The Journal of Pain
Volume 9, Issue 11 , Pages 1036-1048 , November 2008

Partial Infraorbital Nerve Ligation as a Model of Trigeminal Nerve Injury in the Mouse: Behavioral, Neural, and Glial Reactions

  • Mei Xu

      Affiliations

    • Department of Pharmacology, University of Washington, Seattle, Washington
    • Corresponding Author InformationAddress reprint requests to Dr. Mei Xu, Department of Pharmacology, University of Washington, Seattle, WA 98195-7280
    • ,
  • Megumi Aita

      Affiliations

    • Department of Pharmacology, University of Washington, Seattle, Washington
    • Department of Anesthesiology, University of Washington, Seattle, Washington
    • ,
  • Charles Chavkin

      Affiliations

    • Department of Pharmacology, University of Washington, Seattle, Washington

Received 14 January 2008 ,Revised 5 June 2008 ,Accepted 9 June 2008.

References 

  1. Abbadie C, Brown JL, Mantyh PW, Basbaum AI. Spinal cord substance P receptor immunoreactivity increases in both inflammatory and nerve injury models of persistent pain. Neuroscience. 1996;70:201–209
  2. Anderson LC, von Bartheld CS, Byers MR. NGF depletion reduces ipsilateral and contralateral trigeminal satellite cell reactions after inferior alveolar nerve injury in adult rats. Exp Neurol. 1998;150:312–320
  3. Anderson LC, Vakoula A, Veinote R. Inflammatory hypersensitivity in a rat model of trigeminal neuropathic pain. Arch Oral Biol. 2003;48:161–169
  4. Averill S, Michael GJ, Shortland PJ, Leavesley RC, King VR, Bradbury EJ, et al. NGF and GDNF ameliorate the increase in ATF3 expression which occurs in dorsal root ganglion cells in response to peripheral nerve injury. Eur J Neurosci. 2004;19:1437–1445
  5. Bennett GJ, Xie YK. A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain. 1988;33:87–107
  6. Bongenhielm U, Boissonade FM, Westermark A, Robinson PP, Fried K. Sympathetic nerve sprouting fails to occur in the trigeminal ganglion after peripheral nerve injury in the rat. Pain. 1999;99:567–578
  7. Byers MR, Chudler EH, Iadarola MJ. Chronic tooth pulp inflammation causes transient and persistent expression of Fos in dynorphin-rich regions of rat brainstem. Brain Res. 2000;861:191–207
  8. Callahan BL, Gil AS, Levesque A, Mogil JS. Modulation of mechanical and thermal nociceptive sensitivity in the laboratory mouse by behavioral state. J Pain. 2008;9:174–184
  9. Cameron AA, Cliffer KD, Dougherty PM, Garrison CJ, Willis WD, Carlton SM. Time course of degenerative and regenerative changes in the dorsal horn in a rat model of peripheral neuropathy. J Comp Neurol. 1997;379:428–442
  10. Cherkas PS, Tian-Ying Huang, Pannicke T, Tal M, Richenbach A, Hanani M. The effects of axotomy on neurons and satellite glial cells in mouse trigeminal ganglion. Pain. 2004;110:290–298
  11. Chudler EH, Anderson LC, Byers MR. Trigeminal neuronal activity and glial fibrillary acidic protein immunoreactivity after inferior alveolar nerve crush in the adult rat. Pain. 1997;73:141–149
  12. Chudler EH, Anderson LC. Behavioral and electrophysiological consequences of deafferentation following chronic constriction of the infraorbital nerve in adult rats. Arch Oral Biol. 2002;47:165–172
  13. Clemente JT, Parada CA, Veiga MC, Gear RW, Tambeli CH. Sexual dimorphism in the antinociception mediated by kappa opioid receptors in the rat temporomandibular joint. Neurosci Lett. 2004;372:250–255
  14. Dubner R, Ren K. Brainstem mechanisms of persistent pain following injury. J Orofac Pain. 2004;18:299–305
  15. Fu KY, Light AR, Matsushima GK, Maixner W. Microglial reactions after subcutaneous formalin injection into the rat hind paw. Brain Res. 1999;825:59–67
  16. Fukuoka T, Noguchi K. Contribution of the spared primary afferent neurons to the pathomechanisms of neuropathic pain. Mol Neurobiol. 2002;26:57–67
  17. Gardell LR, Vanderah TW, Gardell SE, Wang R, Ossipov MH, Lai J, et al. Enhanced evoked excitatory transmitter release in experimental neuropathy requires descending facilitation. J Neurosci. 2003;23:8370–8379
  18. Garrison CJ, Dougherty PM, Kajander KC, Carlton SM. Staining of glial fibrillary acidic protein (GFAP) in lumbar spinal cord increases following a sciatic nerve constriction injury. Brain Res. 1991;565:1–7
