Therapeutic time window of noninvasive brain stimulation for pain treatment: Inhibition of maladaptive plasticity with early intervention

Expert Review of Medical Devices

Volumn 10, Issue 3, 2013, Pages 339-352

  Andrade, Dafne C ^a   Borges, Igor ^a   Bravo, Gabriela L ^a   Bolognini, Nadia ^b   Fregni, Felipe ^a,c  

^a American Journal of Physical Medicine and Rehabilitation   (United States)

^b UNIVERSITY OF MILANO BICOCCA   (Italy)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

acute brain disorders; central poststroke pain; chronic pain; chronic postsurgical pain; clinical trial design; maladaptive plasticity; noninvasive brain stimulation; spinal cord injury; stroke; traumatic brain injury

Indexed keywords

BRAIN DISORDERS; CENTRAL POSTSTROKE PAIN; CHRONIC PAIN; CHRONIC POSTSURGICAL PAIN; CLINICAL TRIAL DESIGNS; NON-INVASIVE BRAIN STIMULATIONS; SPINAL CORD INJURIES (SCI); STROKE; TRAUMATIC BRAIN INJURIES;

BRAIN; EXPERIMENTS; FUNCTIONAL POLYMERS; PATIENT REHABILITATION;

HEALTH;

N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ANALGESIA; BRAIN DEPTH STIMULATION; CENTRAL NERVOUS SYSTEM SENSITIZATION; CEREBROVASCULAR ACCIDENT; CHRONIC PAIN; EARLY INTERVENTION; EXCITABILITY; HUMAN; NERVE CELL PLASTICITY; NEUROIMAGING; NOCICEPTION; NON INVASIVE PROCEDURE; NONHUMAN; OUTCOME ASSESSMENT; PAIN; POSTOPERATIVE PAIN; RANDOMIZED CONTROLLED TRIAL (TOPIC); REPEAT PROCEDURE; REVIEW; RISK ASSESSMENT; SPINAL CORD INJURY; SPINAL PAIN; TRANSCRANIAL DIRECT CURRENT STIMULATION; TRANSCRANIAL MAGNETIC STIMULATION; TRAUMATIC BRAIN INJURY;

ANIMALS; BRAIN; DEEP BRAIN STIMULATION; EARLY MEDICAL INTERVENTION; HUMANS; NEURONAL PLASTICITY; PAIN MANAGEMENT; TIME FACTORS;

EID: 84877911155     PISSN: 17434440     EISSN: 17452422     Source Type: Journal    
DOI: 10.1586/erd.12.90     Document Type: Review

References (171)

