Effects of distal nerve injuries on dorsal-horn neurons and glia: Relationships between lesion size and mechanical hyperalgesia

Neuroscience

Volumn 158, Issue 2, 2009, Pages 904-914

  Lee, J W ^a   Siegel, S M ^a   Oaklander, A L ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

astrocyte; axotomy; chronic pain; GABA; rat; spinal cord

Indexed keywords

4 AMINOBUTYRIC ACID; CALCITONIN GENE RELATED PEPTIDE; GLIAL FIBRILLARY ACIDIC PROTEIN; ISOLECTIN B4; SUBSTANCE P;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; COLD SENSITIVITY; CONTROLLED STUDY; DISEASE SEVERITY; GLIA; HYPERALGESIA; MALE; MECHANICAL STIMULATION; NERVE CELL; NERVE FIBER; NERVE FIBER TRANSECTION; NERVE INJURY; NEURALGIA; NONHUMAN; PRIORITY JOURNAL; RAT; SPINAL CORD DORSAL HORN; TIBIAL NERVE; TOUCH;

ANIMALS; AXOTOMY; DISEASE MODELS, ANIMAL; FUNCTIONAL LATERALITY; GAMMA-AMINOBUTYRIC ACID; GLIAL FIBRILLARY ACIDIC PROTEIN; GLYCOPROTEINS; HYPERALGESIA; LECTINS; MALE; NEUROGLIA; PAIN MEASUREMENT; PAIN THRESHOLD; POSTERIOR HORN CELLS; RATS; RATS, SPRAGUE-DAWLEY; SPINAL NERVE ROOTS; TIBIAL NEUROPATHY; TIME FACTORS;

EID: 58149464086     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2008.10.010     Document Type: Article

References (46)

