Mutual interaction between motor cortex activation and pain in fibromyalgia: EEG-fNIRS study
Autoři:
Eleonora Gentile aff001; Antonio Brunetti aff002; Katia Ricci aff001; Marianna Delussi aff001; Vitoantonio Bevilacqua aff002; Marina de Tommaso aff001
Působiště autorů:
Applied Neurophysiology and Pain Unit, SMBNOS Department, Bari Aldo Moro University, Polyclinic General Hospital, Bari, Italy
aff001; Department of Electrical and Information Engineering, Polytecnic University of Bari, Bari, Italy
aff002
Vyšlo v časopise:
PLoS ONE 15(1)
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pone.0228158
Souhrn
Background
Experimental and clinical studies suggested an analgesic effect on chronic pain by motor cortex activation. The present study explored the complex mechanisms of interaction between motor and pain during performing the slow and fast finger tapping task alone and in concomitant with nociceptive laser stimulation.
Method
The participants were 38 patients with fibromyalgia (FM) and 21 healthy subjects. We used a simultaneous multimodal method of laser-evoked potentials and functional near-infrared spectroscopy to investigate metabolic and electrical changes during the finger tapping task and concomitant noxious laser stimulation. Functional near-infrared spectroscopy is a portable and optical method to detect cortical metabolic changes. Laser-evoked potentials are a suitable tool to study the nociceptive pathways function.
Results
We found a reduced tone of cortical motor areas in patients with FM compared to controls, especially during the fast finger tapping task. FM patients presented a slow motor performance in all the experimental conditions, requesting rapid movements. The amplitude of laser evoked potentials was different between patients and controls, in each experimental condition, as patients showed smaller evoked responses compared to controls. Concurrent phasic pain stimulation had a low effect on motor cortex metabolism in both groups nor motor activity changed laser evoked responses in a relevant way. There were no correlations between Functional Near-Infrared Spectroscopy (FNIRS) and clinical features in FM patients.
Conclusion
Our findings indicated that a low tone of motor cortex activation could be an intrinsic feature in FM and generate a scarce modulation on pain condition. A simple and repetitive movement such as that of the finger tapping task seems inefficacious in modulating cortical responses to pain both in patients and controls. The complex mechanisms of interaction between networks involved in pain control and motor function require further studies for the important role they play in structuring rehabilitation strategies.
Klíčová slova:
Analysis of variance – Electroencephalography – Fibromyalgia – Functional electrical stimulation – Hands – Lasers – Motor cortex – Signal filtering
Zdroje
1. Wolfe F, Clauw DJ, Fitzcharles M, Goldenberg DL, Katz RS, Mease P, et al. The American College of Rheumatology preliminary diagnostic criteria for fibromyalgia and measurement of symptom severity. Arthritis Care and Research. 2010; 62(5): 600–610. doi: 10.1002/acr.20140 20461783
2. Atzeni F, Talotta R, Masala IF, Giacomelli C, Conversano C, Nucera V,et al.. One year review 2019: fibromyalgia. Clin exp Rheumatol. 2019;37 Suppl 116(1): 3–10.