1. Hamada M, Terao Y, Hanajima R et al. Bidirectional long-term motor cortical plasticity and metaplasticity induced by quadripulse transcranial magnetic stimulation. J. Physiol. (Lond.) 586(16), 3927-3947 (2008).
2. Fricke K, Seeber AA, Thirugnanasambandam N, Paulus W, Nitsche MA, Rothwell JC. Time course of the induction of homeostatic plasticity generated by repeated transcranial direct current stimulation of the human motor cortex. J. Neurophysiol. 105(3), 1141-1149 (2011).
3. Liebetanz D, Nitsche MA, Tergau F, Paulus W. Pharmacological approach to the mechanisms of transcranial DC-stimulation- induced after-effects of human motor cortex excitability. Brain 125(Pt 10), 2238-2247 (2002).
4. Nitsche MA, Fricke K, Henschke U et al. Pharmacological modulation of cortical excitability shifts induced by transcranial direct current stimulation in humans. J. Physiol. (Lond.) 553(Pt 1), 293-301 (2003).
5. Nitsche MA, Kuo MF, Karrasch R, Wächter B, Liebetanz D, Paulus W. Serotonin affects transcranial direct current-induced neuroplasticity in humans. Biol. Psychiatry 66(5), 503-508 (2009).
6. Tokay T, Holl N, Kirschstein T, Zschorlich V, Köhling R. High-frequency magnetic stimulation induces long-term potentiation in rat hippocampal slices. Neurosci. Lett. 461(2), 150-154 (2009).
7. Fregni F, Boggio PS, Lima MC et al. A sham-controlled, Phase II trial of transcranial direct current stimulation for the treatment of central pain in traumatic spinal cord injury. Pain 122(1-2), 197-209 (2006).
8. Fregni F, Freedman S, Pascual-Leone A. Recent advances in the treatment of chronic pain with non-invasive brain stimulation techniques. Lancet Neurol. 6(2), 188-191 (2007).
9. Fregni F, Gimenes R, Valle AC et al. A randomized, sham-controlled, proof of principle study of transcranial direct current stimulation for the treatment of pain in fibromyalgia. Arthritis Rheum. 54(12), 3988-3998 (2006).
10. Lindenberg R, Renga V, Zhu LL, Nair D, Schlaug G. Bihemispheric brain stimulation facilitates motor recovery in chronic stroke patients. Neurology 75(24), 2176-2184 (2010).
11. Kehlet H, Jensen TS, Woolf CJ. Persistent postsurgical pain: risk factors and prevention. Lancet 367(9522), 1618-1625 (2006).
12. Lefaucheur JP. Wasserman EA, Ziemann U, Walsh V, Paus T, Lisanby S. The Oxford Handbook of Transcranial Stimulation. Oxford University Press, NY, USA (2008).
13. Hallett M. Transcranial magnetic stimulation and the human brain. Nature 406(6792), 147-150 (2000).
14. Rossi S, Hallett M, Rossini PM, Pascual-Leone A; Safety of TMS Consensus Group. Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin. Neurophysiol. 120(12), 2008-2039 (2009).
15. Kobayashi M, Pascual-Leone A. Transcranial magnetic stimulation in neurology. Lancet Neurol. 2(3), 145-156 (2003).
16. Ferrarelli F, Haraldsson HM, Barnhart TE et al. A [17F]-fluoromethane PET/TMS study of effective connectivity. Brain Res. Bull. 64(2), 103-113 (2004).
17. Cárdenas-Morales L, Grön G, Kammer T. Exploring the after-effects of theta burst magnetic stimulation on the human motor cortex: a functional imaging study. Hum. Brain Mapp. 32(11), 1948-1960 (2011).
18. Okabe S, Hanajima R, Ohnishi T et al. Functional connectivity revealed by single-photon emission computed tomography (SPECT) during repetitive transcranial magnetic stimulation (rTMS) of the motor cortex. Clin. Neurophysiol. 114(3), 450-457 (2003).
19. Baudewig J, Siebner HR, Bestmann S et al. Functional MRI of cortical activations induced by transcranial magnetic stimulation (TMS). Neuroreport 12(16), 3543-3548 (2001).
20. Fox P, Ingham R, George MS et al. Imaging human intra-cerebral connectivity by PET during TMS. Neuroreport 8(12), 2787-2791 (1997).
21. Speer AM, Willis MW, Herscovitch P et al. Intensity-dependent regional cerebral blood flow during 1-Hz repetitive transcranial magnetic stimulation (rTMS) in healthy volunteers studied with H2 15O positron emission tomography: I. Effects of primary motor cortex rTMS. Biol. Psychiatry 54(8), 818-825 (2003).
22. Siebner HR, Peller M, Willoch F et al. Lasting cortical activation after repetitive TMS of the motor cortex: a glucose metabolic study. Neurology 54(4), 956-963 (2000).
23. Rounis E, Lee L, Siebner HR et al. Frequency specific changes in regional cerebral blood flow and motor system connectivity following rTMS to the primary motor cortex. Neuroimage 26(1), 164-176 (2005).
24. Lee L, Siebner HR, Rowe JB et al. Acute remapping within the motor system induced by low-frequency repetitive transcranial magnetic stimulation. J. Neurosci. 23(12), 5308-5318 (2003).
