Non-invasive Brain Stimulation, a Tool to Revert Maladaptive Plasticity in Neuropathic Pain

Antonino Naro, Demetrio Milardi, Margherita Russo, Carmen Terranova, Vincenzo Rizzo, Alberto Cacciola, Silvia Marino, Rocco S Calabro, Angelo Quartarone, Antonino Naro, Demetrio Milardi, Margherita Russo, Carmen Terranova, Vincenzo Rizzo, Alberto Cacciola, Silvia Marino, Rocco S Calabro, Angelo Quartarone

Abstract

Neuromodulatory effects of non-invasive brain stimulation (NIBS) have been extensively studied in chronic pain. A hypothetic mechanism of action would be to prevent or revert the ongoing maladaptive plasticity within the pain matrix. In this review, the authors discuss the mechanisms underlying the development of maladaptive plasticity in patients with chronic pain and the putative mechanisms of NIBS in modulating synaptic plasticity in neuropathic pain conditions.

Keywords: NIBS; TMS; neuropathic pain; plasticity; tDCS.

References

    1. Ahmed M. A., Mohamed S. A., Sayed D. (2011). Long-term antalgic effects of repetitive transcranial magnetic stimulation of motor cortex and serum beta-endorphin in patients with phantom pain. Neurol. Res. 33 953–958. 10.1179/1743132811Y.0000000045
    1. Andrade D. C., Borges I., Bravo G. L., Bolognini N., Fregni F. (2013). Therapeutic time window of noninvasive brain stimulation for pain treatment: inhibition of maladaptive plasticity with early intervention. Expert Rev. Med. Devices 10 339–352. 10.1586/erd.12.90
    1. André-Obadia N., Mertens P., Gueguen A., Peyron R., Garcia-Larrea L. (2008). Pain relief by rTMS: differential effect of current flow but no specific action on pain subtypes. Neurology 71 833–840. 10.1212/01.wnl.0000325481.61471.f0
    1. Antal A., Lang N., Boros K., Nitsche M., Siebner H. R., Paulus W. (2008). Homeostatic metaplasticity of the motor cortex is altered during headache-free intervals in migraine with aura. Cereb. Cortex 18 2701–2705. 10.1093/cercor/bhn032
    1. Ardolino G., Bossi B., Barbieri S., Priori A. (2005). Non-synaptic mechanisms underlie the after-effects of cathodal transcutaneous direct current stimulation of the human brain. J. Physiol. 568 653–663. 10.1113/jphysiol.2005.088310
    1. Baron N. (2006). Mechanisms of disease: neuropathic pain—a clinical perspective. Nat. Clin. Pract. Neurol. 2 95–106. 10.1038/ncpneuro0113
    1. Baron R., Baron Y., Disbrow E., Roberts T. P. (1999). Brain processing of capsaicin-induced secondary hyperalgesia: a functional MRI study. Neurology 53 548–557. 10.1212/WNL.53.3.548
    1. Baudewig J., Siebner H. R., Bestmann S., Tergau F., Tings T., Paulus W., et al. (2001). Functional MRI of cortical activations induced by transcranial magnetic stimulation (TMS). Neuroreport 12 3543–3548. 10.1097/00001756-200111160-00034
    1. Becerra L., Morris S., Bazes S., Gostic R., Sherman S., Gostic J., et al. (2006). Trigeminal neuropathic pain alters responses in CNS circuits to mechanical (brush) and thermal (cold and heat) stimuli. J. Neurosci. 26 10646–10657. 10.1523/JNEUROSCI.2305-06.2006
    1. Boggio P. S., Amancio E. J., Correa C. F., Cecilio S., Valasek C., et al. (2009). Transcranial DC stimulation coupled with TENS for the treatment of chronic pain: a preliminary study. Clin. J. Pain 25 691–695.
