Residual spinothalamic tract pathways predict development of central pain after spinal cord injury

Brain

Volumn 131, Issue 9, 2008, Pages 2387-2400

  Wasner, Gunnar ^a,b,c   Lee, Bonsan Bonne ^b,d   Engel, Stella ^b,d   McLachlan, Elspeth ^a,b  

^a NEUROSCIENCE RESEARCH AUSTRALIA   (Australia)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

^c UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

^d PRINCE OF WALES HOSPITAL   (Australia)

Author keywords

Central neuropathic pain; Nociceptive afferents; Sensitization; Spinal cord injury; Spinothalamic tract

Indexed keywords

AMITRIPTYLINE; CAPSAICIN; GABAPENTIN; HISTAMINE; MENTHOL; OXYCODONE; PREGABALIN;

ADULT; AGED; ALLODYNIA; ARTICLE; CHRONIC PAIN; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; HEAT SENSITIVITY; HUMAN; HYPERALGESIA; MALE; MOTOR PERFORMANCE; NERVE FIBER DEGENERATION; NEUROPATHIC PAIN; NOCICEPTION; PRIORITY JOURNAL; SKIN BLOOD VESSEL; SKIN SENSITIZATION; SPINAL CORD INJURY; SPINOTHALAMIC TRACT; STIMULUS RESPONSE; THERMAL EXPOSURE; THERMAL STIMULATION; VASODILATATION;

ADULT; CAPSAICIN; COLD; FEMALE; HEAT; HISTAMINE; HUMANS; MALE; MENTHOL; MIDDLE AGED; NERVE FIBERS; NEURALGIA; NOCICEPTORS; PAIN; PAIN MEASUREMENT; PAIN THRESHOLD; PHYSICAL STIMULATION; PROGNOSIS; SENSATION; SPINAL CORD INJURIES; SPINOTHALAMIC TRACTS;

EID: 50849084474     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awn169     Document Type: Article

References (75)