3. Mease PJ, Arnold LM, Crofford LJ, Williams DA, Russell IJ, Humphrey L, et al. Identifying the clinical domains of fibromyalgia: contributions from clinician and patient delphi exercises. Arthritis Rheum. 2008; 59:952–960. doi: 10.1002/art.23826 18576290
4. Knijnik LM, Dussan-Sarria JA, Rozisky JR, Torres IL, Brunoni AR, Fregni F, et al. Repetitive transcranial magnetic stimulation for fibromyalgia: systematic review and meta-analysis. Pain Pract. 2015; 16(3): 294–304. doi: 10.1111/papr.12276 25581213
5. O’Connell NE, Marston L, Spencer S, DeSouza LH, Wand BM (2010) Non-invasive brain stimulation techniques for chronic pain. Cochrane Database Syst Rev. 9: CD008208. doi: 10.1002/14651858
6. Fagerlund AJ, Hansen OA, Aslaksen PM. Transcranial direct current stimulation as a treatment for patients with fibromyalgia. Pain. 2015; 156: 62–71. doi: 10.1016/j.pain.0000000000000006 25599302
7. Fregni F, Gimenes R, Valle AC, Ferreira MJL, Rocha RR, Natalle L, et al. A randomized, sham-controlled, proof of principle study of transcranial direct current stimulation for the treatment of pain in fibromyalgia. Arthritis Rheum. 2006; 54: 3988–3998. doi: 10.1002/art.22195 17133529
8. Valle A, Roizenblatt S, Botte S, Zaghi S, Riberto M, Tufik S, et al. Efficacy of anodal transcranial direct current stimulation (tDCS) for the treatment of fibromyalgia: results of a randomized, sham-controlled longitudinal clinical trial. J Pain Manag. 2009; 2: 353–361. 21170277
9. Polanía R, Paulus W, Nitsche MA. Modulating cortico-striatal and thalamo-cortical functional connectivity with transcranial direct current stimulation. Hum Brain Mapp. 2012; 33: 2499–2508. doi: 10.1002/hbm.21380 21922602
10. Chang WJ, O'Connell NE, Burns E, Chipchase LS, Liston MB, Schabrun SM. Organisation and function of the primary motor cortex in chronic pain: protocol for a systematic review and meta-analysis. BMJ Open. 2015;5(11): e008540. doi: 10.1136/bmjopen-2015-008540 26621512
11. Busch AJ, Webber SC, Brachaniec M, Bidonde J, Bello-Haas VD, Danyliw AD, et al. Exercise therapy for fibromyalgia. Curr. Pain Headache Rep. 2011; 15(5): 358–367. doi: 10.1007/s11916-011-0214-2 21725900
12. La Bianca G, Curatolo M, Romano M, Fierro B, Brighina F. Motor cortex tRNS ameliorates pain, anxiety, depression, quality of life and cognitive impairment in patients with fibromyalgia: preliminary results of a randomized sham-controlled trial. Neurology. 2017; 88 (16 Supplement): S219
13. Köklü K, Sarigül M, Özişler Z, Şirzai H, Özel S. Handgrip Strength in Fibromyalgia, Archives of Rheumatology. 2016; 31(2): 158–161.
14. Devrimsel G, Turkyilmaz AK, Beyazal MS, Karkucak M. Assessment of hand function and disability in fibromyalgia. Z Rheumatol. 2019; 78(9): 889–893 doi: 10.1007/s00393-018-0558-7 30324279
15. Schachter CL, Busch AJ, Peloso PM, Sheppard MS. Effects of short versus long bouts of aerobic exercise in sedentary women with fibromyalgia: a randomized controlled trial. Phys. Ther. 2003; 83(4): 340–358. 12665405
16. Bair MJ, Matthias MS, Nyland KA, Huffman MA, Stubbs DL, Kroenke K, et al. Barriers and facilitators to chronic pain self-management: a qualitative study of primary care patients with comorbid musculoskeletal pain and depression. Pain Med. 2009; 10(7): 1280–1290. doi: 10.1111/j.1526-4637.2009.00707.x 19818038
17. Shin J, von Lühmann A, Kim DW, Mehnert J, Hwang HJ, Müller KR. Simultaneous acquisition of EEG and NIRS during cognitive tasks for an open access dataset. Sci Data. 2018; 5:180003. doi: 10.1038/sdata.2018.3 29437166
18. Gentile E, Ricci K, Delussi M, de Tommaso M. Motor cortex function in fibromyalgia: a pilot study by near-infrared spectroscopy and laser evoked potentials co-recording. Functional Neurology. 2019; 34(2): 107–118.. 31556391
19. Zama T, Shimada S. Simultaneous measurement of electroencephalography and near-infrared spectroscopy during voluntary motor preparation. Scientific reports. 2015; 5: 16438. doi: 10.1038/srep16438 26574186
20. Ahn S, Jun SC. Multi-Modal Integration of EEG-fNIRS for Brain-Computer Interfaces—Current Limitations and Future Directions. Front Hum Neurosci. 2017; 11: 503. doi: 10.3389/fnhum.2017.00503 29093673
21. Gentile E, Ricci K, Delussi M, Brighina F, de Tommaso M. Motor Cortex Function in Fibromyalgia: A Study by Functional Near-Infrared Spectroscopy. Pain Research and Treatment. 2019; doi: 10.1155/2019/2623161