    1. Bolognini N., Olgiati E., Maravita A., Ferraro F., Fregni F. (2013). Motor, and parietal cortex stimulation for phantom limb pain, and sensations. Pain 154 1274–1280. 10.1016/j.pain.2013.03.040
    1. Borich M., Arora S., Kimberley T. J. (2009). Lasting effects of repeated rTMS application in focal hand dystonia. Restor. Neurol. Neurosci. 27 55–65. 10.3233/RNN-2009-0461
    1. Cárdenas-Morales L., Grön G., Kammer T. (2011). Exploring the after-effects of theta burst magnetic stimulation on the human motor cortex: a functional imaging study. Hum. Brain Mapp. 32 1948–1960. 10.1002/hbm.21160
    1. Carvalho A. L., Duarte C. B., Carvalho A. P. (2000). Regulation of AMPA receptors by phosphorylation. Neurochem. Res. 25 1245–1255. 10.1023/A:1007644128886
    1. Coutinho S. V., Urban M. O., Gebhart G. F. (1998). Role of glutamate receptors and nitric oxide in the rostral ventromedial medulla in visceral hyperalgesia. Pain 78 59–69. 10.1016/S0304-3959(98)00137-7
    1. Cruccu G., Aziz T. Z., Garcia-Larrea L., Hansson P., Jensen T. S., Lefaucheur J. P., et al. (2007). European EFNS guidelines on neurostimulation therapy for neuropathic pain. Eur. J. Neurol. 14 952–970. 10.1111/j.1468-1331.2007.01916.x
    1. de Andrade D. C., Mhalla A., Adam F., Texeira M. J., Bouhassira D. (2011). Neuropharmacological basis of rTMS-induced analgesia: the role of endogenous opioids. Pain 152 320–326. 10.1016/j.pain.2010.10.032
    1. Devor M. (2009). Ectopic discharge in Abeta afferents as a source of neuropathic pain. Exp. Brain Res. 196 115–128. 10.1007/s00221-009-1724-6
    1. Devor M., Seltzer Z. (1999). Pathophysiology of Damaged Nerves in Relation to Chronic Pain. Edinburg: Churchill Livingstone.
    1. Djouhri L., Koutsikou S., Fang X., McMullan S., Lawson S. N. (2006). Spontaneous pain, both neuropathic and inflammatory, is related to frequency of spontaneous firing in intact C-fiber nociceptors. J. Neurosci. 26 1281–1292. 10.1523/JNEUROSCI.3388-05.2006
    1. DosSantos M. F., Love T. M., Martikainen I. K., Nascimento T. D., Fregni F., Cummiford C., et al. (2012). Immediate effects of tDCS on the μ-opioid system of a chronic pain patient. Front. Psychiatry 3:93 10.3389/fpsyt.2012.00093
    1. Fagni L., Chavis P., Ango F., Bockaert J. (2000). Complex interactions between mGluRs, intracellular Ca2+ stores and ion channels in neurons. Trends Neurosci. 23 80–88. 10.1016/S0166-2236(99)01492-7
    1. Fang L., Wu J., Zhang X., Lin Q., Willis W. D. (2003). Increased phosphorylation of the GluR1 subunit of spinal cord alpha-amino-3-hydroxy-5-methyl-4-isoxazole propionate receptor in rats following intradermal injection of capsaicin. Neuroscience 122 237–245. 10.1016/S0306-4522(03)00526-8
    1. Ferrarelli F., Haraldsson H. M., Barnhart T. E., Roberts A. D., Oakes T. R., Massimini M., et al. (2004). 17Ffluoromethane PET/TMS study of effective connectivity. Brain Res. Bull. 64 103–113. 10.1016/j.brainresbull.2004.04.020
    1. Fierro B., De Tommaso M., Giglia F., Giglia G., Palermo A., Brighina F. (2010). Repetitive transcranial magnetic stimulation (rTMS) of the dorsolateral prefrontal cortex (DLPFC) during capsaicin-induced pain: modulatory effects on motor cortex excitability. Exp. Brain Res. 203 31–38. 10.1007/s00221-010-2206-6
    1. Foerster B. R., Nascimento T. D., DeBoer M., Bender M. A., Rice I. C., Truong D. Q., et al. (2015). Excitatory and inhibitory brain metabolites as targets of motor cortex transcranial direct current stimulation therapy and predictors of its efficacy in fibromyalgia. Arthritis Rheumatol. 67 576–581. 10.1002/art.38945
    1. Fox P., Ingham R., George M. S., Mayberg H., Ingham J., Roby J., et al. (1997). Imaging human intra-cerebral connectivity by PET during TMS. Neuroreport 8 2787–2791. 10.1097/00001756-199708180-00027
    1. Fregni F., Boggio P. S., Lima M. C., Ferreira M. J., Wagner T., Rigonatti S. P., et al. (2006a). A sham-controlled, phase II trial of transcranial direct current stimulation for the treatment of central pain in traumatic spinal cord injury. Pain 122 197–209. 10.1016/j.pain.2006.02.023
    1. Fregni F., Gimenes R., Valle A. C., Ferreira M. J., Rocha R. R., Natalle L., et al. (2006b). A randomized, sham-controlled, proof of principle study of transcranial direct current stimulation for the treatment of pain in fibromyalgia. Arthritis Rheum 54 3988–3998. 10.1002/art.22195
    1. Fricová J., Klírová M., Šóš P., Tišlerová B., Masopust V., Haeckel M., et al. (2009). Repetitive transcranial stimulation in chronic neurogenic pain. 5th World Congress Institute of Pain, New York, USA. Pain Practice 9:38.