1. Andrew D, Craig AD. Spinothalamic lamina I neurons selectively sensitive to histamine: a central neural pathway for itch. Nat Neurosci 2001; 4: 72-7.
2. Baron R. Capsaicin and nociception: from basic mechanisms to novel drugs. Lancet 2000; 356: 785-7.
3. Baron R, Saguer M. Postherpetic neuralgia. Are C-nociceptors involved in signalling and maintenance of tactile allodynia? Brain 1993; 116: 1477-96.
4. Baron R, Wasner G, Borgstedt R, Hastedt E, Schulte H, Binder A, et al. Effect of sympathetic activity on capsaicin-evoked pain, hyperalgesia, and vasodilatation. Neurology 1999; 52: 923-32.
5. Beric A, Dimitrijevic MR, Lindblom U. Central dysesthesia syndrome in spinal cord injury patients. Pain 1988; 34: 109-16.
6. Bohannon RW, Smith MB. Interrater reliability of a modified Ashworth scale of muscle spasticity. Phys Ther 1987; 67: 206-7.
7. Boivie J, Leijon G, Johansson I. Central post-stroke pain-a study of the mechanisms through analyses of the sensory abnormalities. Pain 1989; 37: 173-85.
8. Bowsher D, Leijon G, Thuomas KA. Central poststroke pain: correlation of MRI with clinical pain characteristics and sensory abnormalities. Neurology 1998; 51: 1352-8.
9. Campbell JN, Meyer RA. Mechanisms of neuropathic pain. Neuron 2006; 52: 77-92.
10. Caterina MJ, Leffler A, Malmberg AB, Martin WJ, Trafton J, Petersen-Zeitz KR, et al. Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 2000; 288: 306-13.
11. Christensen MD, Hulsebosch CE. Spinal cord injury and anti-NGF treatment results in changes in CGRP density and distribution in the dorsal horn in the rat. Exp Neurol 1997; 147: 463-75.
12. Cowey A. Atrophy of retinal ganglion cells after removal of striate cortex in a rhesus monkey. Perception 1974; 3: 257-60.
13. Defrin R, Ohry A, Blumen N, Urca G. Characterization of chronic pain and somatosensory function in spinal cord injury subjects. Pain 2001; 89: 253-63.
14. Detloff MR, Fisher LC, McGaughy V, Longbrake EE, Popovich PG, Basso DM. Remote activation of microglia and pro-inflammatory cytokines predict the onset and severity of below-level neuropathic pain after spinal cord injury in rats. Exp Neurol 2008 [Epub ahead of print].
15. Dimitrijevic MR. Residual motor functions in spinal cord injury. Adv Neurol 1988; 47: 138-55.
16. Djouhri L, Koutsikou S, Fang X, McMullan S, Lawson SN. Spontaneous pain, both neuropathic and inflammatory, is related to frequency of spontaneous firing in intact C-fiber nociceptors. J Neurosci 2006; 26: 1281-92.
17. Donnelly DJ, Popovich PG. Inflammation and its role in neuroprotection, axonal regeneration and functional recovery after spinal cord injury. Exp Neurol 2008; 209: 378-88.
18. Ducreux D, Attal N, Parker F, Bouhassira D. Mechanisms of central neuropathic pain: a combined psychophysical and fMRI study in syringomyelia. Brain 2006; 129: 963-76.
19. Eide PK, Jorum E, Stenehjem AE. Somatosensory findings in patients with spinal cord injury and central dysaesthesia pain. J Neurol Neurosurg Psychiatry 1996; 60: 411-5.
20. Finnerup NB, Jensen TS. Spinal cord injury pain-mechanisms and treatment. Eur J Neurol 2004; 11: 73-82.
21. Finnerup NB, Johannesen IL, Fuglsang-Frederiksen A, Bach FW, Jensen TS. Sensory function in spinal cord injury patients with and without central pain. Brain 2003; 126: 57-70.
22. Finnerup NB, Otto M, McQuay HJ, Jensen TS, Sindrup SH. Algorithm for neuropathic pain treatment: an evidence based proposal. Pain 2005; 118: 289-305.
23. Finnerup NB, Pedersen LH, Terkelsen AJ, Johannesen IL, Jensen TS. Reaction to topical capsaicin in spinal cord injury patients with and without central pain. Exp Neurol 2007a; 205: 190-200.
24. Finnerup NB, Sorensen L, Biering-Sorensen F, Johannesen IL, Jensen TS. Segmental hypersensitivity and spinothalamic function in spinal cord injury pain. Exp Neurol 2007b; 207: 139-49.
25. Fruhstorfer H, Lindblom U, Schmidt WC. Method for quantitative estimation of thermal thresholds in patients. J Neurol Neurosurg Psychiatry 1976; 39: 1071-5.
26. Gao YJ, Ren WH, Zhang YQ, Zhao ZQ. Contributions of the anterior cingulate cortex and amygdala to pain- and fear-conditioned place avoidance in rats. Pain 2004; 110: 343-53.
27. Hains BC, Saab CY, Waxman SG. Changes in electrophysiological properties and sodium channel Nav1.3 expression in thalamic neurons after spinal cord injury. Brain 2005; 128: 2359-71.
