Mechanisms and models of spinal cord stimulation for the treatment of neuropathic pain

Brain Research

Volumn 1569, Issue , 2014, Pages 19-31

  Zhang, Tianhe C ^a   Janik, John J ^c   Grill, Warren M ^a,b  

^a Duke University   (United States)

^b DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Stryker Orthopaedics   (United States)

Author keywords

Chronic pain; Pain processing circuits; Spinal cord stimulation

Indexed keywords

ANALGESIA; BEYOND THE PAIN GATE; CLINICAL PRACTICE; COMPLEX REGIONAL PAIN SYNDROME; COMPUTER SIMULATION; ELECTROENCEPHALOGRAM; ELECTROSTIMULATION; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GATE CONTROL THEORY; NERVOUS SYSTEM PARAMETERS; NEUROPATHIC PAIN; NONHUMAN; PAIN MATRIX; PHANTOM PAIN; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; REVIEW; SPINAL CORD DORSAL HORN; SPINAL CORD INJURY; SPINAL CORD STIMULATION; ANIMAL; BIOLOGICAL MODEL; BRAIN; CHRONIC PAIN; ELECTROSTIMULATION THERAPY; HUMAN; NEURALGIA; PATHOPHYSIOLOGY; SPINAL CORD;

ANIMALIA;

ANIMALS; BRAIN; CHRONIC PAIN; ELECTRIC STIMULATION THERAPY; HUMANS; MODELS, NEUROLOGICAL; NEURALGIA; SPINAL CORD;

EID: 84901802586     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2014.04.039     Document Type: Review

References (121)