  19. Garrison CJ, Dougherty PM, Carlton SM. Quantitative analysis of substance P and calcitonin gene-related peptide immunohistochemical staining in the dorsal horn of neuropathic MK-801 treated rats. Brain Res. 1993;607:205–214
  20. Hai T, Hartman MG. The molecular biology and nomenclature of the activating transcription factor/cAMP responsive element binding family of transcription factors: activating transcription factor proteins and homeostasis. Gene. 2001;273:1–11
  21. Hammond DL, Ackerman L, Holdsworth R, Elzey B. Effects of spinal nerve ligation on immunohistochemically identified neurons in the L4 and L5 dorsal root ganglia of the rat. J Comp Neurol. 2004;475:575–589
  22. Henry MA, Freking AR, Johnson LR, Levinson SR. Increased sodium channel immunofluorescence at myelinated and demyelinated sites following an inflammatory and partial axotomy lesion of the rat infraorbital nerve. Pain. 2006;124:222–233
  23. Holland GR. Experimental trigeminal nerve injury. Crit Rev Oral Biol Med. 1996;7:237–258
  24. Imamura Y, Kawamoto H, Nakanishi O. Characterization of heat-hyperalgesia in an experimental trigeminal neuropathy in rats. Exp Brain Res. 1997;116:97–103
  25. Iwata K, Tsuboi Y, Shima A, Harada T, Ren K, Kanda K, et al. Central neuronal changes after nerve injury: Neuroplastic influences of injury and aging. J Orofac Pain. 2004;18:293–298
  26. Jannetta PJ. Arterial compression of the trigeminal nerve at the pons in patients with trigeminal neuralgia. J Neurosurg. 1967;26:159–162
  27. Jessell T, Tsunoo A, Kanazawa I, Otsuka M, Substance P. depletion in the dorsal horn of rat spinal cord after section of the peripheral processes of primary sensory neurons. Brain Res. 1979;168:247–259
  28. Kajander KC, Xu J. Quantitative evaluation of calcitonin gene-related peptide and substance P levels in rat spinal cord following peripheral nerve injury. Neurosci Lett. 1995;186:184–188
  29. Kalla R, Liu Z, Xu S, Koppius A, Imai Y, Kloss CU, et al. Microglia and the early phase of immune surveillance in the axotomized facial motor nucleus: Impaired microglial activation and lymphocyte recruitment but no effect on neuronal survival or axonal regeneration in macrophage-colony stimulating factor-deficient mice. J Comp Neurol. 2001;436:182–201
  30. Kreutzberg GW. Microglia: A sensor for pathological events in the CNS. Trends Neurosci. 1996;19:312–318
  31. Li JL, Ding YQ, Shigemoto R, Mizuno N. Distribution of trigeminothalamic and spinothalamic-tract neurons showing substance P receptor-like immunoreactivity in the rat. Brain Res. 1996;719:207–212
  32. Lim EJ, Jeon HJ, Yang GY, Lee MK, Ju JS, Han SR, et al. Intracisternal administration of mitogen-activated protein kinase inhibitors reduced mechanical allodynia following chronic constriction injury of infraorbital nerve in rats. Prog Neuropsychopharmacol Biol Psychiatry. 2007;1322–132915;31
  33. Malmberg AB, Basbaum AI. Partial sciatic nerve injury in the mouse as a model of neuropathic pain: Behavioral and neuroanatomical correlates. Pain. 1998;76:215–222
  34. Marfurt CF, Rajchert DM. Trigeminal primary afferent projections to ‘non-trigeminal' areas of the rat central nervous system. J Comp Neurol. 1991;303:489–511
  35. Mørch CD, Hu JW, Arendt-Nielsen L, Sessle BJ. Convergence of cutaneous, musculoskeletal, dural and visceral afferents onto nociceptive neurons in the first cervical dorsal horn. Eur J Neurosci. 2007;26:142–154
  36. Narita M, Yoshida T, Nakajima M, Narita M, Miyatake M, Takagi T, et al. Direct evidence for spinal cord microglia in the development of a neuropathic pain-like state in mice. J Neurochem. 2006;97:1337–1348
  37. Nomura H, Ogawa A, Tashiro A, Morimoto T, Hu JW, Iwata K. Induction of Fos protein-like immunoreactivity in the trigeminal spinal nucleus caudalis and upper cervical cord following noxious and non-noxious mechanical stimulation of the whisker pad of the rat with an inferior alveolar nerve transection. Pain. 2002;95:225–238
  38. Obata K, Yamanaka H, Fukuoka T, Yi D, Tokunaga A, Hashimoto N, et al. Contribution of injured and uninjured dorsal root ganglion neurons to pain behavior and the changes in gene expression following chronic constriction injury of the sciatic nerve in rats. Pain. 2003;101:65–77
