Differential pain modulation properties in central neuropathic pain after spinal cord injury

Pain

Volumn 157, Issue 7, 2016, Pages 1415-1424

  Gruener, Hila ^a   Zeilig, Gabi ^a,b   Laufer, Yocheved ^c   Blumen, Nava ^a,b   Defrin, Ruth ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b SHEBA MEDICAL CENTER   (Israel)

^c UNIVERSITY OF HAIFA   (Israel)

Author keywords

Central neuropathic pain; Descending inhibition, hyperexcitability, mechanism; Spinal cord injury

Indexed keywords

ADULT; ARTICLE; BODY REGIONS; CENTRAL NEUROPATHIC PAIN; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; HUMAN; MALE; NERVE CELL EXCITABILITY; NEUROPATHIC PAIN; PAIN MEASUREMENT; PRIORITY JOURNAL; QUESTIONNAIRE; SPATIAL SUMMATION; SPINAL CORD INJURY; SPINOTHALAMIC TRACT; ADAPTATION; CHRONIC PAIN; COMPLICATION; MIDDLE AGED; NEURALGIA; PAIN THRESHOLD; PATHOPHYSIOLOGY; PHYSICAL STIMULATION; PHYSIOLOGY;

ADAPTATION, PHYSIOLOGICAL; ADULT; CHRONIC PAIN; FEMALE; HUMANS; MALE; MIDDLE AGED; NEURALGIA; PAIN MEASUREMENT; PAIN THRESHOLD; PHYSICAL STIMULATION; SPINAL CORD INJURIES; SPINOTHALAMIC TRACTS;

EID: 84976361898     PISSN: 03043959     EISSN: 18726623     Source Type: Journal    
DOI: 10.1097/j.pain.0000000000000532     Document Type: Article

References (81)