1. D. Abejon, E. Reg, C.d. Pozo, R. Contreras, and J. Insausti Dual spinal cord stimulation for complex pain: preliminary study Neuromodulation 8 2005 105 111
2. P. Aguiar, M. Sousa, and D. Lima NMDA channels together with L-type calcium currents and calcium-activated nonspecific cationic currents are sufficient to generate windup in WDR neurons J. Neurophysiol. 104 2010 1155 1166
3. Al-Kaisy A.; Van Buyten J.-P.; Smet I.; Palmisani S.; Pang D.; Smith T.; 2014. Sustained effectiveness of 10 kHz high-frequency spinal cord stimulation for patients with chronic, low back pain: 24-month results of a prospective multicenter study. Pain medicine n/a-n/a.
4. K.M. Aló, and J. Holsheimer New trends in neuromodulation for the management of neuropathic pain Neurosurgery 50 2002 690 704
5. K.M. Alo, V. Redko, and J. Charnov Four year follow-up of dual electrode spinal cord stimulation for chronic pain Neuromodulation 5 2002 79 88
6. H. Bantli, J. Bloedel, and P. Thienprasit Supraspinal interactions resulting from experimental dorsal column stimulation J. Neurosurg. Pediatr. 42 1975 296 300
7. J. Barchini, S. Tchachaghian, F. Shamaa, S. Jabbur, B. Meyerson, Z. Song, B. Linderoth, and N. Saade Spinal segmental and supraspinal mechanisms underlying the pain-relieving effects of spinal cord stimulation: an experimental study in a rat model of neuropathy Neuroscience 215 2012 196 208
8. D. Bleakman, A. Alt, and E.S. Nisenbaum Glutamate receptors and pain Semin. Cell Dev. Biol. 17 2006 592 604
9. A. Blomqvist, and A.D. Craig Is neuropathic pain caused by the activation of nociceptive-specific neurons due to anatomic sprouting in the dorsal horn? J. Comp. Neurol. 428 2000 1 4
10. N.F. Britton, M.A.J. Chaplain, and S.M. Skevington The role of N-methyl-d-aspartate (NMDA) receptors in wind-up: a mathematical model Math. Med. Biol. 13 1996 193 205
11. N.F. Britton, and S.M. Skevington On the mathematical modelling of pain Neurochem. Res. 21 1996 1133 1140
12. S. Bruehl, A.V. Apkarian, J.C. Ballantyne, A. Berger, D. Borsook, W.G. Chen, J.T. Farrar, J.A. Haythornthwaite, S.D. Horn, M.J. Iadarola, C.E. Inturrisi, L. Lao, S. Mackey, J. Mao, A. Sawczuk, G.R. Uhl, J. Witter, C.J. Woolf, J.-K. Zubieta, and Y. Lin Personalized medicine and opioid analgesic prescribing for chronic pain: opportunities and challenges J. Pain 14 2013 103 113
13. J.-P.V. Butyen The performance and safety of an implantable spinal cord stimulation system in patients with chronic pain: a 5-year study Neuromodulation 6 2003 79 87
14. T. Cameron Safety and efficacy of spinal cord stimulation for the treatment of chronic pain: a 20-year literature review J. Neurosurg. Spine 100 2004 254 267
15. J.N. Campbell, and R.A. Meyer Mechanisms of neuropathic pain Neuron 52 2006 77 92
16. J.M. Chung, D.R. Kenshalo, K.D. Gerhart, and W.D. Willis Excitation of primate spinothalamic neurons by cutaneous C-fiber volleys J. Neurophysiol. 42 1979 1354 1369
17. B. Coburn A theoretical study of epidural electrical stimulation of the spinal cord - Part II: Effects on long myelinated fibers IEEE Trans. Biomed. Eng. 32 1985 978 986
18. B. Coburn, and W.K. Sin A theoretical study of epidural electrical stimulation of the spinal cord - Part I: Finite element analysis of stimulus fields IEEE Trans. Biomed. Eng. 32 1985 971 977
19. R.C. Coghill, D.J. Mayer, and D.D. Price Wide dynamic range but not nociceptive-specific neurons encode multidimensional features of prolonged repetitive heat pain J. Neurophysiol. 69 1993 703 716
20. A.W. Cook, and S.P. Weinstein Chronic dorsal column stimulation in multiple sclerosis. Preliminary report N. Y. State J. Med. 73 1973 2868 2872
21. J.A. Coull, S. Beggs, D. Boudreau, D. Boivin, M. Tsuda, K. Inoue, C. Gravel, M.W. Salter, and Y. De Koninck BDNF from microglia causes the shift in neuronal anion gradient underlying neuropathic pain Nature 438 2005 1017 1021
