rapid inhibitory effect on the WDR response to both noxious and innocuous stimuli. Our results may partially explain the rapid analgesic effect of acute sciatic nerve pressure noted in clinical studies, and also suggest a new model for the study of pain.

【 授权许可】

   
2012 Wang et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Al-Khodairy AW, Bovay P, Gobelet C: Sciatica in the female patient: anatomical considerations, aetiology and review of the literature. Eur Spine J 2007, 16:721-731.
• [2]García S, Cofán F, Combalia A, Casas A, Campistol JM, Oppenheime F: Compression of the sciatic nerve in uremic tumor calcinosis. Neurologia 1999, 14:86-89.
• [3]Lin HL, Chen JT, Liu YF, Cho DY: Sciatica caused by pseudomyxoma peritonei. J Chin Med Assoc 2009, 72:39-41.
• [4]He J, Wu B, Zhang W, Ten G: Immediate and short-term pain relief by acute sciatic nerve press: a randomized controlled trial. BMC Anesthesiol 2007, 16:7-4.
• [5]He J, Jiang X, Zhao B, Xu S, Zhang F, Wei P, Chen Q: Acute pressure block of the sciatic nerve relieves clinical pain but not cold pressor pain. The Clinical Journal of Pain 2010, 26:332-338.
• [6]Benson ER, Schutzer SF: Posttraumatic piriformis syndrome: diagnosis and results of operative treatment. J Bone Joint Surg Am 1999, 81:941-949.
• [7]Mullin V, de Rosayro M: Caudal steroid injection for treatment of piriformis syndrome. Anesth Analg 1990, 71:705-707.
• [8]Solheim LF, Siewers P, Paus B: The piriformis muscle syndrome, sciatic nerve entrapment treated with section of the piriformis muscle. Acta Orthop Scand 1981, 52:73-75.
• [9]Chen WS: Bipartite piriformis muscle: an unusual cause of sciatic nerve entrapment. Pain 1994, 58:269-272.
• [10]Meknas K, Christensen A, Johansen O: The internal obturator muscle may cause sciatic pain. Pain 2003, 104:375-380.
• [11]Sayson SC, Ducey JP, Maybrey JB, Wesley RL, Vermilion D: Sciatic entrapment neuropathy associated with an anomalous piriformis muscle. Pain 1994, 59:149-152.
• [12]He J, Wu B, Jiang X, Zhang F, Zhao T, Zhang W: A new analgesic method, two-minute sciatic nerve press, for immediate pain relief in man: a randomized trial. BMC Anesthesiol 2008, 25:8-1.
• [13]He J, Chen Q: General responses to questions regarding acute sciatic nerve pressure for pain relief. Pain Medicine 2010, 11:1139-1140.
• [14]Staud R: Evidence of involvement of central neural mechanisms in generating fibromyalgia pain. Curr Rheumatol Rep. 2002, 4:299-305.
• [15]Sotgiu ML, Biella G, Riva L: A study of early ongoing activity in dorsal horn units following sciatic nerve constriction. Neuroreport 1994, 5:2609-2612.
• [16]Sotgiu ML, Biella G, Riva L: Poststimulus afterdischarges of spinal WDR and NS units in rats with chronic nerve constriction. Neuroreport 1995, 6:1021-1024.
• [17]Sotgiu ML, Biella G: Contribution of central sensitization to the pain-related abnormal activity in neuropathic rats. Somatosens Mot Res 2000, 17:32-38.
• [18]You HJ, Dahl Morch C, Chen J, Arendt-Nielsen L: Simultaneous recordings of wind-up of paired spinal dorsal horn nociceptive neuron and nociceptive flexion reflex in rats. Brain Res 2003, 960:235-245.
• [19]Zheng JH, Chen J, Arendt-Nielsen L: Complexity of tissue injury-induced nociceptive discharge of dorsal horn wide dynamic range neurons in the rat, correlation with the effect of systemic morphine. Brain Res 2004, 1001:143-149.
• [20]Zheng JH, Jian Z, Chen J: Detection of deterministic behavior within the tissue injury-induced persistent firing of nociceptive neurons in the dorsal horn of the rat spinal cord. J Comput Neurosci 2002, 13:23-34.