1. Albu S, Go?mez-Soriano J, Avila-Martin G, Taylor J. Deficient conditioned pain modulation after spinal cord injury correlates with clinical spontaneous pain measures. PAIN 2015; 156: 260-72
2. Arendt-Nielsen L, Egsgaard LL, Petersen KK, Eskehave TN, Graven-Nielsen T, Hoeck HC, Simonsen OH. Amechanism-based pain sensitivity index to characterize knee osteoarthritis patients with different disease stages and pain levels. Eur J Pain 2015; 19: 1406-17
3. Arendt-Nielsen L, Nie H, Laursen MB, Laursen BS, Madeleine P, Simonsen OH, Graven-Nielsen T. Sensitization in patients with painful knee osteoarthritis. PAIN 2010; 149: 573-81
4. Attal N, Mazaltarine G, Perrouin-Verbe B, Albert T. Chronic neuropathic pain management in spinal cord injury patients. What is the efficacy of pharmacological treatments with a general mode of administration? (oral, transdermal, intravenous). Ann Phys Rehabil Med 2009; 52: 124-41
5. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B 1995; 57: 289-300
6. Bingel U, Herken W, Teutsch S, May A. Habituation to painful stimulation involves the antinociceptive system-A 1-year follow-up of 10 participants. PAIN 2008; 140: 393-4
7. Boroujerdi A, Zeng J, Sharp K, Kim D, Steward O, Luo ZD. Calcium channel alpha-2-delta-1 protein upregulation in dorsal spinal cord mediates spinal cord injury-induced neuropathic pain states. PAIN 2011; 152: 649-55
8. Bouhassira D, Attal N, Brasseur L, Parker F. Quantitative sensory testing in patients with painful or painless syringomyelia. In: Devor M, Rowbotham MC, Wiesenfeld-Hallin Z, editors. Proc. 9th World Congress on Pain. Seattle: IASP Press, 2000. p. 401-10
9. Bowsher D. Central pain: clinical and physiological characteristics. J Neurol Neurosurg Psychiatry 1996; 61: 62-9
10. Brewer KL, McMillan D, Nolan T, Shum K. Cortical changes in cholecystokinin mRNA are related to spontaneous pain behaviors following excitotoxic spinal cord injury in the rat. Brain Res Mol Brain Res 2003; 118: 171-4
11. Campbell JN, Meyer RA. Sensitization of unmyelinated nociceptive afferents in monkey varies with skin type. J Neurophysiol 1983; 49: 98-110
12. Cardenas DD, Felix ER. Pain after spinal cord injury: a review of classification, treatment approaches, and treatment assessment. PM R 2009; 1: 1077-90
13. Coghill RC, Mayer DJ, Price DD. Wide dynamic range but not nociceptive-specific neurons encode multidimensional features of prolonged repetitive heat pain. J Neurophysiol 1993; 69: 703-16
14. Coste J, Voisin DL, Luccarini P, Dallel R. A role for wind-up in trigeminal sensory processing: intensity coding of nociceptive stimuli in the rat. Cephalalgia 2008; 28: 631-9
15. 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
16. Defrin R, Riabinin M, Feingold Y, Schreiber S, Pick CG. Deficient pain modulatory systems in patients with mild traumatic brain and chronic post-Traumatic headache: implications for its mechanism. J Neurotrauma 2015; 32: 28-37
17. Defrin R, Urca G. Spatial summation of heat pain: a reassessment. PAIN 1996; 66: 23-9
18. Desbois C, Le Bars D, Villanueva L. Organization of cortical projections to the medullary subnucleus reticularis dorsalis: a retrograde and anterograde tracing study in the rat. J Comp Neurol 1999; 410: 178-96
19. Dostrovsky JO, Craig AD. The thalamus and pain. In: McMahon S, Koltzenburg M, editors. Wall and Melzack?s textbook of pain. Oxford: Churchill Livingston, 2009. p. 194-9
20. 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
21. Dutton RC, Cuellar JM, Eger EI, Antognini JF, Carstens E. Temporal and spatial determinants of sacral dorsal horn neuronal windup in relation to isoflurane-induced immobility. Anesth Analg 2007; 105: 1665-74
22. Edgar RE, Best LG, Quail PA, Obert AD. Computer-Assisted DREZ microcoagulation: posttraumatic spinal deafferentation pain. J Spinal Disord 1993; 6: 48-56
23. Eide PK, Jorum E, Stenehjem AE. Somatosensory findings in patients with spinal cord injury and central dysaesthesia pain. J Neurol Neurosurg Psychiat 1996; 60: 411-5
24. Endo T, Spenger C, Westman E, Tominaga T, Olson L. Reorganization of sensory processing below the level of spinal cord injury as revealed by fMRI. Exp Neurol 2008; 209: 155-60
25. Finnerup NB, Johannesen IL, Fuglsang-Frederiksen A, Bach FW, Jensen TS. Sensory function in spinal cord injury patientswith and without central pain. Brain 2003; 126: 57-70
26. Finnerup NB, Norrbrink C, Trok K, Piehl F, Johannesen IL, SØrensen JC, Jensen TS, Werhagen L. Phenotypes and predictors of pain following traumatic spinal cord injury: a prospective study. J Pain 2014; 15: 40-8
27. Finnerup NB, Otto M, McQuay HJ, Jensen TS, Sindrup SH. Algorithm for neuropathic pain treatment: an evidence based proposal. PAIN 2005; 118: 289-305
28. Finnerup NB, SØrensen L, Biering-SØrensen F, Johannesen IL, Jensen TS. Segmental hypersensitivity and spinothalamic function in spinal cord injury. Exp Neurol 2007; 207: 139-49
