PAIN
Volume 149, Issue 3 , Pages 495-500 , June 2010

Alteration of cortical excitability in patients with fibromyalgia

  • Alaa Mhalla

      Affiliations

    • INSERM U-987, CHU Ambroise Paré, APHP, F-92100 Boulogne-Billancourt, France
    • These authors contributed equally to this work.
  • ,
  • Daniel Ciampi de Andrade

      Affiliations

    • Department of Neurology, Hospital das Clinicas, University of São Paulo, Brazil
    • These authors contributed equally to this work.
  • ,
  • Sophie Baudic

      Affiliations

    • INSERM U-987, CHU Ambroise Paré, APHP, F-92100 Boulogne-Billancourt, France
  • ,
  • Serge Perrot

      Affiliations

    • INSERM U-987, CHU Ambroise Paré, APHP, F-92100 Boulogne-Billancourt, France
    • CHU Hôtel Dieu, Assistance Publique Hôpitaux de Paris, F-75001 Paris, France
    • Université Paris Descartes, F-75005 Paris, France
  • ,
  • Didier Bouhassira

      Affiliations

    • INSERM U-987, CHU Ambroise Paré, APHP, F-92100 Boulogne-Billancourt, France
    • Corresponding Author InformationCorresponding author at: INSERM U-987, Centre d’Evaluation et de Traitement de la Douleur, Hôpital Ambroise Paré, 9 avenue Charles de Gaulle, 92100 Boulogne-Billancourt, France. Tel.: +33 1 49 09 45 56; fax: +33 1 49 09 44 35.

Received 24 November 2009 ,Revised 4 February 2010 ,Accepted 10 March 2010.