22. J.-G. Cui, B. Linderoth, and B.A. Meyerson Effects of spinal cord stimulation on touch-evoked allodynia involve GABAergic mechanisms. An experimental study in the mononeuropathic rat Pain 66 1996 287 295
23. J. Cui, B. Meyerson, A. Sollevi, and B. Linderoth Effect of spinal cord stimulation on tactile hypersensitivity in mononeuropathic rats is potentiated by simultaneous GABAB and adenosine receptor activation Neurosci. Lett. 247 1998 183 186
24. I. Decosterd, and C.J. Woolf Spared nerve injury: an animal model of persistent peripheral neuropathic pain Pain 87 2000 149 158
25. X. Ding, F. Hua, K. Sutherly, J.L. Ardell, and C.A. Williams C2 spinal cord stimulation induces dynorphin release from rat T4 spinal cord: potential modulation of myocardial ischemia-sensitive neurons Am. J. Physiol. Regul. Integr. Comp. Physiol. 295 2008 R1519
26. D. Dubuisson Effect of dorsal-column stimulation on gelatinosa and marginal neurons of cat spinal cord J. Neurosurg. 70 1989 257 265
27. A.W. Duggan, and F.W. Foong Bicuculline and spinal inhibition produced by dorsal column stimulation in the cat Pain 22 1985 249 259
28. C. El-Khoury, N. Hawwa, M. Baliki, S. Atweh, S. Jabbur, and N. Saade Attenuation of neuropathic pain by segmental and supraspinal activation of the dorsal column system in awake rats Neuroscience 112 2002 541 553
29. A. Farajidavar, S. Saeb, and K. Behbehani Incorporating synaptic time-dependent plasticity and dynamic synapse into a computational model of wind-up Neural Net. 21 2008 241 249
30. H.L. Fields, A. Malick, and R. Burstein Dorsal horn projection targets of ON and OFF cells in the rostral ventromedial medulla J. Neurophysiol. 74 1995 1742 1759
31. R.D. Foreman, J.E. Beall, J.D. Coulter, and W.D. Willis Effects of dorsal column stimulation on primate spinothalamic tract neurons J. Neurophysiol. 39 1976 534 546
32. T.B. Freeman, J.N. Campbell, and D.M. Long Naloxone does not affect pain relief induced by electrical stimulation in man Pain 17 1983 189 195
33. G. Giesler Jr, K. Gerhart, R. Yezierski, T. Wilcox, and W. Willis Postsynaptic inhibition of primate spinothalamic neurons by stimulation in nucleus raphe magnus Brain Res. 204 1981 184 188
34. J. Goff, A. Burkey, D. Goff, and L. Jasmin Reorganization of the spinal dorsal horn in models of chronic pain: correlation with behaviour Neuroscience 82 1997 559 574
35. Y. Guan Spinal cord stimulation: neurophysiological and neurochemical mechanisms of action Curr. Pain Headache Rep. 16 2012 217 225
36. Y. Guan, P.W. Wacnik, F. Yang, A.F. Carteret, C.-Y. Chung, R.A. Meyer, and S.N. Raja Spinal cord stimulation-induced analgesia: electrical stimulation of dorsal column and dorsal roots attenuates dorsal horn neuronal excitability in neuropathic rats Anesthesiology 113 2010 1392 1405
37. R. Hautvast, G. Horst, B. DeJong, M. DeJongste, P. Blanksma, A. Paans, and J. Korf Relative changes in regional cerebral blood flow during spinal cord stimulation in patients with refractory angina pectoris Eur. J. Neurosci. 9 2006 1178 1183
38. M.M. Heinricher, I. Tavares, J.L. Leith, and B.M. Lumb Descending control of nociception: specificity, recruitment and plasticity Brain Res. Rev. 60 2009 214 225
39. P. Hillman, and P.D. Wall Inhibitory and excitatory factors influencing the receptive fields of lamina 5 spinal cord cells Exp. Brain Res. 9 1969 284 306
40. M.L. Hines, and N.T. Carnevale The NEURON simulation environment Neural Comput. 9 1997 1179 1209
41. J. Holsheimer Which neuronal elements are activated directly by spinal cord stimulation Neuromodulation 5 2002 25 31
42. J. Holsheimer, and W. Wesselink Optimum electrode geometry for spinal cord stimulation: the narrow bipole and tripole Med. Biol. Eng. Comput. 35 1997 493 497