29. Gerke MB, Duggan AW, Xu L, Siddall PJ. Thalamic neuronal activity in rats with mechanical allodynia following contusive spinal cord injury. Neurosci 2003; 117: 715-22
30. Geva N, Defrin R. Enhanced pain modulation among triathletes: a possible explanation for their exceptional capabilities. PAIN 2013; 154: 2317-23
31. Granot M, Weissman-Fogel I, Crispel Y, Pud D, Granovsky Y, Sprecher E, Yarnitsky D. Determinants of endogenous analgesia magnitude in a diffuse noxious inhibitory control (DNIC) paradigm: do conditioning stimulus painfulness, gender and personality variables matter? PAIN 2008; 136: 142-9
32. Gustin SM, Wrigley PJ, Siddall PJ, Henderson LA. Brain anatomy changes associated with persistent neuropathic pain following spinal cord injury. Cereb Cortex 2010; 20: 1409-19
33. Gustin SM, Wrigley PJ, Youssef AM, McIndoe L, Wilcox SL, Rae CD, Edden RA, Siddall PJ, Henderson LA. Thalamic activity and biochemical change in individuals with neuropathic pain after spinal cord injury. PAIN 2014; 155: 1027-36
34. Gwak YS, Crown ED, Unabia GC, Hulsebosch CE. Propentofylline attenuates allodynia, glial activation and modulates GABAergic tone after spinal cord injury in the rat. PAIN 2008; 138: 410-22
35. Gwak YS, Kim HK, Kim HY, Leem JW. Bilateral hyperexcitability of thalamic VPL neurons following unilateral spinal injury in rats. J Physiol Sci 2010; 60: 59-66
36. Gwak YS, Tan HY, Nam TS, Paik KS, Hulsebosch CE, Leem JW. Activation of spinal GABA receptors attenuates chronic central neuropathic pain after spinal cord injury. J Neurotrauma 2006; 23: 1111-24
37. Hains BC, Klein JP, Saab CY, Craner MJ, Black JA, Waxman SG. Upregulation of sodium channel Nav1.3 and functional involvement in neuronal hyperexcitability associated with central neuropathic pain after spinal cord injury. J Neurosci 2003; 23: 8881-92
38. Hains BC, Saab CY, Waxman SG. Changes in electrophysiological properties and sodium channel Nav1.3 expression in thalamicneurons after spinal cord injury. Brain 2005; 128: 2359-71
39. Hains BC, Waxman SG. Activated microglia contribute to the maintenance of chronic pain after spinal cord injury. J Neurosci 2006; 26: 4308-17
40. Hains BC, Waxman SG. Sodium channel expression and the molecular pathophysiology of pain after SCI. Prog Brain Res 2007; 161: 195-203
41. Heinricher MM, Fields HL. Central nervous system mechanisms of pain modulation. In: Wall and Melzack?s textbook of pain, 6th edition. Saunders: Elsevier Ltd, 2013. p. 129-42
42. Kenshalo DR, Leonard RB, Chung JM, Willis WD. Responses of primate spinothalamic neurons to graded and to repeated noxious heat stimuli. J Neurophysiol 1979; 42: 1370-89
43. Kjerulf TD, Loeser JD. Neuronal hyperactivity following deafferentation of the lateral cuneate nucleus. Exp Neurol 1973; 39: 70-85
44. Kumru H, Soler D, Vidal J, Tormos JM, Pascual-Leone A, Valls-Sole J. Evoked potentials and quantitative thermal testing in spinal cord injury patients with chronic neuropathic pain. Clin Neurophysiol 2012; 123: 598-604
45. Lenz FA, Tasker RR, Dostrovsky JO, Kwan HC, Gorecki J, Hirayama T, Murphy JT. Abnormal single-unit activity recorded in the somatosensory thalamus of a quadriplegic patient with central pain. PAIN 1987; 31: 225-36
46. 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
47. Lewis GN, Rice DA, McNair PJ. Conditioned pain modulation in populations with chronic pain: a systematic review and meta-Analysis. J Pain 2012; 13: 936-44
48. Loeser JD, Ward AA Jr, White LE Jr. Chronic deafferentation of human spinal cord neurons. J Neurosurg 1968; 29: 48-50
49. Lotze M, Flor H, Grodd W, Larbig W, Birbaumer N. Phantom movements and pain. An fMRI study in upper limb amputees. Brain 2001; 124: 2268-77
50. Masri R, Quiton RL, Lucas JM, Murray PD, Thompson SM, Keller A. Zona incerta: a role in central pain. J Neurophysiol 2009; 102: 181-91
51. Melzack R. The McGill Pain Questionnaire: major properties and scoring methods. PAIN 1975; 1: 277-99
52. Murray PD, Masri R, Keller A. Abnormal anterior pretectal nucleus activity contributes to central pain syndrome. J Neurophysiol 2010; 103: 3044-53
53. Nahman-Averbuch H, Yarnitsky D, Granovsky Y, Sprecher E, Steiner M, Tzuk-Shina T, Pud D. Pronociceptive pain modulation in patients with painful chemotherapy-induced polyneuropathy. J Pain Symptom Manage 2011; 42: 229-38
54. Nathan PW, Smith MC, Cook AW. Sensory effects in man of lesions of the posterior columns and of some other afferent pathways. Brain 1986; 109: 1003-41
55. Normand E, Potvin S, Gaumond I, Cloutier G, Corbin JF, Marchand S. Pain inhibition is deficient in chronic widespread pain but normal in major depressive disorder. J Clin Psychiatry 2011; 72: 219-24