References 

  1. Abeles AM, Pillinger MH, Solitar BM, Abeles M. Narrative review: the pathophysiology of fibromyalgia. Ann Intern Med. 2007;146:726–734
  2. 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. 2006;117:1536–1544
  3. Bajbouj M, Lisanby SH, Lang UE, Danker-Hopfe H, Heuser I, Neu P. Evidence for impaired cortical inhibition in patients with unipolar major depression. Biol Psychiatry. 2006;59:395–400
  4. Beck AT, Rial WY, Rickels K. Short form of depression inventory: cross-validation. Psychol Rep. 1974;34:1184–1186
  5. Burckhardt CS, Clark SR, Bennett RM. The fibromyalgia impact questionnaire: development and validation. J Rheumatol. 1991;18:728–733
  6. Burgmer M, Pogatzki-Zahn E, Gaubitz M, Wessoleck E, Heuft G, Pfleiderer B. Altered brain activity during pain processing in fibromyalgia. NeuroImage. 2009;44:502–508
  7. Casale R, Sarzi-Puttini P, Atzeni F, Gazzoni M, Buskila D, Rainoldi A. Central motor control failure in fibromyalgia: a surface electromyography study. BMC Musculoskelet Disord. 2009;10:78
  8. Cleeland CS, Ryan KM. Pain assessment: global use of the Brief Pain Inventory. Ann Acad Med Singapore. 1994;23:129–138
  9. Daskalakis ZJ, Fitzgerald PB, Christensen BK. The role of cortical inhibition in the pathophysiology and treatment of schizophrenia. Brain Res Rev. 2007;56:427–442
  10. Davey NJ, Smith HC, Savic G, Maskill DW, Ellaway PH, Frankel HL. Comparison of input-output patterns in the corticospinal system of normal subjects and incomplete spinal cord injured patients. Exp Brain Res. 1999;127:382–390
  11. Di Lazzaro V, Oliviero A, Meglio M, Cioni B, Tamburrini G, Tonali P, et al. Direct demonstration of the effect of lorazepam on the excitability of the human motor cortex. Clin Neurophysiol. 2000;111:794–799
  12. Di Lazzaro V, Oliviero A, Pilato F, Saturno E, Dileone M, Mazzone P, et al. The physiological basis of transcranial motor cortex stimulation in conscious humans. Clin Neurophysiol. 2004;115:255–266
  13. Di Lazzaro V, Oliviero A, Profice P, Pennisi MA, Pilato F, Zito G, et al. Ketamine increases human motor cortex excitability to transcranial magnetic stimulation. J Physiol. 2003;547:485–496
  14. Di Lazzaro V, Pilato F, Dileone M, Ranieri F, Ricci V, Profice P, et al. GABAA receptor subtype specific enhancement of inhibition in human motor cortex. J Physiol. 2006;575:721–726
  15. Di Lazzaro V, Pilato F, Oliviero A, Dileone M, Saturno E, Mazzone P, et al. Origin of facilitation of motor-evoked potentials after paired magnetic stimulation: direct recording of epidural activity in conscious humans. J Neurophysiol. 2006;96:1765–1771
  16. Edwards RR, Bingham CO, Bathon J, Haythornthwaite JA. Catastrophizing and pain in arthritis, fibromyalgia, and other rheumatic diseases. Arthritis Rheum. 2006;55:325–332
  17. 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. 2005;113:99–105
  18. Fregni F, Freedman S, Pascual-Leone A. Recent advances in the treatment of chronic pain with non-invasive brain stimulation techniques. Lancet Neurol. 2007;6:188–191
  19. Geisser ME, Casey KL, Brucksch CB, Ribbens CM, Appleton BB, Crofford LJ. Perception of noxious and innocuous heat stimulation among healthy women and women with fibromyalgia: association with mood, somatic focus, and catastrophizing. Pain. 2003;102:243–250
  20. Giesecke T, Gracely RH, Williams DA, Geisser ME, Petzke FW, Clauw DJ. The relationship between depression, clinical pain, and experimental pain in a chronic pain cohort. Arthritis Rheum. 2005;52:1577–1584
  21. Gracely RH, Geisser ME, Giesecke T, Grant MA, Petzke F, Williams DA, et al. Pain catastrophizing and neural responses to pain among persons with fibromyalgia. Brain. 2004;127:835–843
  22. Gracely RH, Petzke F, Wolf JM, Clauw DJ. Functional magnetic resonance imaging evidence of augmented pain processing in fibromyalgia. Arthritis Rheum. 2002;46:1333–1343