43. J.H. Hwang, and T.L. Yaksh The effect of spinal GABA receptor agonists on tactile allodynia in a surgically-induced neuropathic pain model in the rat Pain 70 1997 15 22
44. Illis L.S.; Sedgwick E.M.; Tallis R.C. (1978) Clinical results of spinal cord stimulation. In: Proceedings of the VIIth International Symposium Exern Contr Human Extremities, 523-523 Dubrovnick, Yugoslavia.
45. Illis L.S.; Sedgwick E.M.; Tallis R.C.; 1980. Spinal cord stimulation in multiple sclerosis: clinical results. J. Neurol. Neurosurg. Psychiatry 43, 1-14.
46. S. Janssen, S. Gerard, M. Raijmakers, M. Truin, M. Van Kleef, and E. Joosten Decreased intracellular GABA levels contribute to spinal cord stimulation-induced analgesia in rats suffering from painful peripheral neuropathy: the role of KCC2 and GABA< > A<> receptor-mediated inhibition Neurochem. Int. 60 2012 21 30
47. M. Kawamata, M. Koshizaki, S.G. Shimada, E. Narimatsu, Y. Kozuka, T. Takahashi, A. Namiki, and J.G. Collins Changes in response properties and receptive fields of spinal dorsal horn neurons in rats after surgical incision in hairy skin Anesthesiology 102 2005 141 151
48. A.F. Keller, S. Beggs, M.W. Salter, and Y. De Koninck Transformation of the output of spinal lamina I neurons after nerve injury and microglia stimulation underlying neuropathic pain Mol. Pain 3 2007 27
49. K.J. Kim, Y.W. Yoon, and J.M. Chung Comparison of three rodent neuropathic pain models Exp. Brain Res. 113 1997 200 206
50. E.T.M.D. Kiriakopoulos, R.R.M.D. Tasker, S.M.A. Nicosia, M.L.P. Wood, and D.J.M.D. Mikulis Functional magnetic resonance imaging: a potential tool for the evaluation of spinal cord stimulation: technical case report Neurosurgery August 41 1997 501 504
51. T. Kohno, K. Moore, H. Baba, and C. Woolf Peripheral nerve injury alters excitatory synaptic transmission in lamina II of the rat dorsal horn J. Physiol. 548 2003 131 138
52. K. Kumar, S. Malik, and D. Demeria Treatment of chronic pain with spinal cord stimulation versus alternative therapies: cost-effectiveness analysis Neurosurgery July 51 2002 106 116
53. K. Kumar, and S. Rizvi Cost-effectiveness of spinal cord stimulation therapy in management of chronic pain Pain Med. 2013
54. K. Kumar, R.S. Taylor, L. Jacques, S. Eldabe, M. Meglio, J. Molet, S. Thomson, J. O'Callaghan, E. Eisenberg, G. Milbouw, E. Buchser, G. Fortini, J. Richardson, and R.B. North Spinal cord stimulation versus conventional medical management for neuropathic pain: a multicentre randomised controlled trial in patients with failed back surgery syndrome Pain 132 2007 179 188
55. K. Kumar, C. Toth, R.K. Nath, and P. Laing Epidural spinal cord stimulation for treatment of chronic pain - some predictors of success. A 15-year experience Surg. Neurol. 50 1998 110 121
56. G. Lavertu, S.L. Côté, and Y. De Koninck Enhancing K-Cl co-transport restores normal spinothalamic sensory coding in a neuropathic pain model Brain 2013
57. H.A. Lekan, and S.M. Carlton Glutamatergic and GABAergic input to rat spinothalamic tract cells in the superficial dorsal horn J. Comp. Neurol. 361 1995 417 428
58. G. Lind, G. Schechtmann, J. Winter, B.A. Meyerson, and B. Linderoth Baclofen-enhanced spinal cord stimulation and intrathecal baclofen alone for neuropathic pain: long-term outcome of a pilot study Eur. J. Pain 12 2008 132 136
59. G. Lind, B.A. Meyerson, J. Winter, and B. Linderoth Intrathecal baclofen as adjuvant therapy to enhance the effect of spinal cord stimulation in neuropathic pain: a pilot study Eur J Pain 8 2004 377 383
60. Lind G.; Schechtmann G.; Winter J.; Linderoth B.; 2007. Drug-enhanced spinal stimulation for pain: a new strategy. In: Operative Neuromodulation, Springer, pp 57-63