25. Takano B, Drzezga A, Peller M et al. Short-term modulation of regional excitability and blood flow in human motor cortex following rapid-rate transcranial magnetic stimulation. Neuroimage 23(3), 849-859 (2004).
26. Gaynor LM, Kühn AA, Dileone M et al. Suppression of beta oscillations in the subthalamic nucleus following cortical stimulation in humans. Eur. J. Neurosci. 28(8), 1686-1695 (2008).
27. Speer AM, Willis MW, Herscovitch P et al. Intensity-dependent regional cerebral blood flow during 1-Hz repetitive transcranial magnetic stimulation (rTMS) in healthy volunteers studied with H2 15O positron emission tomography: II. Effects of prefrontal cortex rTMS. Biol. Psychiatry 54(8), 826-832 (2003).
28. Michael N, Gösling M, Reutemann M et al. Metabolic changes after repetitive transcranial magnetic stimulation (rTMS) of the left prefrontal cortex: a sham- controlled proton magnetic resonance spectroscopy (1H MRS) study of healthy brain. Eur. J. Neurosci. 17(11), 2462-2468 (2003).
29. Paus T, Castro-Alamancos MA, Petrides M. Cortico-cortical connectivity of the human mid-dorsolateral frontal cortex and its modulation by repetitive transcranial magnetic stimulation. Eur. J. Neurosci. 14(8), 1405-1411 (2001).
30. Zheng XM. Regional cerebral blood flow changes in drug-resistant depressed patients following treatment with transcranial magnetic stimulation: a statistical parametric mapping analysis. Psychiatry Res. 100(2), 75-80 (2000).
31. Loo CK, Sachdev PS, Haindl W et al. High (15 Hz) and low (1 Hz) frequency transcranial magnetic stimulation have different acute effects on regional cerebral blood flow in depressed patients. Psychol. Med. 33(6), 997-1006 (2003).
32. Sibon I, Strafella AP, Gravel P et al. Acute prefrontal cortex TMS in healthy volunteers: effects on brain 11C-alphaMtrp trapping. Neuroimage 34(4), 1658-1664 (2007).
33. Ziemann U. TMS induced plasticity in human cortex. Rev. Neurosci. 15(4), 253-266 (2004).
34. Thickbroom GW. Transcranial magnetic stimulation and synaptic plasticity: experimental framework and human models. Exp. Brain Res. 180(4), 583-593 (2007).
35. Huang YZ, Rothwell JC, Edwards MJ, Chen RS. Effect of physiological activity on an NMDA-dependent form of cortical plasticity in human. Cereb. Cortex 18(3), 563-570 (2008).
36. Malenka RC, Bear MF. LTP and LTD: an embarrassment of riches. Neuron 44(1), 5-21 (2004).
37. Nitsche MA, Paulus W. Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation. J. Physiol. (Lond.) 527(3) 633-639 (2000).
38. Nitsche MA, Cohen LG, Wassermann EM et al. Transcranial direct current stimulation: state of the art 2008. Brain Stimul. 1(3), 206-223 (2008).
39. Stagg CJ, O'Shea J, Kincses ZT, Woolrich M, Matthews PM, Johansen-Berg H. Modulation of movement-associated cortical activation by transcranial direct current stimulation. Eur. J. Neurosci. 30(7), 1412-1423 (2009).
40. Kwon YH, Ko MH, Ahn SH et al. Primary motor cortex activation by transcranial direct current stimulation in the human brain. Neurosci. Lett. 435(1), 56-59 (2008).
41. Jang SH, Ahn SH, Byun WM, Kim CS, Lee MY, Kwon YH. The effect of transcranial direct current stimulation on the cortical activation by motor task in the human brain: an fMRI study. Neurosci. Lett. 460(2), 117-120 (2009).
42. Lang N, Siebner HR, Ward NS et al. How does transcranial DC stimulation of the primary motor cortex alter regional neuronal activity in the human brain? Eur. J. Neurosci. 22(2), 495-504 (2005).
43. Antal A, Polania R, Schmidt-Samoa C, Dechent P, Paulus W. Transcranial direct current stimulation over the primary motor cortex during fMRI. Neuroimage 55(2), 590-596 (2011).
44. Baudewig J, Nitsche MA, Paulus W, Frahm J. Regional modulation of BOLD MRI responses to human sensorimotor activation by transcranial direct current stimulation. Magn. Reson. Med. 45(2), 196-201 (2001).
45. Keeser D, Padberg F, Reisinger E et al. Prefrontal direct current stimulation modulates resting EEG and event-related potentials in healthy subjects: a standardized low resolution tomography (sLORETA) study. Neuroimage 55(2), 644-657 (2011).
46. Nitsche MA, Lampe C, Antal A et al. Dopaminergic modulation of long-lasting direct current-induced cortical excitability changes in the human motor cortex. Eur. J. Neurosci. 23(6), 1651-1657 (2006).
47. Nitsche MA, Liebetanz D, Schlitterlau A et al. GABAergic modulation of DC stimulation-induced motor cortex excitability shifts in humans. Eur. J. Neurosci. 19(10), 2720-2726 (2004).
48. Pascual-Leone A, Amedi A, Fregni F, Merabet LB. The plastic human brain cortex. Annu. Rev. Neurosci. 28, 377-401 (2005).