  23. Graff-Guerrero A, González-Olvera J, Fresán A, Gómez-Martín D, Méndez-Núñez JC, Pellicer F. Repetitive transcranial magnetic stimulation of dorsolateral prefrontal cortex increases tolerance to human experimental pain. Brain Res Cogn Brain Res. 2005;25:153–160
  24. Harris RE, Clauw DJ, Scott DJ, McLean SA, Gracely RH, Zubieta JK. Decreased central mu-opioid receptor availability in fibromyalgia. J Neurosci. 2007;27:10000–10006
  25. Harris RE, Sundgren PC, Craig AD, Kirshenbaum E, Sen A, Napadow V, et al. Elevated insular glutamate in fibromyalgia is associated with experimental pain. Arthritis Rheum. 2009;60:3146–3152
  26. Hassett AL, Cone JD, Patella SJ, Sigal LH. The role of catastrophizing in the pain and depression of women with fibromyalgia syndrome. Arthritis Rheum. 2000;43:2493–2500
  27. Hsu MC, Harris RE, Sundgren PC, Welsh RC, Fernandes CR, Clauw DJ, et al. No consistent difference in gray matter volume between individuals with fibromyalgia and age-matched healthy subjects when controlling for affective disorder. Pain. 2009;143:262–267
  28. Ilic TV, Meintzschel F, Cleff U, Ruge D, Kessler KR, Ziemann U. Short-interval paired-pulse inhibition and facilitation of human motor cortex: the dimension of stimulus intensity. J Physiol. 2002;545:153–167
  29. Kapogiannis D, Wassermann EM. Transcranial magnetic stimulation in clinical pharmacology. Cent Nerv Syst Agents Med Chem. 2008;8:234–240
  30. Keefe FJ, Brown GK, Wallston KA, Caldwell DS. Coping with rheumatoid arthritis pain: catastrophizing as a maladaptive strategy. Pain. 1989;37:51–56
  31. Kobayashi M, Pascual-Leone A. Transcranial magnetic stimulation in neurology. Lancet Neurol. 2003;2:145–156
  32. Kosek E, Ekholm J, Hansson P. Sensory dysfunction in fibromyalgia patients with implications for pathogenic mechanisms. Pain. 1996;68:375–383
  33. Kuchinad A, Schweinhardt P, Seminowicz DA, Wood PB, Chizh BA, Bushnell MC. Accelerated brain gray matter loss in fibromyalgia patients: premature aging of the brain?. J Neurosci. 2007;27:4004–4007
  34. Kujirai T, Caramia MD, Rothwell JC, Day BL, Thompson PD, Ferbert A, et al. Corticocortical inhibition in human motor cortex. J Physiol. 1993;471:501–519
  35. Lautenbacher S, Rollman GB. Possible deficiencies of pain modulation in fibromyalgia. Clin J Pain. 1997;13:189–196
  36. Lefaucheur JP, Drouot X, Menard-Lefaucheur I, Keravel Y, Nguyen JP. Motor cortex rTMS restores defective intracortical inhibition in chronic neuropathic pain. Neurology. 2006;67:1568–1574
  37. Lefaucheur JP, Lucas B, Andraud F, Hogrel JY, Bellivier F, Del Cul A, et al. Inter-hemispheric asymmetry of motor corticospinal excitability in major depression studied by transcranial magnetic stimulation. J Psychiatr Res. 2008;42:389–398
  38. Lefaucheur JP. The use of repetitive transcranial magnetic stimulation (rTMS) in chronic neuropathic pain. Neurophysiol Clin. 2006;36:117–124
  39. Liepert J, Schwenkreis P, Tegenthoff M, Malin JP. The glutamate antagonist riluzole suppresses intracortical facilitation. J Neural Transm. 1997;104:1207–1214
  40. Lutz J, Jäger L, de Quervain D, Krauseneck T, Padberg F, Wichnalek M, et al. White and gray matter abnormalities in the brain of patients with fibromyalgia: a diffusion-tensor and volumetric imaging study. Arthritis Rheum. 2008;58:3960–3969
  41. McDonnell MN, Orekhov Y, Ziemann U. The role of GABA(B) receptors in intracortical inhibition in the human motor cortex. Exp Brain Res. 2006;173:86–93
  42. Mease PJ, Clauw DJ, Arnold LM, Goldenberg DL, Witter J, Williams DA, et al. Fibromyalgia syndrome. J Rheumatol. 2005;32:2270–2277
  43. Mountz JM, Bradley LA, Modell JG, Alexander RW, Triana-Alexander M, Aaron LA, et al. Fibromyalgia in women. Abnormalities of regional cerebral blood flow in the thalamus and the caudate nucleus are associated with low pain threshold levels. Arthritis Rheum. 1995;38:926–938
  44. Nahmias F, Debes C, de Andrade DC, Mhalla A, Bouhassira D. Diffuse analgesic effects of unilateral repetitive transcranial magnetic stimulation (rTMS) in healthy volunteers. Pain. 2009;147:224–232