61. U. Lindblom, and B.A. Meyerson Influence on touch, vibration and cutaneous pain of dorsal column stimulation in man Pain 1 1975 257 270
62. U. Lindblom, D.N. Tapper, and Z. Wiesenfeld The effect of dorsal column stimulation on the nociceptive response of dorsal horn cells and its relevance for pain suppression Pain 4 1978 133 144
63. B. Linderoth, and R.D. Foreman Physiology of spinal cord stimulation: review and update Neuromodulation 2 1999 150 164
64. B. Linderoth, and R.D. Foreman Mechanisms of spinal cord stimulation in painful syndromes: role of animal models Pain Med. 7 2006 S14 S26-S14-S26
65. B. Linderoth, R.D. Foreman, and B.A. Meyerson Mechanisms of action of spinal cord stimulation Textbook of Stereotactic and Functional Neurosurgery 2331-2348 2009 McGraw Hill pp
66. I.V. Melnick, S.F.A. Santos, K. Szokol, P. Szucs, and B.V. Safronov Ionic basis of tonic firing in spinal substantia gelatinosa neurons of rat J. Neurophysiol. 91 2004 646 655
67. R. Melzack, and P.D. Wall Pain mechanisms: a new theory Science 150 1965 971 979
68. D. Menetrey, G. Giesler Jr, and J. Besson An analysis of response properties of spinal cord dorsal horn neurones to nonnoxious and noxious stimuli in the spinal rat Exp. Brain Res. 27 1977 15 33
69. B.A. Meyerson, and B. Linderoth Spinal cord stimulation: mechanisms of action in neuropathic and ischemic pain Electrical Stimulation and the Relief of Pain vol. 15 2003 The Netherlands: Elsevier B.V 161 182
70. B.A. Meyerson, B. Ren, P. Herregodts, and B. Linderoth Spinal cord stimulation in animal models of mononeuropathy: effects on the withdrawal response and the flexor reflex Pain 61 1995 229 243
71. M. Millan Descending control of pain Prog. Neurobiol. 66 2002 355 474
72. K. Moore, T. Kohno, L. Karchewski, J. Scholz, H. Baba, and C. Woolf 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
73. R.B. North, D.H. Kidd, M. Zahurak, C.S. James, and D.M. Long Spinal cord stimulation for chronic, intractable pain: experience over two decades Neurosurgery 32 1993 384 395
74. J.C. Oakley, and J.P. Prager Spinal cord stimulation: mechanisms of action Spine 27 2002 2574 2583
75. S.A. Prescott, and Y. De Koninck Integration time in a subset of spinal lamina I neurons is lengthened by sodium and calcium currents acting synergistically to prolong subthreshold depolarization J. Neurosci. 25 2005 4743 4754
76. S.A. Prescott, Y. De Koninck, and T.J. Sejnowski Biophysical basis for three distinct dynamical mechanisms of action potential initiation PLoS Comput. Biol. 4 2008 e1000198
77. S.A. Prescott, and S. Ratté Pain processing by spinal microcircuits: afferent combinatorics Curr. Opin. Neurobiol. 22 2012 631 639
78. C. Qin, X. Yang, M. Wu, J.P. Farber, B. Linderoth, and R.D. Foreman Modulation of neuronal activity in dorsal column nuclei by upper cervical spinal cord stimulation in rats Neuroscience 164 2009 770 776
79. V. Sankarasubramanian, J. Buitenweg, J. Holsheimer, and P. Veltink Electrode alignment of transverse tripoles using a percutaneous triple-lead approach in spinal cord stimulation J. Neural Eng. 8 2011 016010
80. K. Sato, E. King, L. Johanek, and K. Sluka Spinal cord stimulation reduces hypersensitivity through activation of opioid receptors in a frequency-dependent manner Eur. J. Pain 17 2013 551 561
81. G. Schechtmann, G. Lind, J. Winter, B.A. Meyerson, and B. Linderoth Intrathecal clonidine and baclofen enhance the pain-relieving effect of spinal cord stimulation: a comparative placebo-controlled, randomized trial Neurosurgery 67 2010 173 181
82. C.N. Shealy, J. Mortimer, and N.R. Hagfors Dorsal column electroanalgesia Survey Anesthesiol. 16 1972 15 16