49. Rosenkranz K, Butler K, Williamon A, Cordivari C, Lees AJ, Rothwell JC. Sensorimotor reorganization by proprioceptive training in musician's dystonia and writer's cramp. Neurology 70(4), 304-315 (2008).
50. Tyvaert L, Houdayer E, Devanne H, Monaca C, Cassim F, Derambure P. The effect of repetitive transcranial magnetic stimulation on dystonia: a clinical and pathophysiological approach. Neurophysiol. Clin. 36(3), 135-143 (2006).
51. Havrankova P, Jech R, Walker ND et al. Repetitive TMS of the somatosensory cortex improves writer's cramp and enhances cortical activity. Neuro Endocrinol. Lett. 31(1), 73-86 (2010).
52. Murase N, Rothwell JC, Kaji R et al. Subthreshold low-frequency repetitive transcranial magnetic stimulation over the premotor cortex modulates writer's cramp. Brain 128(Pt 1), 104-115 (2005).
53. Borich M, Arora S, Kimberley TJ. Lasting effects of repeated rTMS application in focal hand dystonia. Restor. Neurol. Neurosci. 27(1), 55-65 (2009).
54. Sampson SM, Kung S, McAlpine DE, Sandroni P. The use of slow-frequency prefrontal repetitive transcranial magnetic stimulation in refractory neuropathic pain. J. ECT 27(1), 33-37 (2011).
55. Borckardt JJ, Smith AR, Reeves ST et al. A pilot study investigating the effects of fast left prefrontal rTMS on chronic neuropathic pain. Pain Med. 10(5), 840-849 (2009).
56. Leung A, Donohue M, Xu R et al. rTMS for suppressing neuropathic pain: a meta-analysis. J. Pain 10(12), 1205-1216 (2009).
57. Sampson SM, Rome JD, Rummans TA. Slow-frequency rTMS reduces fibromyalgia pain. Pain Med. 7(2), 115-118 (2006).
58. Passard A, Attal N, Benadhira R et al. Effects of unilateral repetitive transcranial magnetic stimulation of the motor cortex on chronic widespread pain in fibromyalgia. Brain 130(Pt 10), 2661-2670 (2007).
59. Short EB, Borckardt JJ, Anderson BS et al. Ten sessions of adjunctive left prefrontal rTMS significantly reduces fibromyalgia pain: a randomized, controlled pilot study. Pain 152(11), 2477-2484 (2011).
60. Mhalla A, Baudic S, Ciampi de Andrade D et al. Long-term maintenance of the analgesic effects of transcranial magnetic stimulation in fibromyalgia. Pain 152(7), 1478-1485 (2011).
61. Mori F, Codecà C, Kusayanagi H et al. Effects of anodal transcranial direct current stimulation on chronic neuropathic pain in patients with multiple sclerosis. J. Pain 11(5), 436-442 (2010).
62. Fenton BW, Palmieri PA, Boggio P, Fanning J, Fregni F. A preliminary study of transcranial direct current stimulation for the treatment of refractory chronic pelvic pain. Brain Stimul. 2(2), 103-107 (2009).
63. Brighina F, Piazza A, Vitello G et al. rTMS of the prefrontal cortex in the treatment of chronic migraine: a pilot study. J. Neurol. Sci. 227(1), 67-71 (2004).
64. Fregni F, Potvin K, Dasilva D et al. Clinical effects and brain metabolic correlates in non-invasive cortical neuromodulation for visceral pain. Eur. J. Pain 15(1), 53-60 (2011).
65. Pleger B, Janssen F, Schwenkreis P, Völker B, Maier C, Tegenthoff M. Repetitive transcranial magnetic stimulation of the motor cortex attenuates pain perception in complex regional pain syndrome type I. Neurosci. Lett. 356(2), 87-90 (2004).
66. Picarelli H, Teixeira MJ, de Andrade DC et al. Repetitive transcranial magnetic stimulation is efficacious as an add-on to pharmacological therapy in complex regional pain syndrome (CRPS) type I. J. Pain 11(11), 1203-1210 (2010).
67. Lefaucheur JP, Drouot X, Ménard-Lefaucheur I, Keravel Y, Nguyen JP. Motor cortex rTMS restores defective intracortical inhibition in chronic neuropathic pain. Neurology 67(9), 1568-1574 (2006).
68. Eisenberg E, Chistyakov AV, Yudashkin M, Kaplan B, Hafner H, Feinsod M. Evidence for cortical hyperexcitability of the affected limb representation area in CRPS: a psychophysical and transcranial magnetic stimulation study. Pain 113(1-2), 99-105 (2005).
69. Salerno A, Thomas E, Olive P, Blotman F, Picot MC, Georgesco M. Motor cortical dysfunction disclosed by single and double magnetic stimulation in patients with fibromyalgia. Clin. Neurophysiol. 111(6), 994-1001 (2000).
70. Schwenkreis P, Janssen F, Rommel O et al. Bilateral motor cortex disinhibition in complex regional pain syndrome (CRPS) type I of the hand. Neurology 61(4), 515-519 (2003).
71. Latremoliere A, Woolf CJ. Central sensitization: a generator of pain hypersensitivity by central neural plasticity. J. Pain 10(9), 895-926 (2009).
72. Petersen-Felix S, Curatolo M. Neuroplasticity - an important factor in acute and chronic pain. Swiss Med. Wkly 132(21-22), 273-278 (2002).
