PAIN
Volume 151, Issue 2 , Pages 447-459 , November 2010

Increased excitability and spontaneous activity of rat sensory neurons following in vitro stimulation of sympathetic fiber sprouts in the isolated dorsal root ganglion

  • Wenrui Xie
    • ,
  • Judith A. Strong
    • ,
  • Jun-Ming Zhang

      Affiliations

    • Corresponding Author InformationCorresponding author. Address: Department of Anesthesiology, University of Cincinnati College of Medicine, 231 Albert Sabin Way, P.O. Box 670531, Cincinnati, OH 45267-0531, USA. Tel.: +1 513 558 2427; fax: +1 513 558 0995.

Received 15 December 2009 ,Revised 3 August 2010 ,Accepted 4 August 2010.

References 

  1. Abdulla FA, Smith PA. Ectopic alpha2-adrenoceptors couple to N-type Ca2+ channels in axotomized rat sensory neurons. J Neurosci. 1997;17:1633–1641
  2. AbuRahma AF, Robinson PA, Powell M, Bastug D, Boland JP. Sympathectomy for reflex sympathetic dystrophy: factors affecting outcome. Ann Vasc Surg. 1994;8:372–379
  3. Amir R. Axonal cross-excitation in nerve-end neuromas: comparison of A- and C-fibers. J Neurophysiol. 1992;68:1160–1166
  4. Amir R, Devor M. Chemically mediated cross-excitation in rat dorsal root ganglia. J Neurosci. 1996;16:4733–4741
  5. Amir R, Devor M. Functional cross-excitation between afferent A- and C-neurons in dorsal root ganglia. Neuroscience. 2000;95:189–195
  6. Baron R, Janig W, Kollmann W. Sympathetic and afferent somata projecting in hindlimb nerves and the anatomical organization of the lumbar sympathetic nervous system of the rat. J Comp Neurol. 1988;275:460–468
  7. Blenk KH, Habler HJ, Janig W. Neomycin and gadolinium applied to an L5 spinal nerve lesion prevent mechanical allodynia-like behaviour in rats. Pain. 1997;70:155–165
  8. Broadley KJ. Automonic pharmacology. London: Taylor and Francis; 1996;
  9. Brock JA, Cunnane TC. Studies on the mode of action of bretylium and guanethidine in post-ganglionic sympathetic nerve fibres. Naunyn Schmiedebergs Arch Pharmacol. 1988;338:504–509
  10. Burchiel KJ. Spontaneous impulse generation in normal and denervated dorsal root ganglia: sensitivity to alpha-adrenergic stimulation and hypoxia. Exp Neurol. 1984;85:257–272
  11. Chien SQ, Li C-L, Li H, Xie W, Zhang J-M. Sympathetic fiber sprouting in chronically compressed dorsal root ganglia without peripheral axotomy. J Neuropathic Pain Symptom Palliation. 2005;1:19–23
  12. Chung K, Chung JM. Sympathetic sprouting in the dorsal root ganglion after spinal nerve ligation: evidence of regenerative collateral sprouting. Brain Res. 2001;895:204–212
  13. Chung K, Kim HJ, Na HS, Park MJ, Chung JM. Abnormalities of sympathetic innervation in the area of an injured peripheral nerve in a rat model of neuropathic pain. Neurosic Lett. 1993;162:85–88
  14. Chung K, Lee BH, Yoon YW, Chung JM. Sympathetic sprouting in the dorsal root ganglia of the injured peripheral nerve in a rat neuropathic pain model. J Comp Neurol. 1996;376:241–252
  15. Czeh G, Kudo N, Kuno M. Membrane properties and conduction velocity in sensory neurones following central or peripheral axotomy. J Physiol Lond. 1977;170:165–180
  16. Devor M. Response of nerves to injury in relation to neuropathic pain. In:  McMahon S,  Koltzenburg M editor. Wall and Melzack’s textbook of pain. Philadelphia: Elsevier/Churchill Livingston; 2006;
  17. Devor M. Ectopic discharge in Abeta afferents as a source of neuropathic pain. Exp Brain Res. 2009;196:115–128
  18. Devor M, Janig W, Michaelis M. Modulation of activity in dorsal root ganglion neurons by sympathetic activation in nerve-injured rats. J Neurophysiol. 1994;71:38–47
  19. Djouhri L, Lawson SN. Abeta-fiber nociceptive primary afferent neurons: a review of incidence and properties in relation to other afferent A-fiber neurons in mammals. Brain Res Brain Res Rev. 2004;46:131–145