83. R. Shechter, F. Yang, Q. Xu, Y.-K. Cheong, S.-Q. He, A. Sdrulla, A.F. Carteret, P.W. Wacnik, X. Dong, and R.A. Meyer Conventional and kilohertz-frequency spinal cord stimulation produces intensity-and frequency-dependent inhibition of mechanical hypersensitivity in a rat model of neuropathic pain Anesthesiology 119 2013 422 432
84. D.A. Simone, L.S. Sorkin, U. Oh, J.M. Chung, C. Owens, R.H. LaMotte, and W.D. Willis Neurogenic hyperalgesia: central neural correlates in responses of spinothalamic tract neurons J. Neurophysiol. 66 1991 228 246
85. L. Sivilotti, and C.J. Woolf The contribution of GABAA and glycine receptors to central sensitization: disinhibition and touch-evoked allodynia in the spinal cord J. Neurophysiol. 72 1994 169 179
86. H. Smits, M. van Kleef, and E.A. Joosten Spinal cord stimulation of dorsal columns in a rat model of neuropathic pain: evidence for a segmental spinal mechanism of pain relief Pain 153 2012 177 183
87. Z. Song, O. Ansah, B. Meyerson, A. Pertovaara, and B. Linderoth Exploration of supraspinal mechanisms in effects of spinal cord stimulation: role of the locus coeruleus Neuroscience 253 2013 426 434
88. Z. Song, B.A. Meyerson, and B. Linderoth Spinal 5-HT receptors that contribute to the pain-relieving effects of spinal cord stimulation in a rat model of neuropathy Pain 152 2011 1666 1673
89. Z. Song, C. Ultenius, B.A. Meyerson, and B. Linderoth Pain relief by spinal cord stimulation involves serotonergic mechanisms: an experimental study in a rat model of mononeuropathy Pain 147 2009 241 248
90. Z. Song, H. Viisanen, B.A. Meyerson, A. Pertovaara, and B. Linderoth Efficacy of kilohertz-frequency and conventional spinal cord stimulation in rat models of different pain conditions Neuromodul.: Technol. Neural Interface 2014
91. A. Stancák, J. Kozák, I. Vrba, J. Tintera, J. Vrána, H. Polácek, and M. Stancák Functional magnetic resonance imaging of cerebral activation during spinal cord stimulation in failed back surgery syndrome patients Eur. J. Pain 12 2008 137
92. J. Struijk, J. Holsheimer, G. van der Heide, and H. Boom Recruitment of dorsal column fibers in spinal cord stimulation: influence of collateral branching IEEE Trans. Biomed. Eng. 39 1992 903 912
93. J.J. Struijk, J. Holsheimer, G. Barolat, J. He, and H.B.K. Boom Paresthesia thresholds in spinal cord stimulation: a comparison of theoretical results with clinical data IEEE Trans. Rehabil. Eng. 1 1993 101 108
94. J.J. Struijk, J. Holsheimer, and H.B.K. Boom Excitation of dorsal root fibers in spinal cord stimulation: a theoretical study IEEE Trans. Biomed. Eng. 40 1993 632 639
95. J.J. Struijk, J. Holsheimer, B.K. van Veen, and H.B.K. Boom Epidural spinal cord stimulation: calculation of field potentials with special reference to dorsal column nerve fibers IEEE Trans. Biomed. Eng. 38 1991 104 110
96. R. Suzuki, L. Rygh, and A. Dickenson Bad news from the brain: descending 5-HT pathways that control spinal pain processing Trends Pharmacol. Sci. 25 2004 613 617
97. P. Szucs, L.L. Luz, R. Pinho, P. Aguiar, Z. Antal, S.Y.X. Tiong, A.J. Todd, and B.V. Safronov Axon diversity of lamina I local-circuit neurons in the lumbar spinal cord J. Comp. Neurol. 521 2013 2719 2741
98. M.S. Tabet, S.A. Soueidan, M. Bitar, S.F. Atweh, and S.J. Jabbur Supraspinal modulation of nociception in awake rats by stimulation of the dorsal column nuclei Brain Res. 369 1986 307 310
99. R. Taylor, J. Van Buyten, and E. Buchser Spinal cord stimulation for chronic back and leg pain and failed back surgery syndrome: a systematic review and analysis of prognostic factors Spine 30 2005 152 160
100. R.S. Taylor, M.J. Desai, P. Rigoard, and R.J. Taylor Predictors of pain relief following spinal cord stimulation in chronic back and leg pain and failed back surgery syndrome: a systematic review and meta-regression analysis Pain Pract 2013
101. A.J. Todd Neuronal circuitry for pain processing in the dorsal horn Nat. Rev. Neurosci. 11 2010 823 836