73. Wang CK, Myunghae Hah J, Carroll I. Factors contributing to pain chronicity. Curr. Pain Headache Rep. 13(1), 7-11 (2009).
74. Ikeda H, Stark J, Fischer H et al. Synaptic amplifier of inflammatory pain in the spinal dorsal horn. Science 312(5780), 1659-1662 (2006).
75. Zhuo M. A synaptic model for pain: long-term potentiation in the anterior cingulate cortex. Mol. Cells 23(3), 259-271 (2007).
76. Urban MO, Gebhart GF. Supraspinal contributions to hyperalgesia. Proc. Natl Acad. Sci. USA 96(14), 7687-7692 (1999).
77. Coutinho SV, Urban MO, Gebhart GF. Role of glutamate receptors and nitric oxide in the rostral ventromedial medulla in visceral hyperalgesia. Pain 78(1), 59-69 (1998).
78. Urban MO, Coutinho SV, Gebhart GF. Involvement of excitatory amino acid receptors and nitric oxide in the rostral ventromedial medulla in modulating secondary hyperalgesia produced by mustard oil. Pain 81(1-2), 45-55 (1999).
79. Kawamura J, Kaneko T, Kaneko M et al. Neuron-immune interactions in the sensitized thalamus induced by mustard oil application to rat molar pulp. J. Dent. Res. 89(11), 1309-1314 (2010).
80. Kaneko M, Kaneko T, Kaneko R et al. The role of N-methyl-d-aspartate receptor subunits in the rat thalamic mediodorsal nucleus during central sensitization. Brain Res. 1371, 16-22 (2011).
81. Martinez V, Ben Ammar S, Judet T, Bouhassira D, Chauvin M, Fletcher D. Risk factors predictive of chronic postsurgical neuropathic pain: the value of the iliac crest bone harvest model. Pain 153(7), 1478-1483 (2012).
82. De Kock M, Lavand'homme P, Waterloos H. 'Balanced analgesia' in the perioperative period: is there a place for ketamine? Pain 92(3), 373-380 (2001).
83. Salengros JC, Huybrechts I, Ducart A et al. Different anesthetic techniques associated with different incidences of chronic post-thoracotomy pain: low-dose remifentanil plus presurgical epidural analgesia is preferable to high-dose remifentanil with postsurgical epidural analgesia. J. Cardiothorac. Vasc. Anesth. 24(4), 608-616 (2010).
84. Seifert F, Maihöfner C. Functional and structural imaging of pain-induced neuroplasticity. Curr. Opin. Anaesthesiol. 24(5), 515-523 (2011).
85. Voscopoulos C, Lema M. When does acute pain become chronic? Br. J. Anaesth. 105(Suppl. 1), i69-i85 (2010).
86. Ren K, Dubner R. Descending modulation in persistent pain: an update. Pain 100(1-2), 1-6 (2002).
87. Heinricher MM, Tavares I, Leith JL, Lumb BM. Descending control of nociception: specificity, recruitment and plasticity. Brain Res. Rev. 60(1), 214-225 (2009).
88. Kincaid W, Neubert MJ, Xu M, Kim CJ, Heinricher MM. Role for medullary pain facilitating neurons in secondary thermal hyperalgesia. J. Neurophysiol. 95(1), 33-41 (2006).
89. Kovelowski CJ, Ossipov MH, Sun H, Lai J, Malan TP, Porreca F. Supraspinal cholecystokinin may drive tonic descending facilitation mechanisms to maintain neuropathic pain in the rat. Pain 87(3), 265-273 (2000).
90. Pertovaara A, Wei H, Hämäläinen MM. Lidocaine in the rostroventromedial medulla and the periaqueductal gray attenuates allodynia in neuropathic rats. Neurosci. Lett. 218(2), 127-130 (1996).
91. Porreca F, Burgess SE, Gardell LR et al. Inhibition of neuropathic pain by selective ablation of brainstem medullary cells expressing the mu-opioid receptor. J. Neurosci. 21(14), 5281-5288 (2001).
92. Urban MO, Zahn PK, Gebhart GF. Descending facilitatory influences from the rostral medial medulla mediate secondary, but not primary hyperalgesia in the rat. Neuroscience 90(2), 349-352 (1999).
93. Vanderah TW, Suenaga NM, Ossipov MH, Malan TP Jr, Lai J, Porreca F. Tonic descending facilitation from the rostral ventromedial medulla mediates opioidinduced abnormal pain and antinociceptive tolerance. J. Neurosci. 21(1), 279-286 (2001).
94. Vera-Portocarrero LP, Zhang ET, Ossipov MH et al. Descending facilitation from the rostral ventromedial medulla maintains nerve injury-induced central sensitization. Neuroscience 140(4), 1311-1320 (2006).
95. Calejesan AA, Kim SJ, Zhuo M. Descending facilitatory modulation of a behavioral nociceptive response by stimulation in the adult rat anterior cingulate cortex. Eur. J. Pain 4(1), 83-96 (2000).
96. Moylan Governo RJ, Morris PG, Prior MJ, Marsden CA, Chapman V. Capsaicinevoked brain activation and central sensitization in anaesthetised rats: a functional magnetic resonance imaging study. Pain 126(1-3), 35-45 (2006).
97. Chu H, Sun J, Xu H, Niu Z, Xu M. Effect of periaqueductal gray melanocortin 4 receptor in pain facilitation and glial activation in rat model of chronic constriction injury. Neurol. Res. 34(9), 871-888 (2012).