1. Albrecht P.J., Hines S., Eisenberg E., Pud D., Finlay D.R., Connolly M.K., Pare M., Davar G., and Rice F.L. Pathologic alterations of cutaneous innervation and vasculature in affected limbs from patients with complex regional pain syndrome. Pain 120 (2006) 244-266
2. Anseloni V.C., Weng H.R., Terayama R., Letizia D., Davis B.J., Ren K., Dubner R., and Ennis M. Age-dependency of analgesia elicited by intraoral sucrose in acute and persistent pain models. Pain 97 (2002) 93-103
3. Bajrovic F., and Sketelj J. Extent of nociceptive dermatomes in adult rats is not primarily maintained by axonal competition. Exp Neurol 150 (1998) 115-121
4. Bennett G.J., and Xie Y.K. A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain 33 (1988) 87-107
5. Chaplan S.R., Bach F.W., Pogrel J.W., Chung J.M., and Yaksh T.L. Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods 53 (1994) 55-63
6. Choi Y., Yoon Y.W., Na H.S., Kim S.H., and Chung J.M. Behavioral signs of ongoing pain and cold allodynia in a rat model of neuropathic pain. Pain 59 (1994) 369-376
7. Colburn R.W., DeLeo J.A., Rickman A.J., Yeager M.P., Kwon P., and Hickey W.F. Dissociation of microglial activation and neuropathic pain behaviors following peripheral nerve injury in the rat. J Neuroimmunol 79 (1997) 163-175
8. Decosterd I., and Woolf C.J. Spared nerve injury: an animal model of persistent peripheral neuropathic pain. Pain 87 (2000) 149-158
9. DeLeo J.A., Rutkowski M.D., Stalder A.K., and Campbell I.L. Transgenic expression of TNF by astrocytes increases mechanical allodynia in a mouse neuropathy model. Neuroreport 11 (2000) 599-602
10. Devor M., and Claman D. Mapping and plasticity of acid phosphatase afferents in the rat dorsal horn. Brain Res 190 (1980) 17-28
11. Dey D.D., Landrum O., and Oaklander A.L. Central neuropathic itch from spinal-cord cavernous hemangioma: a human case, a possible animal model, and hypotheses about pathogenesis. Pain 113 (2005) 233-237
12. Eaton M.J., Plunkett J.A., Karmally S., Martinez M.A., and Montanez K. Changes in GAD- and GABA-immunoreactivity in the spinal dorsal horn after peripheral nerve injury and promotion of recovery by lumbar transplant of immortalized serotonergic precursors. J Chem Neuroanat 16 (1998) 57-72
13. Forrest S.L., and Keast J.R. Expression of receptors for glial cell line-derived neurotrophic factor family ligands in sacral spinal cord reveals separate targets of pelvic afferent fibers. J Comp Neurol 506 (2008) 989-1002
14. Garrison C.J., Dougherty P.M., Kajander K.C., and Carlton S.M. Staining of glial fibrillary acidic protein (GFAP) in lumbar spinal cord increases following a sciatic nerve constriction injury. Brain Res 565 (1991) 1-7
15. Gonzalez H.L., Carmichael N., Dostrovsky J.O., and Charlton M.P. Evaluation of the time course of plasma extravasation in the skin by digital image analysis. J Pain 6 (2005) 681-688
16. Hajos F., Csillik B., and Knyihar-Csillik E. Alterations in glial fibrillary acidic protein immunoreactivity in the upper dorsal horn of the rat spinal cord in the course of transganglionic degenerative atrophy and regenerative proliferation. Neurosci Lett 117 (1990) 8-13
17. Hama A.T., and Borsook D. Behavioral and pharmacological characterization of a distal peripheral nerve injury in the rat. Pharmacol Biochem Behav 81 (2005) 170-181
18. Horowitz S.H. Peripheral nerve injury and causalgia secondary to routine venipuncture. Neurology 44 (1994) 962-964
19. Ibuki T., Hama A.T., Wang X.T., Pappas G.D., and Sagen J. Loss of GABA-immunoreactivity in the spinal dorsal horn of rats with peripheral nerve injury and promotion of recovery by adrenal medullary grafts. Neuroscience 76 (1997) 845-858
20. Jones D.L., and Sorkin L.S. Systemic gabapentin and S(+)-3-isobutyl-gamma-aminobutyric acid block secondary hyperalgesia. Brain Res 810 (1998) 93-99
21. Kapadia S.E., and LaMotte C.C. Deafferentation-induced alterations in the rat dorsal horn: I. Comparison of peripheral nerve injury vs. rhizotomy effects on presynaptic, postsynaptic, and glial processes. J Comp Neurol 266 (1987) 183-197
22. Kim S.H., and Chung J.M. An experimental model for peripheral neuropathy produced by segmental spinal nerve ligation in the rat. Pain 50 (1992) 355-363
23. Ledeboer A., Liu T., Shumilla J.A., Mahoney J.H., Vijay S., Gross M.I., Vargas J.A., Sultzbaugh L., Claypool M.D., Sanftner L.M., Watkins L.R., and Johnson K.W. The glial modulatory drug AV411 attenuates mechanical allodynia in rat models of neuropathic pain. Neuron Glia Biol 2 (2006) 279-291