102. C. Torsney Inflammatory pain unmasks heterosynaptic facilitation in lamina I neurokinin 1 receptor-expressing neurons in rat spinal cord J. Neurosci. 31 2011 5158 5168
103. C. Torsney, and A.B. MacDermott Disinhibition opens the gate to pathological pain signaling in superficial neurokinin 1 receptor-expressing neurons in rat spinal cord J. Neurosci. 26 2006 1833 1843
104. I. Tracey, and P.W. Mantyh The cerebral signature for pain perception and its modulation Neuron 55 2007 377 391
105. J. Turner, J. Loeser, R. Deyo, and S. Sanders Spinal cord stimulation for patients with failed back surgery syndrome or complex regional pain syndrome: a systematic review of effectiveness and complications Pain 108 2004 137 147
106. H. Viisanen, and A. Pertovaara Roles of the rostroventromedial medulla and the spinal 5-HT1A receptor in descending antinociception induced by motor cortex stimulation in the neuropathic rat Neurosci. Lett. 476 2010 133 137
107. A. von Hehn Christian, R. Baron, and J. Woolf Clifford Deconstructing the neuropathic pain phenotype to reveal neural mechanisms Neuron 73 2012 638 652
108. P.D. Wall, and R. Melzack Textbook of Pain 1996 Churchill Livingstone Edinburgh
109. J. Wallin, A. Fiskå, A. Tjølsen, B. Linderoth, and K. Hole Spinal cord stimulation inhibits long-term potentiation of spinal wide dynamic range neurons Brain Res. 973 2003 39 43
110. W.A. Wesselink, J. Holsheimer, and H.B.K. Boom Analysis of current density and related parameters in spinal cord stimulation IEEE Trans. Rehabil. Eng. 6 1998 200 207
111. W.A. Wesselink, J. Holsheimer, B. Nuttin, H.B.K. Boom, G.W. King, J.M. Gybels, and P. de Sutter Estimation of fiber diameters in the spinal dorsal columns from clinical data IEEE Trans. Rehabil. Eng. 45 1998 1355 1362
112. W.D. Willis, D.L. Trevino, J.D. Coulter, and R.A. Maunz Responses of primate spinothalamic tract neurons to natural stimulation of hindlimb J. Neurophysiol. 37 1974 358 372
113. C. Woolf, and P. Wall Chronic peripheral nerve section diminishes the primary afferent A-fibre mediated inhibition of rat dorsal horn neurones Brain Res. 242 1982 77 85
114. C.J. Woolf, P. Shortland, and R.E. Coggeshall Peripheral nerve injury triggers central sprouting of myelinated afferents Nature 355 1992 75 78
115. C.J. Woolf, P. Shortland, M. Reynolds, J. Ridings, T. Doubell, and R.E. Coggeshall Reorganization of central terminals of myelinated primary afferents in the rat dorsal horn following peripheral axotomy J. Comp. Neurol. 360 1995 121 134
116. C.J.W. Woolf Central sensitization: implications for the diagnosis and treatment of pain Pain 152 2011 S2 S15-S12-S15
117. V. Yakhnitsa, B. Linderoth, and B.A. Meyerson Spinal cord stimulation attenuates dorsal horn neuronal hyperexcitability in a rat model of mononeuropathy Pain 79 1999 223 233
118. F. Yang, A. Carteret, P. Wacnik, C.-Y. Chung, L. Xing, X. Dong, R. Meyer, S. Raja, and Y. Guan Bipolar spinal cord stimulation attenuates mechanical hypersensitivity at an intensity that activates a small portion of A-fiber afferents in spinal nerve-injured rats Neuroscience 199 2011 470 480
119. F. Yang, Q. Xu, Y.K. Cheong, R. Shechter, A. Sdrulla, S.Q. He, V. Tiwari, X. Dong, P.W. Wacnik, R. Meyer, S.N. Raja, and Y. Guan Comparison of intensity-dependent inhibition of spinal wide-dynamic range neurons by dorsal column and peripheral nerve stimulation in a rat model of neuropathic pain Eur. J. Pain 2014
120. H.U. Zeilhofer, H. Wildner, and G.E. Yévenes Fast synaptic inhibition in spinal sensory processing and pain control Physiol. Rev. 92 2012 193 235
121. J. Zheng, Y. Lu, and E.R. Perl Inhibitory neurones of the spinal substantia gelatinosa mediate interaction of signals from primary afferents J. Physiol. 588 2010 2065 2075