98. Kalita J, Kumar B, Misra UK, Pradhan PK. Central post stroke pain: clinical, MRI, and SPECT correlation. Pain Med. 12(2), 282-288 (2011).
99. Porreca F, Ossipov MH, Gebhart GF. Chronic pain and medullary descending facilitation. Trends Neurosci. 25(6), 319-325 (2002).
100. Terayama R, Guan Y, Dubner R, Ren K. Activity-induced plasticity in brain stem pain modulatory circuitry after inflammation. Neuroreport 11(9), 1915-1919 (2000).
101. Burgess SE, Gardell LR, Ossipov MH et al. Time-dependent descending facilitation from the rostral ventromedial medulla maintains, but does not initiate, neuropathic pain. J. Neurosci. 22(12), 5129-5136 (2002).
102. Ossipov MH, Dussor GO, Porreca F. Central modulation of pain. J. Clin. Invest. 120(11), 3779-3787 (2010).
103. Zambreanu L, Wise RG, Brooks JC, Iannetti GD, Tracey I. A role for the brainstem in central sensitisation in humans. Evidence from functional magnetic resonance imaging. Pain 114(3), 397-407 (2005).
104. Iadarola MJ, Berman KF, Zeffiro TA et al. Neural activation during acute capsaicinevoked pain and allodynia assessed with PET. Brain 121, 931-947 (1998).
105. Baron R, Baron Y, Disbrow E, Roberts TP. Brain processing of capsaicin-induced secondary hyperalgesia: a functional MRI study. Neurology 53(3), 548-557 (1999).
106. Witting N, Kupers RC, Svensson P, Arendt-Nielsen L, Gjedde A, Jensen TS. Experimental brush-evoked allodynia activates posterior parietal cortex. Neurology 57(10), 1817-1824 (2001).
107. Maihöfner C, Schmelz M, Forster C, Neundörfer B, Handwerker HO. Neural activation during experimental allodynia: a functional magnetic resonance imaging study. Eur. J. Neurosci. 19(12), 3211-3218 (2004).
108. Lee MC, Zambreanu L, Menon DK, Tracey I. Identifying brain activity specifically related to the maintenance and perceptual consequence of central sensitization in humans. J. Neurosci. 28(45), 11642-11649 (2008).
109. Seifert F, Bschorer K, De Col R et al. Medial prefrontal cortex activity is predictive for hyperalgesia and pharmacological antihyperalgesia. J. Neurosci. 29(19), 6167-6175 (2009).
110. Mainero C, Zhang WT, Kumar A, Rosen BR, Sorensen AG. Mapping the spinal and supraspinal pathways of dynamic mechanical allodynia in the human trigeminal system using cardiac-gated fMRI. Neuroimage 35(3), 1201-1210 (2007).
111. Becerra L, Morris S, Bazes S et al. Trigeminal neuropathic pain alters responses in CNS circuits to mechanical (brush) and thermal (cold and heat) stimuli. J. Neurosci. 26(42), 10646-10657 (2006).
112. Seifert F, Maihöfner C. Representation of cold allodynia in the human brain - a functional MRI study. Neuroimage 35(3), 1168-1180 (2007).
113. Geha PY, Baliki MN, Wang X, Harden RN, Paice JA, Apkarian AV. Brain dynamics for perception of tactile allodynia (touch-induced pain) in postherpetic neuralgia. Pain 138(3), 641-656 (2008).
114. Lorenz J, Cross DJ, Minoshima S, Morrow TJ, Paulson PE, Casey KL. A unique representation of heat allodynia in the human brain. Neuron 35(2), 383-393 (2002).
115. Lorenz J, Minoshima S, Casey KL. Keeping pain out of mind: the role of the dorsolateral prefrontal cortex in pain modulation. Brain 126(Pt 5), 1079-1091 (2003).
116. Peyron R, Laurent B, García-Larrea L. Functional imaging of brain responses to pain. A review and meta-analysis (2000). Neurophysiol. Clin. 30(5), 263-288 (2000).
117. Antal A, Paulus W. Effects of transcranial theta-burst stimulation on acute pain perception. Restor. Neurol. Neurosci. 28(4), 477-484 (2010).
118. Johnson S, Summers J, Pridmore S. Changes to somatosensory detection and pain thresholds following high frequency repetitive TMS of the motor cortex in individuals suffering from chronic pain. Pain 123(1-2), 187-192 (2006).
119. Brighina F, De Tommaso M, Giglia F et al. Modulation of pain perception by transcranial magnetic stimulation of left prefrontal cortex. J. Headache Pain 12(2), 185-191 (2011).
120. Tamura Y, Okabe S, Ohnishi T et al. Effects of 1-Hz repetitive transcranial magnetic stimulation on acute pain induced by capsaicin. Pain 107(1-2), 107-115 (2004).
121. Borckardt JJ, Reeves ST, Weinstein M et al. Significant analgesic effects of one session of postoperative left prefrontal cortex repetitive transcranial magnetic stimulation: a replication study. Brain Stimul. 1(2), 122-127 (2008).
122. Borckardt JJ, Weinstein M, Reeves ST et al. Postoperative left prefrontal repetitive transcranial magnetic stimulation reduces patient-controlled analgesia use. Anesthesiology 105(3), 557-562 (2006).