28. Hains BC, Waxman SG. Activated microglia contribute to the maintenance of chronic pain after spinal cord injury. J Neurosci 2006; 26: 4308-17.
29. Hains BC, Waxman SG. Sodium channel expression and the molecular pathophysiology of pain after SCI. Prog Brain Res 2007; 161: 195-203.
30. Johnson H, Cowey A. Transneuronal retrograde degeneration of retinal ganglion cells following restricted lesions of striate cortex in the monkey. Exp Brain Res 2000; 132: 269-75.
31. Krenz NR, Weaver LC. Sprouting of primary afferent fibers after spinal cord transection in the rat. Neuroscience 1998; 85: 443-58.
32. Kuesgen B, Frankel HL, Anand P. Decreased cutaneous sensory axon-reflex vasodilatation below the lesion in patients with complete spinal cord injury. Somatosens Mot Res 2002; 19: 149-52.
33. LaMotte RH, Lundberg LE, Torebjörk HE. Pain, hyperalgesia and activity in nociceptive C units in humans after intradermal injection of capsaicin. J Physiol (Lond) 1992; 448: 749-64.
34. Lenz FA, Kwan HC, Martin R, Tasker R, Richardson RT, Dostrovsky JO. Characteristics of somatotopic organization and spontaneous neuronal activity in the region of the thalamic principal sensory nucleus in patients with spinal cord transection. J Neurophysiol 1994; 72: 1570-87.
35. Lin Q, Wu J, Willis WD. Dorsal root reflexes and cutaneous neurogenic inflammation after intradermal injection of capsaicin in rats. J Neurophysiol 1999; 82: 2602-11.
36. Maynard FM Jr, Bracken MB, Creasey G, Ditunno JF Jr, Donovan WH, Ducker TB, et al. International standards for neurological and functional classification of spinal cord injury. American Spinal Injury Association. Spinal Cord 1997; 35: 266-74.
37. McKay SM, Brooks DJ, Hu P, McLachlan EM. Distinct types of microglial activation in white and grey matter of rat lumbosacral cord after mid-thoracic spinal transection. J Neuropathol Exp Neurol 2007; 66: 698-710.
38. Meller ST, Gebhart GF. Nitric oxide (NO) and nociceptive processing in the spinal cord. Pain 1993; 52: 127-36.
39. Namer B, Seifert F, Handwerker HO, Maihofner C. TRPA1 and TRPM8 activation in humans: effects of cinnamaldehyde and menthol. Neuroreport 2005; 16: 955-9.
40. Österberg A, Boivie J, Thuomas KA. Central pain in multiple sclerosis-prevalence and clinical characteristics. Eur J Pain 2005; 9: 531-42.
41. Parrent AG, Lozano AM, Dostrovsky JO, Tasker RR. Central pain in the absence of functional sensory thalamus. Stereotact Funct Neurosurg 1992; 59: 9-14.
42. Popovich PG, Wei P, Stokes BT. Cellular inflammatory response after spinal cord injury in Sprague-Dawley and Lewis rats. J Comp Neurol 1997; 377: 443-64.
43. Rolke R, Baron R, Maier C, Tolle TR, Treede RD, Beyer A, et al. Quantitative sensory testing in the German Research Network on Neuropathic Pain (DFNS): standardized protocol and reference values. Pain 2006; 123: 231-43.
44. Saab CY, Waxman SG, Hains BC. Alarm or curse? The pain of neuroinflammation. Brain Res Rev 2008; 58: 226-35.
45. Schafers M, Lee DH, Brors D, Yaksh TL, Sorkin LS. Increased sensitivity of injured and adjacent uninjured rat primary sensory neurons to exogenous tumor necrosis factor-alpha after spinal nerve ligation. J Neurosci 2003; 23: 3028-38.
46. Schmelz M. A neural pathway for itch. Nat Neurosci 2001; 4: 9-10.
47. Schmelz M, Michael K, Weidner C, Schmidt R, Torebjörk HE, Handwerker HO. Which nerve fibers mediate the axon reflex flare in human skin? Neuroreport 2000; 11: 645-8.
48. Schmelz M, Schmidt R, Bickel A, Handwerker HO, Torebjörk HE. Specific C-receptors for itch in human skin. J Neurosci 1997; 17: 8003-8.
49. Schmidt R, Schmelz M, Torebjork HE, Handwerker HO. Mechano-insensitive nociceptors encode pain evoked by tonic pressure to human skin. Neuroscience 2000; 98: 793-800.
50. Schmitt AB, Buss A, Breuer S, Brook GA, Pech K, Martin D, et al. Major histocompatibility complex class II expression by activated microglia caudal to lesions of descending tracts in the human spinal cord is not associated with a T cell response. Acta Neuropathol 2000; 100: 528-36.
51. Scholz J, Woolf CJ. The neuropathic pain triad: neurons, immune cells and glia. Nat Neurosci 2007; 10: 1361-8.