• [21]Dahlin LB, Shyu BC, Danielsen N, Andersson SA: Effects of nerve compression or ischaemia on conduction properties of myelinated and non-myelinated nerve fibres, An experimental study in the rabbit common peroneal nerve. Acta Physiol Scand 1989, 136:97-105.
• [22]Fern R, Harrison PJ: The contribution of ischaemia and deformation to the conduction block generated by compression of the cat sciatic nerve. Exp Physiol 1994, 79:583-592.
• [23]Gelberman RH, Szabo RM, Williamson RV, Dimick MP: Sensibility testing in peripheral-nerve compression syndromes. An experimental study in humans. J Bone Joint Surg Am 1983, 65:632-638.
• [24]Lundborg G, Dahlin LB: The pathophysiology of nerve compression. Hand Clin. 1992, 8:215-227.
• [25]Macgregor RJ, Sharpless SK, Luttges MW: A pressure vessel model for nerve compression. J Neurol Sci 1975, 24:299-304.
• [26]Ochoa J, Fowler TJ, Gilliatt RW: Anatomical changes in peripheral nerves compressed by a pneumatic tourniquet. J Anat 1972, 113:433-455.
• [27]Powell HC, Myers RR: Pathology of experimental nerve compression. Lab Invest 1986, 55:91-100.
• [28]Le Bars D, Dickenson AH, Besson JM: Diffuse nosious inhibitory control (DNIC). I. Effects on dorsal horn convergent neurons in the rat. Pain 1979, 6:283-304.
• [29]Le Bars D, Dickenson AH, Besson JM: Diffuse nosious inhibitory control (DNIC). II. Lack of effect on non-convergent neurons, supraspinal involvement and theoretical implications. Pain 1979, 6:305-327.
• [30]Geffeney SL, Goodman MB: How we feel: ion channel partnerships that detect mechanical inputs and give rise to touch and pain perception. Neuron 2012, 74:609-619.
• [31]Kang S, Jang JH, Price MP, Gautam M, Benson CJ, Gong H, Welsh MJ, Brennan TJ: Simultaneous disruption of mouse ASIC1a, ASIC2 and ASIC3 genes enhances cutaneous mechanosensitivity. PLoS One 2012, 7:e35225.
• [32]Page AJ, et al.: The ion channel ASIC1 contributes to visceral but not cutaneous mechanoreceptor function. Gastroenterology 2004, 127:1739-1747.
• [33]Page AJ, Brierley SM, Martin CM, Hughes PA, Blackshaw LA: Acid sensing ion channels 2 and 3 are required for inhibiton of visceral nociceptors by benzamil. Pain 2007, 133:150-160.
• [34]Price MP, Thompson RJ, Eshcol JO, Wemmie JA, Benson CJ: Stomatin Modulates Gating of Acid-sensing Ion Channels. J Biol Chem 2004, 279:53886-53891.
• [35]Mogil JS, Breese NM, et al.: Transgenic expression of a dominant-negative ASIC3 subunit leads to increased sensitivity to mechanical and inflammatory stimuli. J Neurosci 2005, 25:9893-9901.
• [36]Alvarez dela Rosa D, Zhang P, Shao D, White F, Canessa CM: Functional implications of the localization and activity of acid-sensitive channels in rat peripheral nervous system. Proc Natl Acad Sci USA 2002, 99:326-331.
• [37]Hanai F, Matsui N, Hongo N: Changes in responses of wide dynamic range neurons in the spinal dorsal horn after dorsal root or dorsal root ganglion compression. Spine 1996, 21:1408-1415.
• [38]Kawasaki M, Ushida T, Tani T, Yamamoto H: Changes of wide dynamic range neuronal responses to mechanical cutaneous stimuli following acute compression of the rat sciatic nerve. J Orthop Sci 2002, 7:111-116.
• [39]Light AR, Perl ER: Peripheral sensory systems. In Periperal neuropathy. Edited by Dyck PJ, Thomas PK. Philadelphia: WB Saunders; 1993:149-163.