123. Groppa S, Muthuraman M, Otto B, Deuschl G, Siebner HR, Raethjen J. Subcortical substrates of TMS induced modulation of the cortico-cortical connectivity. Brain Stimul. 6(2), 138-146 (2013).
124. Volz MS, Mendonca M, Pinheiro FS, Cui H, Santana M, Fregni F. Dissociation of motor task-induced cortical excitability and pain perception changes in healthy volunteers. PLoS One 7(3), e34273 (2012).
125. de Andrade DC, Mhalla A, Adam F, Texeira MJ, Bouhassira D. Neuropharmacological basis of rTMSinduced analgesia: the role of endogenous opioids. Pain 152(2), 320-326 (2011).
126. Csifcsak G, Antal A, Hillers F et al. Modulatory effects of transcranial direct current stimulation on laser-evoked potentials. Pain Med. 10(1), 122-132 (2009).
127. Boggio PS, Zaghi S, Lopes M, Fregni F. Modulatory effects of anodal transcranial direct current stimulation on perception and pain thresholds in healthy volunteers. Eur. J. Neurol. 15(10), 1124-1130 (2008).
128. Mylius V, Jung M, Menzler K et al. Effects of transcranial direct current stimulation on pain perception and working memory. Eur. J. Pain 16(7), 974-982 (2012).
129. Antal A, Brepohl N, Poreisz C, Boros K, Csifcsak G, Paulus W. Transcranial direct current stimulation over somatosensory cortex decreases experimentally induced acute pain perception. Clin. J. Pain 24(1), 56-63 (2008).
130. Borckardt JJ, Romagnuolo J, Reeves ST et al. Feasibility, safety, and effectiveness of transcranial direct current stimulation for decreasing post-ERCP pain: a randomized, sham-controlled, pilot study. Gastrointest. Endosc. 73(6), 1158-1164 (2011).
131. Chen R, Cohen LG, Hallett M. Nervous system reorganization following injury. Neuroscience 111(4), 761-773 (2002).
132. Kumar G, Soni CR. Central post-stroke pain: current evidence. J. Neurol. Sci. 284(1-2), 10-17 (2009).
133. Hong JH, Bai DS, Jeong JY et al. Injury of the spino-thalamo-cortical pathway is necessary for central post-stroke pain. Eur. Neurol. 64(3), 163-168 (2010).
134. Kumar B, Kalita J, Kumar G, Misra UK. Central poststroke pain: a review of pathophysiology and treatment. Anesth. Analg. 108(5), 1645-1657 (2009).
135. Peyron R, García-Larrea L, Grégoire MC et al. Allodynia after lateral-medullary (Wallenberg) infarct. A PET study. Brain 121, 345-356 (1998).
136. Klit H, Finnerup NB, Jensen TS. Central post-stroke pain: clinical characteristics, pathophysiology, and management. Lancet Neurol. 8(9), 857-868 (2009).
137. Canavero S, Bonicalzi V, Dotta M, Vighetti S, Asteggiano G, Cocito D. Transcranial magnetic cortical stimulation relieves central pain. Stereotact. Funct. Neurosurg. 78(3-4), 192-196 (2002).
138. Lefaucheur JP, Drouot X, Menard-Lefaucheur I et al. Neurogenic pain relief by repetitive transcranial magnetic cortical stimulation depends on the origin and the site of pain. J. Neurol. Neurosurg. Psychiatr. 75(4), 612-616 (2004).
139. Khedr EM, Ahmed MA, Fathy N, Rothwell JC. Therapeutic trial of repetitive transcranial magnetic stimulation after acute ischemic stroke. Neurology 65(3), 466-468 (2005).
140. André-Obadia N, Peyron R, Mertens P, Mauguière F, Laurent B, Garcia-Larrea L. Transcranial magnetic stimulation for pain control. Double-blind study of different frequencies against placebo, and correlation with motor cortex stimulation efficacy. Clin. Neurophysiol. 117(7), 1536-1544 (2006).
141. Hirayama A, Saitoh Y, Kishima H et al. Reduction of intractable deafferentation pain by navigation-guided repetitive transcranial magnetic stimulation of the primary motor cortex. Pain 122(1-2), 22-27 (2006).
142. Khedr EM, Etraby AE, Hemeda M, Nasef AM, Razek AA. Long-term effect of repetitive transcranial magnetic stimulation on motor function recovery after acute ischemic stroke. Acta Neurol. Scand. 121(1), 30-37 (2010).
143. Khaleel SH, Bayoumy IM, El-Nabil LM, Moustafa RR. Differential hemodynamic response to repetitive transcranial magnetic stimulation in acute stroke patients with cortical versus subcortical infarcts. Eur. Neurol. 63(6), 337-342 (2010).
144. Rossi C, Sallustio F, Di Legge S, Stanzione P, Koch G. Transcranial direct current stimulation of the affected hemisphere does not accelerate recovery of acute stroke patients. Eur. J. Neurol. 20(1), 202-204 (2013).
145. Ding Y, Kastin AJ, Pan W. Neural plasticity after spinal cord injury. Curr. Pharm. Des. 11(11), 1441-1450 (2005).
146. Jain N, Catania KC, Kaas JH. Deactivation and reactivation of somatosensory cortex after dorsal spinal cord injury. Nature 386(6624), 495-498 (1997).
147. Weng HR, Lee JI, Lenz FA et al. Functional plasticity in primate somatosensory thalamus following chronic lesion of the ventral lateral spinal cord. Neuroscience 101(2), 393-401 (2000).