24. Lee B.H., Won R., Baik E.J., Lee S.H., and Moon C.H. An animal model of neuropathic pain employing injury to the sciatic nerve branches. Neuroreport 11 (2000) 657-661
25. Liu L., Rudin M., and Kozlova E.N. Glial cell proliferation in the spinal cord after dorsal rhizotomy or sciatic nerve transection in the adult rat. Exp Brain Res 131 (2000) 64-73
26. Miletic G., Draganic P., Pankratz M.T., and Miletic V. Muscimol prevents long-lasting potentiation of dorsal horn field potentials in rats with chronic constriction injury exhibiting decreased levels of the GABA transporter GAT-1. Pain 105 (2003) 347-353
27. Moore K.A., Kohno T., Karchewski L.A., Scholz J., Baba H., and Woolf C.J. Partial peripheral nerve injury promotes a selective loss of GABAergic inhibition in the superficial dorsal horn of the spinal cord. J Neurosci 22 (2002) 6724-6731
28. Murray M., Wang S.D., Goldberger M.E., and Levitt P. Modification of astrocytes in the spinal cord following dorsal root or peripheral nerve lesions. Exp Neurol 110 (1990) 248-257
29. Oaklander A.L. The density of remaining nerve endings in human skin with and without postherpetic neuralgia after shingles. Pain 92 (2001) 139-145
30. Oaklander A.L., Rissmiller J.G., Gelman L.B., Zheng L., Chang Y., and Gott R. Evidence of focal small-fiber axonal degeneration in complex regional pain syndrome-I (reflex sympathetic dystrophy). Pain 120 (2006) 235-243
31. Polgár E., Hughes D.I., Riddell J.S., Maxwell D.J., Puskar Z., and Todd A.J. Selective loss of spinal GABAergic or glycinergic neurons is not necessary for development of thermal hyperalgesia in the chronic constriction injury model of neuropathic pain. Pain 104 (2003) 229-239
32. Roberts L.A., Beyer C., and Komisaruk B.R. Nociceptive responses to altered GABAergic activity at the spinal cord. Life Sci 39 (1986) 1667-1674
33. Shields S.D., Eckert III W.A., and Basbaum A.I. Spared nerve injury model of neuropathic pain in the mouse: a behavioral and anatomic analysis. J Pain 4 (2003) 465-470
34. Siegel S.M., Lee J.W., and Oaklander A.L. Needlestick distal nerve injury in rats models symptoms of complex regional pain syndrome. Anesth Analg 105 (2007) 1820-1829
35. Somers D.L., and Clemente F.R. Dorsal horn synaptosomal content of aspartate, glutamate, glycine and GABA are differentially altered following chronic constriction injury to the rat sciatic nerve. Neurosci Lett 323 (2002) 171-174
36. Sommer C., and Schafers M. Painful mononeuropathy in C57BL/Wld mice with delayed wallerian degeneration: differential effects of cytokine production and nerve regeneration on thermal and mechanical hypersensitivity. Brain Res 784 (1998) 154-162
37. Swett J.E., and Woolf C.J. The somatotopic organization of primary afferent terminals in the superficial laminae of the dorsal horn of the rat spinal cord. J Comp Neurol 231 (1985) 66-77
38. Tal M., and Bennett G.J. Extra-territorial pain in rats with a peripheral mononeuropathy: mechano-hyperalgesia and mechano-allodynia in the territory of an uninjured nerve. Pain 57 (1994) 375-382
39. Todd A.J., and Sullivan A.C. Light microscope study of the coexistence of GABA-like and glycine-like immunoreactivities in the spinal cord of the rat. J Comp Neurol 296 (1990) 496-505
40. van der Laan L., ter Laak H.J., Gabreels-Festen A., Gabreels F., and Goris R.J. Complex regional pain syndrome type I (RSD): pathology of skeletal muscle and peripheral nerve. Neurology 51 (1998) 20-25
41. Vierck C.J., Hansson P.T., and Yezierski R.P. Clinical and pre-clinical pain assessment: are we measuring the same thing?. Pain 135 (2008) 7-10
42. Villar M.J., Cortes R., Theodorsson E., Wiesenfeld-Hallin Z., Schalling M., Fahrenkrug J., Emson P.C., and Hokfelt T. Neuropeptide expression in rat dorsal root ganglion cells and spinal cord after peripheral nerve injury with special reference to galanin. Neuroscience 33 (1989) 587-604
43. Watkins L.R., Martin D., Ulrich P., Tracey K.J., and Maier S.F. Evidence for the involvement of spinal cord glia in subcutaneous formalin induced hyperalgesia in the rat. Pain 71 (1997) 225-235
44. Yamamoto T., and Yaksh T.L. Effects of intrathecal strychnine and bicuculline on nerve compression-induced thermal hyperalgesia and selective antagonism by MK-801. Pain 54 (1993) 79-84
45. Zelenka M., Schafers M., and Sommer C. Intraneural injection of interleukin-1beta and tumor necrosis factor-alpha into rat sciatic nerve at physiological doses induces signs of neuropathic pain. Pain 111 (2005) 257-263
46. Zimmermann M. Ethical guidelines for investigations of experimental pain in conscious animals. Pain 16 (1983) 109-110