52. Sherwood AM, Dimitrijevic MR, McKay WB. Evidence of subclinical brain influence in clinically complete spinal cord injury: discomplete SCI. J Neurol Sci 1992; 110: 90-8.
53. Siddall PJ, McClelland JM, Rutkowski SB, Cousins MJ. A longitudinal study of the prevalence and characteristics of pain in the first 5 years following spinal cord injury. Pain 2003; 103: 249-57.
54. Siddall PJ, Middleton JW. A proposed algorithm for the management of pain following spinal cord injury. Spinal Cord 2006; 44: 67-77.
55. Siddall PJ, Taylor DA, McClelland JM, Rutkowski SB, Cousins MJ. Pain report and the relationship of pain to physical factors in the first 6 months following spinal cord injury. Pain 1999; 81: 187-97.
56. Siddall PJ, Yezierski RP, Loeser JD. Pain following spinal cord injury: clinical features, prevalence and taxonomy. IASP Newsletter 2000; 3: 3-7.
57. Siddall PJ, Yezierski RP, Loeser JD. Taxonomy and epidemiology of spinal cord injury pain. In: Yezierski RP, Burchiel K, editors. Progress in pain research and management, vol. 23. spinal cord injury pain: assessment, mechanisms, management. Seattle: IASP Press; 2002. p. 9-24.
58. Snow BJ, Tsui JK, Bhatt MH, Varelas M, Hashimoto SA, Calne DB. Treatment of spasticity with botulinum toxin: a double-blind study. Ann Neurol 1990; 28: 512-5.
59. Störmer S, Gerner HJ, Gruninger W, Metzmacher K, Follinger S, Wienke C, et al. Chronic pain/dysaesthesiae in spinal cord injury patients: results of a multicentre study. Spinal Cord 1997; 35: 446-55.
60. Szolcsanyi J. Forty years in capsaicin research for sensory pharmacology and physiology. Neuropeptides 2004; 38: 377-84.
61. Vestergaard K, Nielsen J, Andersen G, Ingeman-Nielsen M, Arendt-Nielsen L, Jensen TS. Sensory abnormalities in consecutive, unselected patients with central post-stroke pain. Pain 1995; 61: 177-86.
62. Vierck CJJ, Siddall P, Yezierski RP. Pain following spinal cord injury: animal models and mechanistic studies. Pain 2000; 89: 1-5.
63. Wasner G, Binder A, Kopper F, Baron R. No effect of sympathetic sudomotor activity on capsaicin-evoked ongoing pain and hyperalgesia. Pain 2000; 84: 331-8.
64. Wasner G, Brechot A, Schattschneider J, Allardt A, Binder A, Jensen TS, et al. Effect of sympathetic muscle vasoconstrictor activity on capsaicin-induced muscle pain. Muscle Nerve 2002; 26: 113-21.
65. Wasner G, Brock JA. Determinants of thermal pain thresholds in normal subjects. Clin Neurophysiol 2008 (in press).
66. Wasner G, Naleschinski D, Baron R. A role for peripheral afferents in the pathophysiology and treatment of at-level neuropathic pain in spinal cord injury? A case report. Pain 2007; 131: 219-25.
67. Wasner G, Schattschneider J, Binder A, Baron R. Topical menthol-a human model for cold pain by activation and sensitization of C nociceptors. Brain 2004; 127: 1159-71.
68. Waxman SG, Hains BC. Fire and phantoms after spinal cord injury: Na+ channels and central pain. Trends Neurosci 2006; 29: 207-15.
69. Weaver LC, Verghese P, Bruce JC, Fehlings MG, Krenz NR, Marsh DR. Autonomic dysreflexia and primary afferent sprouting after clip-compression injury of the rat spinal cord. J Neurotrauma 2001; 18: 1107-19.
70. Weng HR, Dougherty PM. Response properties of dorsal root reflexes in cutaneous C fibers before and after intradermal capsaicin injection in rats. Neuroscience 2005; 132: 823-31.
71. Whitton TL, Johnson RW, Lovell AT. Use of the Rydel-Seiffer graduated tuning fork in the assessment of vibration threshold in postherpetic neuralgia patients and healthy controls. Eur J Pain 2005; 9: 167-71.
72. Wu G, Ringkamp M, Hartke TV, Murinson BB, Campbell JN, Griffin JW, et al. Early onset of spontaneous activity in uninjured C-fiber nociceptors after injury to neighboring nerve fibers. J Neurosci 2001; 21: RC140.
73. Yarnitsky D, Ochoa JL. Warm and cold specific somatosensory systems. Psychophysical thresholds, reaction times and peripheral conduction velocities. Brain 1991; 114: 1819-26.
74. Yezierski RP. Spinal cord injury: a model of central neuropathic pain. Neurosignals 2005; 14: 182-93.
75. Zhao P, Waxman SG, Hains BC. Modulation of thalamic nociceptive processing after spinal cord injury through remote activation of thalamic microglia by cysteine cysteine chemokine ligand 21. J Neurosci 2007; 27: 8893-902.