    1. Fritsch B., Reis J., Martinowich K., Schambra H. M., Ji Y., Cohen L. G., et al. (2010). Direct current stimulation promotes BDNF-dependent synaptic plasticity: potential implications for motor learning. Neuron 66 198–204. 10.1016/j.neuron.2010.03.035
    1. Gaynor L. M., Kühn A. A., Dileone M., Litvak V., Eusebio A., Pogosyan A., et al. (2008). Suppression of beta oscillations in the subthalamic nucleus following cortical stimulation in humans. Eur. J. Neurosci. 28 1686–1695. 10.1111/j.1460-9568.2008.06363.x
    1. Geha P. Y., Baliki M. N., Wang X., Harden R. N., Paice J. A., Apkarian A. V. (2008). Brain dynamics for perception of tactile allodynia (touch-induced pain) in postherpetic neuralgia. Pain 138 641–656. 10.1016/j.pain.2008.02.021
    1. Havrankova P., Jech R., Walker N. D., Operto G., Tauchmanova J., Vymazal J., et al. (2010). Repetitive TMS of the somatosensory cortex improves writer’s cramp and enhances cortical activity. NeuroEndocrinol. Lett. 31 73–86.
    1. Holsheimer J., Lefaucheur J. P., Buitenweg J. R., Goujon C., Nineb A., Nguyen J. P. (2007a). The role of intra-operative motor evoked potentials in the optimization of chronic cortical stimulation for the treatment of neuropathic pain. Clin. Neurophysiol. 118 2287–2296. 10.1016/j.clinph.2007.07.015
    1. Holsheimer J., Nguyen J. P., Lefaucheur J. P., Manola L. (2007b). Cathodal, anodal or bifocal stimulation of the motor cortex in the management of chronic pain. Acta Neurochir. Suppl. 97 57–66. 10.1007/978-3-211-33081-4_7
    1. Huang Y. Z., Rothwell J. C., Edwards M. J., Chen R. S. (2008). Effect of physiological activity on an NMDA-dependent form of cortical plasticity in human. Cereb. Cortex 18 563–570. 10.1093/cercor/bhm087
    1. Iadarola M. J., Berman K. F., Zeffiro T. A., Byas-Smith M. G., Gracely R. H., Max M. B., et al. (1998). Neural activation during acute capsaicinevoked pain and allodynia assessed with PET. Brain 121 931–947. 10.1093/brain/121.5.931
    1. Irlbacher K., Kuhnert J., Roricht S., Meyer B. U., Brandt S. A. (2006). Central and peripheral deafferent pain: therapy with repetitive transcranial magnetic stimulation. Nervenarzt 77 1198–1203.
    1. Ji R. R., Kohno T., Moore K. A., Woolf C. J. (2003). Central sensitization and LTP: do pain and memory share similar mechanisms? Trends Neurosci. 26 696–705. 10.1016/j.tins.2003.09.017
    1. Kaneko M., Kaneko T., Kaneko R., Chokechanachaisakul U., Kawamura J., Sunakawa M., et al. (2011). The role of N-methyl-d-aspartate receptor subunits in the rat thalamic mediodorsal nucleus during central sensitization. Brain Res. 1371 16–22. 10.1016/j.brainres.2010.11.054
    1. Kang J. S., Terranova C., Hilker R., Quartarone A., Ziemann U. (2011). Deficient homeostatic regulation of practice-dependent plasticity in writer’s cramp. Cereb. Cortex 21 1203–1212. 10.1093/cercor/bhq204
    1. Kawamura J., Kaneko T., Kaneko M., Sunakawa M., Kaneko R., Chokechanachaisakul U., et al. (2010). Neuron-immune interactions in the sensitized thalamus induced by mustard oil application to rat molar pulp. J. Dent. Res. 89 1309–1314. 10.1177/0022034510377202
    1. Kim W., Kim S. K. (2016). Neural circuit remodeling and structural plasticity in the cortex during chronic pain. Korean J. Physiol. Pharmacol. 20 1–8. 10.4196/kjpp.2016.20.1.1
    1. Knotkova H., Portenoy R. K., Cruciani R. A. (2013). Transcranial direct current stimulation (tDCS) relieved itching in a patient with chronic neuropathic pain. Clin. J. Pain 29 621–622. 10.1097/AJP.0b013e31826b1329
    1. Kobayashi M., Pascual-Leone A. (2003). Transcranial magnetic stimulation in neurology. Lancet Neurol. 2 145–156. 10.1016/S1474-4422(03)00321-1
    1. Koltzenburg M., Lundberg L. E., Torebjork H. E. (1992a). Dynamic and static components of mechanical hyperalgesia in human hairy skin. Pain 51 207–219.