  20. Gurtu S, Smith PA. Electrophysiological characteristics of hamster dorsal root ganglion cells and their response to axotomy. J Neurophysiol. 1988;59:408–423
  21. Helke CJ, Rabchevsky A. Axotomy alters putative neurotransmitters in visceral sensory neurons of the nodose and petrosal ganglia. Brain Res. 1991;551:44–51
  22. Katz DM. Expression of catecholaminergic characteristics by primary sensory neurons in the normal adult rat in vivo. Proc Natl Acad Sci USA. 1983;80:3526–3530
  23. Kim HJ, Na HS, Sung B, Hong SK. Amount of sympathetic sprouting in the dorsal root ganglia is not correlated to the level of sympathetic dependence of neuropathic pain in a rat model. Neurosci Lett. 1998;245:21–24
  24. Kim SH, Chung JM. An experimental model for peripheral neuropathy produced by segmental spinal nerve ligation in the rat. Pain. 1992;50:355–363
  25. Kim YI, Na HS, Kim SH, Han HC, Yoon YW, Sung B, et al. Cell type-specific changes of the membrane properties of peripherally-axotomized dorsal root ganglion neurons in a rat model of neuropathic pain. Neuroscience. 1998;86:301–309
  26. Kinnman E, Levine JD. Sensory and sympathetic contributions to nerve injury-induced sensory abnormalities in the rat. Neuroscience. 1995;64:751–767
  27. Koerber HR, Druzinsky RE, Mendell LM. Properties of somata of spinal dorsal root ganglion cells differ according to peripheral receptor innervated. J Neurophysiol. 1988;60:1584–1596
  28. Koerber HR, Woodbury CJ. Comprehensive phenotyping of sensory neurons using an ex vivo somatosensory system. Physiol Behav. 2002;77:589–594
  29. Lee BH, Yoon YW, Chung K, Chung JM. Comparison of sympathetic sprouting in sensory ganglia in three animal models of neuropathic pain. Exp Brain Res. 1998;120:432–438
  30. Li H, Xie W, Strong JA, Zhang J-M. Systemic antiinflammatory corticosteroid reduces mechanical pain behavior, sympathetic sprouting, and elevation of proinflammatory cytokines in a rat model of neuropathic pain. Anesthesiology. 2007;107:469–477
  31. Ma C, Shu Y, Zheng Z, Chen Y, Yao H, Greenquist KW, et al. Similar electrophysiological changes in axotomized and neighboring intact dorsal root ganglion neurons. J Neurophysiol. 2003;89:1588–1602
  32. Ma W, Bisby MA. Partial sciatic nerve transection induced tyrosine hydroxidase immunoreactive axon sprouting around both injured and spared dorsal root ganglion neurons which project to the gracile nucleus in middle-aged rats. Neurosci Lett. 1999;275:117–120
  33. Maruo K, Yamamoto H, Yamamoto S, Nagata T, Fujikawa H, Kanno T, et al. Modulation of P2X receptors via adrenergic pathways in rat dorsal root ganglion neurons after sciatic nerve injury. Pain. 2006;120:106–112
  34. McLachlan EM, Jang W, Devor M, Michaelis M. Peripheral nerve injury triggers noradrenergic sprouting within dorsal root ganglia. Nature. 1993;363:543–546
  35. Meisner JG, Waldron JB, Sawynok J. Alpha1-adrenergic receptors augment P2X3 receptor-mediated nociceptive responses in the uninjured state. J Pain. 2007;8:556–562
  36. Nagy I, Urban L, Woolf CJ. Morphological and membrane properties of young rat lumbar and thoracic dorsal root ganglion cells with unmyelinated axons. Brain Res. 1993;609:193–200
  37. Park SK, Chung K, Chung JM. Effects of purinergic and adrenergic antagonists in a rat model of painful peripheral neuropathy. Pain. 2000;87:171–179
  38. Pertin M, Allchorne AJ, Beggah AT, Woolf CJ, Decosterd I. Delayed sympathetic dependence in the spared nerve injury (SNI) model of neuropathic pain. Mol Pain. 2007;3:21
  39. Petersen M, Zhang J, Zhang J-M, LaMotte RH. Abnormal spontaneous activity and responses to norepinephrine in dissociated dorsal root ganglion cells after chronic nerve constriction. Pain. 1996;67:391–397
  40. Price J. An immunohistochemical and quantitative examination of dorsal root ganglion neuronal subpopulations. J Neurosci. 1985;5:2051–2059