  45. Passard A, Attal N, Benadhira R, Brasseur L, Saba G, Sichere P, et al. Effects of unilateral repetitive transcranial magnetic stimulation of the motor cortex on chronic widespread pain in fibromyalgia. Brain. 2007;130:2661–2670
  46. Pierrynowski MR, Tiidus PM, Galea V. Women with fibromyalgia walk with an altered muscle synergy. Gait Posture. 2005;22:210–218
  47. Price DD, Staud R. Neurobiology of fibromyalgia syndrome. J Rheumatol Suppl. 2005;75:22–28
  48. Reis J, Swayne OB, Vandermeeren Y, Camus M, Dimyan MA, Harris-Love M, et al. Contribution of transcranial magnetic stimulation to the understanding of cortical mechanisms involved in motor control. J Physiol. 2008;586:325–351
  49. 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. 2000;111:994–1001
  50. Schmidt-Wilcke T, Luerding R, Weigand T, Jürgens T, Schuierer G, Leinisch E, et al. Striatal grey matter increase in patients suffering from fibromyalgia – a voxel-based morphometry study. Pain. 2007;132:S109–S116
  51. Schwenkreis P, Janssen F, Rommel O, Pleger B, Völker B, Hosbach I, et al. Bilateral motor cortex disinhibition in complex regional pain syndrome (CRPS) type I of the hand. Neurology. 2003;61:515–519
  52. Schwenkreis P, Witscher K, Janssen F, Addo A, Dertwinkel R, Zenz M, et al. Influence of the N-methyl-d-aspartate antagonist memantine on human motor cortex excitability. Neurosci Lett. 1999;270:137–140
  53. Staud R, Cannon RC, Mauderli AP, Robinson ME, Price DD, Vierck CJ. Temporal summation of pain from mechanical stimulation of muscle tissue in normal controls and subjects with fibromyalgia syndrome. Pain. 2003;102:87–95
  54. Staud R, Robinson ME, Price DD. Isometric exercise has opposite effects on central pain mechanisms in fibromyalgia patients compared to normal controls. Pain. 2005;118:176–184
  55. Staud R, Robinson ME, Vierck CJ, Price DD. Diffuse noxious inhibitory controls (DNIC) attenuate temporal summation of second pain in normal males but not in normal females or fibromyalgia patients. Pain. 2003;101:167–174
  56. Sullivan MJL, Bishop S, Pivik J. The pain catastrophizing scale: development and validation. Psychol Assess. 1995;7:432–524
  57. Summers J, Johnson S, Pridmore S, Oberoi G. Changes to cold detection and pain thresholds following low and high frequency transcranial magnetic stimulation of the motor cortex. Neurosci Lett. 2004;368:197–200
  58. Valmunen T, Pertovaara A, Taiminen T, Virtanen A, Parkkola R, Jääskeläinen SK. Modulation of facial sensitivity by navigated rTMS in healthy subjects. Pain. 2009;142:149–158
  59. Wolfe F, Ross K, Anderson J, Russell IJ, Hebert L. The prevalence and characteristics of fibromyalgia in the general population. Arthritis Rheum. 1995;38:19–28
  60. Wolfe F, Smythe HA, Yunus MB, Bennett RM, Bombardier C, Goldenberg DL, et al. The American College of Rheumatology 1990 criteria for the classification of fibromyalgia. Report of the Multicenter Criteria Committee. Arthritis Rheum. 1990;33:160–172
  61. Wood PB, Patterson JC, Sunderland JJ, Tainter KH, Glabus MF, Lilien DL. Reduced presynaptic dopamine activity in fibromyalgia syndrome demonstrated with positron emission tomography: a pilot study. J Pain. 2007;8:51–58
  62. Ziemann U. TMS and drugs. Clin Neurophysiol. 2004;115:1717–1729
  63. Ziemann U, Chen R, Cohen LG, Hallett M. Dextromethorphan decreases the excitability of the human motor cortex. Neurology. 1998;51:1320–1324
  64. Ziemann U, Lonnecker S, Steinhoff BJ, Paulus W. The effect of lorazepam on the motor cortical excitability in man. Exp Brain Res. 1996;109:127–135
  65. Ziemann U, Rothwell JC, Ridding MC. Interaction between intracortical inhibition and facilitation in human motor cortex. J Physiol. 1996;496:873–881
  66. Zigmond AS, Snaith RP. The hospital anxiety and depression scale. Acta Psychiatr Scand. 1983;67:361–370

PII: S0304-3959(10)00158-2

doi: 10.1016/j.pain.2010.03.009

PAIN
Volume 149, Issue 3 , Pages 495-500 , June 2010