    1. Koltzenburg M., Wahren L. K., Torebjork H. E. (1992b). Dynamic changes of mechanical hyperalgesia in neuropathic pain states and healthy subjects depend on the ongoing activity of unmyelinated nociceptive afferents. Pflugers. Arch. 420:452.
    1. Latremoliere A., Woolf C. J. (2009). Central sensitization: a generator of pain hypersensitivity by central neural plasticity. J. Pain 10 895–926. 10.1016/j.jpain.2009.06.012
    1. Lee L., Siebner H. R., Rowe J. B., Rizzo V., Rothwell J. C., Frackowiak R. S., et al. (2003). Acute remapping within the motor system induced by low-frequency repetitive transcranial magnetic stimulation. J. Neurosci. 23 5308–5318.
    1. Lee M. C., Zambreanu L., Menon D. K., Tracey I. (2008). Identifying brain activity specifically related to the maintenance and perceptual consequence of central sensitization in humans. J. Neurosci. 28 11642–11649. 10.1523/JNEUROSCI.2638-08.2008
    1. Lefaucheur J. P. (2006). The use of repetitive transcranial magnetic stimulation (rTMS) in chronic neuropathic pain. Neurophysiol. Clin. 36 117–124. 10.1016/j.neucli.2006.08.002
    1. Lefaucheur J. P. (2008). Principles of therapeutic use of transcranial and epidural cortical stimulation. Clin. Neurophysiol. 119 2179–2184. 10.1016/j.clinph.2008.07.007
    1. Lefaucheur J. P. (2016). Cortical neurostimulation for neuropathic pain: state of the art and perspectives. Pain 157 S81–S89. 10.1097/j.pain.0000000000000401
    1. Lefaucheur J. P., Ayache S. S., Sorel M., Farhat W. H., Zouari H. G., Ciampi de Andrade D., et al. (2012). Analgesic effects of repetitive transcranial magnetic stimulation of the motor cortex in neuropathic pain: influence of theta burst stimulation priming. Eur. J. Pain 1 1403–1413. 10.1002/j.1532-2149.2012.00150.x
    1. Lefaucheur J. P., Drouot X., Ménard-Lefaucheur I., Keravel Y., Nguyen J. P. (2006). Motor cortex rTMS improves defective intracortical inhibition in patients with chronic neuropathic pain: correlation with pain relief. Neurology 67 1568–1574. 10.1212/01.wnl.0000242731.10074.3c
    1. Lefaucheur J. P., Drouot X., Ménard-Lefaucheur I., Zerah F., Bendib B., Cesaro P., et al. (2004). Neurogenic pain relief by repetitive transcranial magnetic cortical stimulation depends on the origin and the site of pain. J. Neurol. Neurosurg. Psychiatry 75 612–616. 10.1136/jnnp.2003.022236
    1. Leung W. W., Jones A. Y., Ng S. S., Wong C. Y., Lee J. F. (2013). Acupuncture transcutaneous electrical nerve stimulation reduces discomfort associated with barostat-induced rectal distension: a randomized-controlled study. World J. Gastroenterol. 19 381–388. 10.3748/wjg.v19.i3.381
    1. Loo C. K., Sachdev P. S., Haindl W., Wen W., Mitchell P. B., Croker V. M., et al. (2003). High (15Hz) and low (1Hz) frequency transcranial magnetic stimulation have different acute effects on regional cerebral blood flow in depressed patients. Psychol. Med. 33 997–1006. 10.1017/S0033291703007955
    1. Lorenz J., Cross D. J., Minoshima S., Morrow T. J., Paulson P. E., Casey K. L. (2002). A unique representation of heat allodynia in the human brain. Neuron 35 383–393. 10.1016/S0896-6273(02)00767-5