148. Kumru H, Vidal J, Kofler M, Portell E, Valls-Solé J. Alterations in excitatory and inhibitory brainstem interneuronal circuits after severe spinal cord injury. J. Neurotrauma 27(4), 721-728 (2010).
149. Hou S, Duale H, Rabchevsky AG. Intraspinal sprouting of unmyelinated pelvic afferents after complete spinal cord injury is correlated with autonomic dysreflexia induced by visceral pain. Neuroscience 159(1), 369-379 (2009).
150. Wrigley PJ, Press SR, Gustin SM et al. Neuropathic pain and primary somatosensory cortex reorganization following spinal cord injury. Pain 141(1-2), 52-59 (2009).
151. Burchiel KJ, Hsu FP. Pain and spasticity after spinal cord injury: mechanisms and treatment. Spine 26(24 Suppl.), S146-S160 (2001).
152. Hulsebosch CE. Gliopathy ensures persistent inflammation and chronic pain after spinal cord injury. Exp. Neurol. 214(1), 6-9 (2008).
153. Wang G, Thompson SM. Maladaptive homeostatic plasticity in a rodent model of central pain syndrome: thalamic hyperexcitability after spinothalamic tract lesions. J. Neurosci. 28(46), 11959-11969 (2008).
154. Golarai G, Greenwood AC, Feeney DM, Connor JA. Physiological and structural evidence for hippocampal involvement in persistent seizure susceptibility after traumatic brain injury. J. Neurosci. 21(21), 8523-8537 (2001).
155. Gottesman RF, Komotar R, Hillis AE. Neurologic aspects of traumatic brain injury. Int. Rev. Psychiatry 15(4), 302-309 (2003).
156. Nampiaparampil DE. Prevalence of chronic pain after traumatic brain injury: a systematic review. JAMA 300(6), 711-719 (2008).
157. Ofek H, Defrin R. The characteristics of chronic central pain after traumatic brain injury. Pain 131(3), 330-340 (2007).
158. Walker WC. Pain pathoetiology after TBI: neural and nonneural mechanisms. J. Head Trauma Rehabil. 19(1), 72-81 (2004).
159. Brunoni AR, Fregni F. Clinical trial design in non-invasive brain stimulation psychiatric research. Int. J. Methods Psychiatr. Res. 20(2), e19-e30 (2011).
160. Loo CK, Taylor JL, Gandevia SC, McDarmont BN, Mitchell PB, Sachdev PS. Transcranial magnetic stimulation (TMS) in controlled treatment studies: are some 'sham' forms active? Biol. Psychiatry 47(4), 325-331 (2000).
161. Gandiga PC, Hummel FC, Cohen LG. Transcranial DC stimulation (tDCS): a tool for double-blind sham-controlled clinical studies in brain stimulation. Clin. Neurophysiol. 117(4), 845-850 (2006).
162. Poreisz C, Boros K, Antal A, Paulus W. Safety aspects of transcranial direct current stimulation concerning healthy subjects and patients. Brain Res. Bull. 72(4-6), 208-214 (2007).
163. O'Connell NE, Cossar J, Marston L et al. Rethinking clinical trials of transcranial direct current stimulation: participant and assessor blinding is inadequate at intensities of 2mA. PLoS One 7(10), e47514 (2012).
164. Lisanby SH, Gutman D, Luber B, Schroeder C, Sackeim HA. Sham TMS: intracerebral measurement of the induced electrical field and the induction of motor-evoked potentials. Biol. Psychiatry 49(5), 460-463 (2001).
165. Brunoni AR, Amadera J, Berbel B, Volz MS, Rizzerio BG, Fregni F. A systematic review on reporting and assessment of adverse effects associated with transcranial direct current stimulation. Int. J. Neuropsychopharmacol. 14(8), 1133-1145 (2011).
166. Reis J, Schambra HM, Cohen LG et al. Noninvasive cortical stimulation enhances motor skill acquisition over multiple days through an effect on consolidation. Proc. Natl Acad. Sci. USA 106(5), 1590-1595 (2009).
167. Kim YH, You SH, Ko MH et al. Repetitive transcranial magnetic stimulation- induced corticomotor excitability and associated motor skill acquisition in chronic stroke. Stroke 37(6), 1471-1476 (2006).
168. Baeken C, Schrijvers DL, Sabbe BG, Vanderhasselt MA, De Raedt R. Impact of one HF-rTMS session on fine motor function in right-handed healthy female subjects: a comparison of stimulation over the left versus the right dorsolateral prefrontal cortex. Neuropsychobiology 65(2), 96-102 (2012).
169. Clinical Trials in Neurology. Guiloff RJ (Ed.). Springer, Berlin, Germany (2001).
170. Boggio PS, Amancio EJ, Correa CF et al. Transcranial DC stimulation coupled with TENS for the treatment of chronic pain: a preliminary study. Clin. J. Pain 25(8), 691-695 (2009).
171. Datta A, Bikson M, Fregni F. Transcranial direct current stimulation in patients with skull defects and skull plates: high-resolution computational FEM study of factors altering cortical current flow. Neuroimage 52(4), 1268-1278 (2010).