56. Pattany PM, Yezierski RP, Widerström-Noga EG, Bowen BC, Martinez-Arizala A, Garcia BR, Quencer RM. Proton magnetic resonance spectroscopy of the thalamus in patients with chronic neuropathic pain after spinal cord injury. Am J Neuroradiol 2002; 23: 901-5
57. Peng YB, RingkampM, Meyer RA, Campbell JN. Fatigue and paradoxical enhancement of heat response in C-fiber nociceptors from cross-modal excitation. J Neurosci 2003; 23: 4766-74
58. Sandkuhler J, Chen JG, Cheng G, Randic M. Low-frequency stimulation of afferent Adelta-fibers induces long-Term depression at primary afferent synapses with substantia gelatinosa neurons in the rat. J Neurosci 1997; 17: 6483-91
59. Siddall PJ. Management of neuropathic pain following spinal cord injury: now and in the future. Spinal Cord 2009; 47: 352-9
60. Siddall PJ, Middleton JW. A proposed algorithm for the management of pain following spinal cord injury. Spinal Cord 2006; 44: 67-77
61. 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
62. 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
63. Staud R, Cannon RC, Mauderli AP, Robinson ME, Price DD, Vierck CJ Jr. Temporal summation of pain from mechanical stimulation of muscle tissue in normal controls and subjects with fibromyalgia syndrome. PAIN 2003; 102: 87-95
64. Staud R, Weyl EE, Riley JL III, Fillingim RB. Slow temporal summation of pain for assessment of central pain sensitivity and clinical pain of fibromyalgia patients. PLoS One 2014; 9: e89086
65. Störmer S, Gerner HJ, Gruninger W, Metzmacher K, Follinger S, Wienke C, Aldinger W, Walker N, Zimmermann M, Paeslack V. Chronic pain/dysaesthesia in spinal cord injury patients: results of a multicentre study. Spinal Cord 1997; 35: 446-55
66. Teasell RW, Mehta S, Aubut JA, Foulon B, Wolfe DL, Hsieh JT, Townson AF, Short C; Spinal Cord Injury Rehabilitation Evidence Research Team. A systematic review of pharmacologic treatments of pain after spinal cord injury. Arch Phys Med Rehabil 2010; 91: 816-31
67. van Wijk G, Veldhuijzen DS. Perspective on diffuse noxious inhibitory controls as a model of endogenous pain modulation in clinical pain syndromes. J Pain 2010; 11: 408-19
68. Villanueva L, Bouhassira D, Le Bars D. The medullary subnucleus reticularis dorsalis (SRD) as a key link in both the transmission and modulation of pain signals. PAIN 1996; 67: 231-40
69. Wasner G, Lee BB, Engel S, McLachlan E. Residual spinothalamic tract pathways predict development of central pain after spinal cord injury. Brain 2008; 131: 2387-400
70. Weissman-Fogel I, Dror A, Defrin R. Temporal and spatial aspects of experimental tonic pain: understanding pain adaptation and intensification. Eur J Pain 2015; 19: 408-18
71. Weissman-Fogel I, Sprecher E, Granovsky Y, Yarnitsky D. Repeated noxious stimulation of the skin enhances cutaneous pain perception of migraine patients in-between attacks: clinical evidence for continuous sub-Threshold increase in membrane excitability of central trigeminovascular neurons. PAIN 2003; 104: 693-700
72. Werhagen L, Budh CN, Hultling C, Molander C. Neuropathic pain after traumatic spinal cord injury-relations to gender, spinal level, completeness, and age at the time of injury. Spinal Cord 2004; 42: 665-73
73. Widerström-Noga E, Biering-SØrensen F, Bryce T, Cardenas DD, Finnerup NB, Jensen MP, Richards JS, Siddall PJ. The international spinal cord injury pain basic data set. Spinal Cord 2008; 46: 818-23
74. Wiesenfeld-Hallin Z, Aldskogius H, Grant G, Hao JX, Hökfelt T, Xu XJ. Central inhibitory dysfunctions: mechanisms and clinical implications. Behave Brain Sci 1997; 20: 420-5
75. Willis WD, Westlund KN. Neuroanatomy of the pain system and of the pathways that modulate pain. J Clin Neurophysiol 1997; 14: 2-31
76. Wrigley PJ, Press SR, Gustin SM, Macefield VG, Gandevia SC, Cousins MJ, Middleton JW, Henderson LA, Siddall PJ. Neuropathic pain and primary somatosensory cortex reorganization following spinal cord injury. PAIN 2009; 141: 52-9
77. Yarnitsky D. Conditioned pain modulation (the diffuse noxious inhibitory control-like effect): its relevance for acute and chronic pain states. Curr Opin Anaesthesiol 2010; 23: 611-5
78. Yarnitsky D, Granot M, Nahman-Averbuch H, Khamaisi M, Granovsky Y. Conditioned pain modulation predicts duloxetine efficacy in painful diabetic neuropathy. PAIN 2012; 153: 1193-8
79. Yezierski RP, Park SH. The mechanosensitivity of spinal sensory neurons following intraspinal injections of quisqualic acid in the rat. Neurosci Lett 1993; 157: 115-19
80. Zeilig G, Enosh S, Rubin-Asher D, Lehr B, Defrin R. The nature and course of sensory changes following spinal cord injury: predictive properties and implications on the mechanism of central pain. Brain 2012; 135: 418-30
81. Zhang AL, Hao JX, Seiger A, Xu XJ, Wiesenfeld-Hallin Z, Grant G, Aldskogius H. Decreased GABA immunoreactivity in spinal cord dorsal horn neurons after transient spinal cord ischemia in the rat. Brain Res 1994; 656: 187-90