    1. Lorenz J., Minoshima S., Casey K. L. (2003). Keeping pain out of mind: the role of the dorsolateral prefrontal cortex in pain modulation. Brain 126 1079–1091. 10.1093/brain/awg102
    1. Maihöfner C., Schmelz M., Forster C., Neundörfer B., Handwerker H. O. (2004). Neural activation during experimental allodynia: a functional magnetic resonance imaging study. Eur. J. Neurosci. 19 3211–3218. 10.1111/j.1460-9568.2004.03437.x
    1. Mainero C., Zhang W. T., Kumar A., Rosen B. R., Sorensen A. G. (2007). Mapping the spinal and supraspinal pathways of dynamic mechanical allodynia in the human trigeminal system using cardiac-gated fMRI. Neuroimage 35 1201–1210. 10.1016/j.neuroimage.2007.01.024
    1. Malenka R. C., Bear M. F. (2004). LTP and LTD: an embarrassment of riches. Neuron 44 5–21. 10.1016/j.neuron.2004.09.012
    1. Mhalla A., Baudic S., Ciampi deAndrade D., Gautron M., Perrot S., Teixeira M. J., et al. (2011). Long-term maintenance of the analgesic effects of transcranial magnetic stimulation in fibromyalgia. Pain 152 1478–1485. 10.1016/j.pain.2011.01.034
    1. Michael N., Gösling M., Reutemann M., Kersting A., Heindel W., Arolt V., et al. (2003). 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 2462–2468. 10.1046/j.1460-9568.2003.02683.x
    1. Moloney T. M., Witney A. G. (2013). Transcranial direct current stimulation (tDCS) priming of 1Hz repetitive transcranial magnetic stimulation (rTMS) modulates experimental pain thresholds. Neurosci. Lett. 534 289–294. 10.1016/j.neulet.2012.11.049
    1. Moore K. A., Kohno T., Karchewski L. A., Scholz J., Baba H., Woolf C. J. (2002). Partial peripheral nerve injury promotes a selective loss of GABAergic inhibition in the superficial dorsal horn of the spinal cord. J. Neurosci. 22 6724–6731.
    1. Murase N., Rothwell J. C., Kaji R., Urushihara R., Nakamura K., Murayama N., et al. (2005). Subthreshold low-frequency repetitive transcranial magnetic stimulation over the premotor cortex modulates writer’s cramp. Brain 128 104–115. 10.1093/brain/awh315
    1. Mylius V., Borckardt J. J., Lefaucheur J. P. (2012). Noninvasive cortical modulation of experimental pain. Pain 153 1350–1363. 10.1016/j.pain.2012.04.009
    1. Ngernyam N., Jensen M. P., Auvichayapat N., Punjaruk W., Auvichayapat P. (2013). Transcranial direct current stimulation in neuropathic pain. J. Pain Relief. 3:1.
    1. Nguyen J. P., Nizard J., Keravel Y., Lefaucheur J. P. (2011). Invasive brain stimulation for the treatment of neuropathic pain. Nat. Rev. Neurol. 7 699–709. 10.1038/nrneurol.2011.138
    1. Nitsche M. A., Cohen L. G., Wassermann E. M., Priori A., Lang N., Antal A., et al. (2008). Transcranial direct current stimulation: state of the art 2008. Brain Stimul. 1 206–223. 10.1016/j.brs.2008.06.004
    1. Nitsche M. A., Fricke K., Henschke U., Schlitterlau A., Liebetanz D., Lang N., et al. (2003). Pharmacological modulation of cortical excitability shifts induced by transcranial direct current stimulation in humans. J. Physiol. 553 293–301. 10.1113/jphysiol.2003.049916
    1. Nitsche M. A., Lampe C., Antal A., Liebetanz D., Lang N., Tergau F., et al. (2006). Dopaminergic modulation of long-lasting direct current-induced cortical excitability changes in the human motor cortex. Eur. J. Neurosci. 23 1651–1657. 10.1111/j.1460-9568.2006.04676.x