  41. Price J, Mudge AW. A subpopulation of rat dorsal root ganglion neurones is catecholaminergic. Nature. 1983;301:241–243
  42. Ramer MS, Bisby MA. Rapid sprouting of sympathetic axons in dorsal root ganglia of rats with a chronic constriction injury. Pain. 1997;70:237–244
  43. Ramer MS, Bisby MA. Differences in sympathetic innervation of mouse DRG following proximal or distal nerve lesions. Exp Neurol. 1998;152:197–207
  44. Ritter AM, Mendell LM. Somal membrane properties of physiologically identified sensory neurons in the rat: effects of nerve growth factor. J Neurophysiol. 1992;68:2033–2041
  45. Roberts WJ. A hypothesis on the physiological basis for causalgia and related pains. Pain. 1986;24:297–311
  46. Shinder V, Govrin-Lippmann R, Cohen S, Belenky M, Ilin P, Fried K, et al. Structural basis of sympathetic-sensory coupling in rat and human dorsal root ganglia following peripheral nerve injury. J Neurocytol. 1999;28:743–761
  47. Sihvonen T, Lindgren KA, Airaksinen O, Leino E, Partanen J, Hanninen O. Dorsal ramus irritation associated with recurrent low back pain and its relief with local anesthetic or training therapy. J Spinal Disord. 1995;8:8–14
  48. Song XJ, Hu SJ, Greenquist KW, Zhang J-M, LaMotte RH. Mechanical and thermal hyperalgesia and ectopic neuronal discharge after chronic compression of dorsal root ganglia. J Neurophysiol. 1999;82:3347–3358
  49. Stebbing MJ, Eschenfelder S, Habler HJ, Acosta MC, Janig W, McLachlan EM. Changes in the action potential in sensory neurones after peripheral axotomy in vivo. Neuroreport. 1999;10:201–206
  50. Takahashi Y, Chiba T, Kurokawa M, Aoki Y, Takahashi K, Yamagata M. Stereoscopic structure of sensory nerve fibers in the lumbar spine and related tissues. Spine [Phila Pa 1976]. 2003;28:871–880
  51. Takahashi Y, Nakajima Y. Dermatomes in the rat limbs as determined by antidromic stimulation of sensory C-fibers in spinal nerves. Pain. 1996;67:197–202
  52. Vega JA. Presence of catecholamine-related enzymes in a subpopulation of primary sensory neurons in dorsal root ganglia of the rat. Cell Mol Biol. 1991;37:519–530
  53. Villiere V, McLachlan EM. Electrophysiological properties of neurons in intact rat dorsal root ganglia classified by conduction velocity and action potential duration. J Neurophysiol. 1996;76:1924–1941
  54. Wiesenfeld-Hallin Z. Partially overlapping territories of nerves to hindlimb foot skin demonstrated by plasma extravasation to antidromic C-fiber stimulation in the rat. Neurosci Lett. 1988;84:261–265
  55. Woodbury CJ, Kullmann FA, McIlwrath SL, Koerber HR. Identity of myelinated cutaneous sensory neurons projecting to nocireceptive laminae following nerve injury in adult mice. J Comp Neurol. 2008;508:500–509
  56. Xie W, Strong JA, Li H, Zhang J-M. Sympathetic sprouting near sensory neurons after nerve injury occurs preferentially on spontaneously active cells and is reduced by early nerve block. J Neurophysiol. 2007;97:492–502
  57. Xie W, Strong JA, Zhang J-M. Sympathetic nerve sprouting is closely related to the pattern of spontaneous activity in axotomized DRG neurons. Soc Neurosci Abstr. 2008;759:2
  58. Xie WR, Deng H, Li H, Bowen TL, Strong JA, Zhang J-M. Robust increase of cutaneous sensitivity, cytokine production and sympathetic sprouting in rats with localized inflammatory irritation of the spinal ganglia. Neuroscience. 2006;142:809–822
  59. Zhang J-M, Song XJ, LaMotte RH. Enhanced excitability of sensory neurons in rats with cutaneous hyperalgesia produced by chronic compression of the dorsal root ganglion. J Neurophysiol. 1999;82:3359–3366
  60. Zhang JM, Strong JA. Recent evidence for activity-dependent initiation of sympathetic sprouting and neuropathic pain. Sheng Li Xue Bao. 2008;60:617–627

PII: S0304-3959(10)00474-4

doi: 10.1016/j.pain.2010.08.006

PAIN
Volume 151, Issue 2 , Pages 447-459 , November 2010

Article Tools

* Image Usage & Resolution