  39. Ogawa A, Dai Y, Yamanaka H, Iwata K, Niwa H, Noguchi K. Ca (2+)/calmodulin-protein kinase II-alpha in the trigeminal subnucleus caudalis contributes to neuropathic pain following inferior alveolar nerve transection. Exp Neurol. 2005;192:310–319
  40. Piao ZG, Cho IH, Park CK, Hong JP, Choi SY, Lee SJ, et al. Activation of glia and microglial p38 MAPK in medullary dorsal horn contributes to tactile hypersensitivity following trigeminal sensory nerve injury. Pain. 2006;121:219–231
  41. Robinson PP, Boissonade FM, Loescher AR, Smith KG, Yates JM. Peripheral mechanisms for the initiation of pain following trigeminal nerve injury. J Orofacial Pain. 2004;18:287–292
  42. Seltzer Z, Dubner R, Shir Y. A novel behavioral model of neuropathic pain disorders produced in rats by partial sciatic nerve injury. Pain. 1990;43:205–218
  43. Sessle BJ. Orofacial pain. In:  Merskey H,  Loeser JD,  Dubner R editor. The Paths of Pain 1975-2005. Seattle: IASP Press; 2005;p. 131–151
  44. Stephenson JS, Byers MR. GFAP immunoreactivity in trigeminal ganglion satellite cells after tooth injury in rats. Exp Neurol. 1995;131:11–22
  45. Sugiyo S, Takemura M, Dubner R, Ren K. Trigeminal transition zone/rostral ventromedial medulla connections and facilitation of orofacial hyperalgesia after masseter inflammation in rats. J Comp Neurol. 2005;493:510–523
  46. Todd AJ, Puskar Z, Spike RC, Hughes C, Watt C, Forrest L. Projection neurons in lamina I of rat spinal cord with the neurokinin 1 receptor are selectively innervated by substance p-containing afferents and respond to noxious stimulation. J Neurosci. 2002;22:4103–4113
  47. Tsuboi Y, Takeda M, Tanimoto T, Ikeda M, Matsumoto S, Kitagawa J, et al. Alteration of the second branch of the trigeminal nerve activity following inferior alveolar nerve transection in rats. Pain. 2004;111:323–334
  48. Tsujino H, Kondo E, Fukuoka T. Activating transcription factor 3 (ATF3) induction by axotomy in sensory and motoneurons: A novel neuronal marker of nerve injury. Mol Cell Neurosci. 2000;15:170–182
  49. Tsuzuki K, Fukuoka T, Sakagami M, Noguchi K. Increase of preprotachykinin mRNA in the uninjured mandibular neurons after rat infraorbital nerve transection. Neurosci Lett. 2003;345:57–60
  50. Vahidy WH, Ong WY, Farooqui AA, Yeo JF. Effects of intracerebroventricular injections of free fatty acids, lysophospholipids, or platelet activating factor in a mouse model of orofacial pain. Exp Brain Res. 2006;174:781–785
  51. Vos BP, Maciewicz RJ. Behavioral changes following ligation of the infraorbital nerve in rat: An animal model of trigeminal neuropathic pain. In:  Besson JM,  Guilbaud G editor. Lesions of Primary Afferent Fibers as a Tool for the Study of Clinical Pain. Amsterdam: Elsevier; 1991;p. 147–158
  52. Vos BP, Strassman AM, Maciewicz RJ. Behavioral evidence of trigeminal neuropathic pain following chronic constriction injury to the rat's infraorbital nerve. J Neurosci. 1994;14:2708–2723
  53. Vos BP, Hans G, Adriaensen H. Behavioral assessment of facial pain in rats: face grooming patterns after painful and non-painful sensory disturbances in the territory of the rat's infraorbital nerve. Pain. 1998;76:173–178
  54. Watkins LR, Milligan ED, Maier SF. Spinal cord glia: New players in pain. Pain. 2001;93:201–205
  55. Xu M, Bruchas MR, Ippolito DL, Gendron L, Chavkin C. Sciatic nerve ligation-induced proliferation of spinal cord astrocytes is mediated by kappa opioid activation of p38 mitogen-activated protein kinase. J Neurosci. 2007;27:2570–2581
  56. Xu M, Petraschka M, McLaughlin JP, Westenbroek RE, Caron MG, Lefkowitz RJ, et al. Neuropathic pain activates the endogenous kappa opioid system in mouse spinal cord and induces opioid receptor tolerance. J Neurosci. 2004;24:4576–4584

 Supported by USPHS grant DA11672 from the National Institute of Health (NIH) to C.C., by the Treuer Foundation (C.C., M.X.) and by the UW-Anesthesia Research and Training Fund (M.R.B.). M.A. was supported by a fellowship from the Japan Society for the Promotion of Science.

PII: S1526-5900(08)00626-3

doi: 10.1016/j.jpain.2008.06.006

The Journal of Pain
Volume 9, Issue 11 , Pages 1036-1048 , November 2008

Article Tools

* Image Usage & Resolution