    1. Nitsche M. A., Liebetanz D., Schlitterlau A., Henschke U., Fricke K., Frommann K., et al. (2004). GABAergic modulation of DC stimulation-induced motor cortex excitability shifts in humans. Eur. J. Neurosci. 19 2720–2726. 10.1111/j.0953-816X.2004.03398.x
    1. Nitsche M. A., Paulus W. (2000). Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation. J. Physiol. (Lond.) 527 633–639. 10.1111/j.1469-7793.2000.t01-1-00633.x
    1. Nitsche M. A., Paulus W. (2001). Sustained excitability elevations induced by transcranial DC motor cortex stimulation in humans. Neurology 57 1899–1901. 10.1212/WNL.57.10.1899
    1. Nowak L. G., Bullier J. (1998). Axons, but not cell bodies, are activated by electrical stimulation in cortical gray matter. I. Evidence from chronaxie measurements. Exp. Brain Res. 118 477–488. 10.1007/s002210050304
    1. O’Connell N. E., Cossar J., Marston L., Wand B. M., Bunce D., De Souza L. H., et al. (2013). Transcranial direct current stimulation of the motor cortex in the treatment of chronic nonspecific low back pain: a randomized, double-blind exploratory study. Clin. J. Pain 29 26–34. 10.1097/AJP.0b013e318247ec09
    1. Ohn S. H., Chang W. H., Park C. H., Kim S. T., Lee J. I., Pascual-Leone A., et al. (2012). Neural correlates of the antinociceptive effects of repetitive transcranial magnetic stimulation on central pain after stroke. Neurorehabil. Neural Repair 26 344–352. 10.1177/1545968311423110
    1. Okabe S., Hanajima R., Ohnishi T., Nishikawa M., Imabayashi E., Takano H., et al. (2003). Functional connectivity revealed by single-photon emission computed tomography (SPECT) during repetitive transcranial magnetic stimulation (rTMS) of the motor cortex. Clin. Neurophysiol. 114 450–457. 10.1016/S1388-2457(02)00408-X
    1. Pascual-Leone A., Amedi A., Fregni F., Merabet L. B. (2005). The plastic human brain cortex. Annu. Rev. Neurosci. 28 377–401. 10.1146/annurev.neuro.27.070203.144216
    1. Paus T., Castro-Alamancos M. A., Petrides M. (2001). Cortico-cortical connectivity of the human mid-dorsolateral frontal cortex and its modulation by repetitive transcranial magnetic stimulation. Eur. J. Neurosci. 14 1405–1411. 10.1046/j.0953-816x.2001.01757.x
    1. Peterchev A. V., Wagner T. A., Miranda P. C., Nitsche M. A., Paulus W., Lisanby S. H., et al. (2012). Fundamentals of transcranial electric and magnetic stimulation dose: definition, selection, and reporting practices. Brain Stimul. 5 435–453. 10.1016/j.brs.2011.10.001
    1. Quartarone A., Bagnato S., Rizzo V., Morgante F., Sant’angelo A., Battaglia F., et al. (2005a). Distinct changes in cortical and spinal excitability following high-frequency repetitive TMS to the human motor cortex. Exp. Brain Res. 161 114–124. 10.1007/s00221-004-2052-5
    1. Quartarone A., Rizzo V., Bagnato S., Morgante F., Sant’Angelo A., Romano M., et al. (2005b). Homeostatic-like plasticity of the primary motor hand area is impaired in focal hand dystonia. Brain 128 1943–1950. 10.1093/brain/awh527
    1. Quartarone A., Siebner H. R., Rothwell J. C. (2006). Task-specific hand dystonia: can too much plasticity be bad for you? Trends Neurosci. 29 192–199. 10.1016/j.tins.2006.02.007
    1. Rokyta R., Fricová J. (2012). Neurostimulation methods in the treatment of chronic pain. Physiol. Res. 61 S23–S31.
    1. Rokyta R., Kršiak M., Kozák J. (2012). ). Pain – The Monography of Algesiology. Praha: Tigis; 747.
    1. Rothwell J. C. (1997). Techniques and mechanisms of action of transcranial stimulation of the human motor cortex. J. Neurosci. Methods 74 113–122. 10.1016/S0165-0270(97)02242-5
    1. Rounis E., Lee L., Siebner H. R., Rowe J. B., Friston K. J., Rothwell J. C., et al. (2005). Frequency specific changes in regional cerebral blood flow and motor system connectivity following rTMS to the primary motor cortex. Neuroimage 26 164–176. 10.1016/j.neuroimage.2005.01.037
    1. Scholz J., Broom D. C., Youn D. H., Mills C. D., Kohno T., Suter M. R., et al. (2005). Blocking caspase activity prevents transsynaptic neuronal apoptosis and the loss of inhibition in lamina II of the dorsal horn after peripheral nerve injury. J. Neurosci. 25 7317–7323. 10.1523/JNEUROSCI.1526-05.2005
    1. Seifert F., Bschorer K., De Col R., Filitz J., Peltz E., Koppert W., et al. (2009). Medial prefrontal cortex activity is predictive for hyperalgesia and pharmacological antihyperalgesia. J. Neurosci. 29 6167–6175. 10.1523/JNEUROSCI.4654-08.2009
    1. Seifert F., Maihöfner C. (2007). Representation of cold allodynia in the human brain – a functional MRI study. Neuroimage 35 1168–1180. 10.1016/j.neuroimage.2007.01.021
    1. Sherrington C. S. (1906). Observations on the scratch-reflex in the spinal dog. J. Physiol. 34 1–50. 10.1113/jphysiol.1906.sp001139
    1. Siebner H. R., Peller M., Willoch F., Minoshima S., Boecker H., Auer C., et al. (2000). Lasting cortical activation after repetitive TMS of the motor cortex: a glucose metabolic study. Neurology 54 956–963. 10.1212/WNL.54.4.956
    1. Siebner H. R., Rothwell J. C. (2003). Transcranial magnetic stimulation: new insights into representational cortical plasticity. Exp. Brain Res. 148 1–16. 10.1007/s00221-002-1234-2
    1. Soler M. D., Kumru H., Pelayo R., Vidal J., Tormos J. M., Fregni F., et al. (2010). Effectiveness of transcranial direct current stimulation and visual illusion on neuropathic pain in spinal cord injury. Brain 133 2565–2577. 10.1093/brain/awq184
    1. Speer A. M., Willis M. W., Herscovitch P., Daube-Witherspoon M., Shelton J. R., Benson B. E., et al. (2003). Intensity-dependent regional cerebral blood flow during 1-Hz repetitive transcranial magnetic stimulation (rTMS) in healthy volunteers studied with H2 positron emission tomography: I. Effects of primary motor cortex rTMS. Biol. Psychiatry 54 818–825. 10.1016/S0006-3223(03)00002-7
    1. Takano B., Drzezga A., Peller M., Sax I., Schwaiger M., Lee L., et al. (2004). Short-term .modulation of regional excitability and blood flow in human motorcortex following rapid-rate transcranial magnetic stimulation. Neuroimage 23849–859
    1. Tamura Y., Okabe S., Ohnishi T., Saito D., Arai N., Mochio S., et al. (2004). Effects of 1-Hz repetitive transcranial magnetic stimulation on acute pain induced by capsaicin. Pain 107 107–115. 10.1016/j.pain.2003.10.011
    1. Tang C. M., Dichter M., Morad M. (1990). Modulation of the N-methyl-D-aspartate channel by extracellular H+. Proc. Natl. Acad. Sci. U.S.A. 87 6445–6449. 10.1073/pnas.87.16.6445
    1. Taylor J. J., Borckardt J. J., George M. S. (2012). Endogenous opioids mediate left dorsolateral prefrontal cortex rTMS-induced analgesia. Pain 153 1219–1225. 10.1016/j.pain.2012.02.030
    1. Treister R., Lang M., Klein M. M., Oaklander A. L. (2013). Non-invasive transcranial magnetic stimulation (TMS) of the motor cortex for neuropathic pain—at the tipping point? Rambam Maimonides Med. J. 4 e0023 10.5041/RMMJ.10130
    1. Tsubokawa T., Katayama Y., Yamamoto T., Hirayama T., Koyama S. (1991). Treatment of thalamic pain by chronic motor cortex stimulation. Pacing Clin. Electrophysiol. 14 131–134. 10.1111/j.1540-8159.1991.tb04058.x
    1. Urban M. O., Coutinho S. V., Gebhart G. F. (1999). Involvement of excitatory amino acid receptors and nitric oxide in the rostral ventromedial medulla in modulating secondary hyperalgesia produced by mustard oil. Pain 81 45–55. 10.1016/S0304-3959(98)00265-6
    1. Urban M. O., Gebhart G. F. (1999). Supraspinal contributions to hyperalgesia. Proc. Natl. Acad. Sci. U.S.A. 96 7687–7692. 10.1073/pnas.96.14.7687
    1. Vera-Portocarrero L. P., Zhang E. T., Ossipov M. H., Xie J. Y., King T., Lai J., et al. (2006). Descending facilitation from the rostral ventromedial medulla maintains nerve injury-induced central sensitization. Neuroscience 140 1311–1320. 10.1016/j.neuroscience.2006.03.016
    1. Villanueva L., Fields H. L. (2004). “Endogenous central mechanisms of pain modulation,” in Progress in Pain Research and Management. The Pain System in Normal and Pathological States: A Primer for Clinicians eds Villanueva L., Dickenson A. H., Ollat H. (Seattle: IASP Press; ), 223–246.
    1. Wang H. Y., Crupi D., Liu J., Stucky A., Cruciata G., Di Rocco A., et al. (2011). Repetitive transcranial magnetic stimulation enhances BDNF-TrkB signaling in both brain and lymphocyte. J. Neurosci. 31 11044–11054. 10.1523/JNEUROSCI.2125-11.2011
    1. Wasserman E. M., Epstein C. M., Ziemann U., Walsh V., Paus T., Lisanby S. H. (2008). The Oxford Handbook of Transcranial Stimulation. Oxford: Oxford University Press.
    1. Witting N., Kupers R. C., Svensson P., Arendt-Nielsen L., Gjedde A., Jensen T. S. (2001). Experimental brush-evoked allodynia activates posterior parietal cortex. Neurology 57 1817–1824. 10.1212/WNL.57.10.1817
    1. Woolf C. J. (1983). Evidence for a central component of post-injury pain hypersensitivity. Nature 306 686–688. 10.1038/306686a0
    1. Woolf C. J. (2007). Central sensitization: uncovering the relation between pain and plasticity. Anesthesiology 106 864–867. 10.1097/01.anes.0000264769.87038.55
    1. Woolf C. J. (2011). Central sensitization: implications for the diagnosis and treatment of pain. Pain 152 S2–S15. 10.1016/j.pain.2010.09.030
    1. Woolf C. J., King A. E. (1990). Dynamic alterations in the cutaneous mechanoreceptive fields of dorsal horn neurons in the rat spinal cord. J. Neurosci. 10 2717–2726.
    1. Woolf C. J., Salter M. W. (2000). Neuronal plasticity: increasing the gain in pain. Science 288 1765–1769. 10.1126/science.288.5472.1765
    1. Woolf C. J., Shortland P., Coggeshall R. E. (1992). Peripheral nerve injury triggers central sprouting of myelinated afferents. Nature 355 75–78. 10.1038/355075a0
    1. Woolf C. J., Shortland P., Reynolds M., Ridings J., Doubell T., Coggeshall R. E. (1995). Reorganization of central terminals of myelinated primary afferents in the rat dorsal horn following peripheral axotomy. J. Comp. Neurol. 360 121–134. 10.1002/cne.903600109
    1. Woolf C. J., Thompson S. W. (1991). The induction and maintenance of central sensitization is dependent on N-methyl-D-aspartic acid receptor activation: implications for the treatment of post-injury pain hypersensitivity states. Pain 44 293–299. 10.1016/0304-3959(91)90100-C
    1. Xiao H. S., Huang Q. H., Zhang F. X., Bao L., Lu Y. J., Guo C., et al. (2002). Identification of gene expression profile of dorsal root ganglion in the rat peripheral axotomy model of neuropathic pain. Proc. Natl. Acad. Sci. U.S.A. 99 8360–8365. 10.1073/pnas.122231899
    1. Yoon E. J., Kim Y. K., Kim H. R., Kim S. E., Lee Y., Shin H. I. (2014). Transcranial direct current stimulation to lessen neuropathic pain after spinal cord injury: a mechanistic PET study. Neurorehabil. Neural Repair 28 250–259. 10.1177/1545968313507632
    1. Zambreanu L., Wise R. G., Brooks J. C., Iannetti G. D., Tracey I. (2005). A role for the brainstem in central sensitisation in humans. Evidence from functional magnetic resonance imaging. Pain 114 397–407.
    1. Zhang X., Cao B., Yan N., Liu J., Wang J., Tung V. O., et al. (2013). Vagus nerve stimulation modulates visceral pain-related affective memory. Behav. Brain Res. 236 8–15. 10.1016/j.bbr.2012.08.027
    1. Zheng X. M. (2000). Regional cerebral blood flow changes in drug-resistant depressed patients following treatment with transcranial magnetic stimulation: a statistical parametric mapping analysis. Psychiatry Res. 100 75–80. 10.1016/S0925-4927(00)00073-1
    1. Zhuang Z. Y., Gerner P., Woolf C. J., Ji R. R. (2005). ERK is sequentially activated in neurons, microglia, and astrocytes by spinal nerve ligation and contributes to mechanical allodynia in this neuropathic pain model. Pain 114 149–159. 10.1016/j.pain.2004.12.022
    1. Zhuo M. (2007). A synaptic model for pain: long-term potentiation in the anterior cingulate cortex. Mol. Cells 23 259–271.
    1. Ziemann U. (2004). TMS induced plasticity in human cortex. Rev. Neurosci. 15 253–266. 10.1515/REVNEURO.2004.15.4.253

Source: PubMed

Sponsor e collaboratori

Condizioni mediche

Interventi farmacologici

3
Sottoscrivi