22. Oldfield RC. The assessment and analysis of handedness: The Edinburgh inventory, Neuropsychologia. 1971; 9: 97–113.
23. Sarzi-Puttini P, Atzeni F, Fiorini T, Panni B, Randisi G, Turiel M, Carrabba M. Validation of an Italian version of the Fibromyalgia Impact Questionnaire (FIQ-I), Clin Exp Rheumatol. 2003; 21(4): 459–464. 12942697
24. Moyano S, Kilstein JG, Alegre de Miguel C. New diagnostic criteria for fibromyalgia: Here to stay?. Reumatol Clin. 2015; 11(4): 210–214. doi: 10.1016/j.reuma.2014.07.008 25443560
25. Zung WW (1971) A rating instrument for anxiety disorders. Psychosomatics, 12: 371–379. doi: 10.1016/S0033-3182(71)71479-0 5172928
26. Zung WW (1965) A self-rating depression scale. Archives of General Psychiatry, 12: 63–70. doi: 10.1001/archpsyc.1965.01720310065008 14221692
27. Belza B, Miyawaki CE, Liu M, Aree-Ue S, Fessel M, Minott KR, et al. A Systematic Review of Studies Using the Multidimensional Assessment of Fatigue Scale. J Nurs Meas. 2018; 26(1): 36–75. doi: 10.1891/1061-3749.26.1.36 29724278
28. Kuboyama N, Nabetani T, Shibuya K, Machida K, Ogaki T. The effect of maximal finger tapping on cerebral activation. Journal of physiological anthropology and applied human science. 2004; 23: 105–110. doi: 10.2114/jpa.23.105 15314267
29. Treede RD, Lorenz J, Baumgärtner U. Clinical usefulness of laser-evoked potentials. Neurophysiol Clin. 2003; 33(6): 303–314. doi: 10.1016/j.neucli.2003.10.009 14678844
30. de Tommaso M, Ricci K, Libro G, Vecchio E, Delussi M, Montemurno A, et al. Pain Processing and Vegetative Dysfunction in Fibromyalgia: A Study by Sympathetic Skin Response and Laser Evoked Potentials. Pain Res Treat. 2017; 28. doi: 10.1155/2017/9747148
31. Xu Y, Graber H, Barbour R. Nirlab user manual. Available from: https://www.nitrc.org/frs/shownotes.php?release_id=2663.
32. Cope M, Delpy DT. System for long-term measurement of cerebral blood and tissue oxygenation on newborn infants by near infra-red transillumination. Medical & Biological Engineering & Computing. 1988; 26(3): 289–294.
33. Baker WB, Parthasarathy AB, Busch DR, Mesquita RC, Greenberg JH, Yodh AG. Modified Beer-Lambert law for blood flow. Biomedical optics express. 2014; 5(11): 4053–4075. doi: 10.1364/BOE.5.004053 25426330
34. Valeriani M, Rambaud L, Mauguière F. Scalp topography and dipolar source modelling of potentials evoked by CO2 laser stimulation of the hand. Electroencephalography and Clinical Neurophysiology. 1996; 100(4): 343–353. doi: 10.1016/0168-5597(96)95625-7 17441304
35. Ye JC, Tak S, Jang KE, Jung J, Jang J. NIRS-SPM: statistical parametric mapping for near-infrared spectroscopy. Neuroimage. 2009; 44(2): 428–447. doi: 10.1016/j.neuroimage.2008.08.036 18848897
36. Arun KM, Smitha KA, Rajesh PG, Kesavadas C. Functional near-infrared spectroscopy is in moderate accordance with functional MRI in determining lateralisation of frontal language areas. The neuroradiology journal. 2018; 31(2): 133–141. doi: 10.1177/1971400917739083 29072554
37. Seghier ML. Laterality index in functional MRI: methodological issues. Magnetic resonance imaging. 2008; 26(5): 594–601. doi: 10.1016/j.mri.2007.10.010 18158224
38. Wolfe F. Pain extent and diagnosis: development and validation of the regional pain scale in 12,799 patients with rheumatic disease. J Rheumatol. 2003; 30(2): 369–378. 12563698
39. Witt ST, Laird AR, Meyerand ME. Functional neuroimaging correlates of finger-tapping task variations: an ALE meta-analysis. NeuroImage. 2008; 42(1): 343–356. doi: 10.1016/j.neuroimage.2008.04.025 18511305
40. Costa ID, Gamundí A, Miranda JG, França LG, De Santana CN, Montoya P. Altered Functional Performance in Patients with Fibromyalgia. Frontiers in human neuroscience. 2017; 11: 14. doi: 10.3389/fnhum.2017.00014 28184193
41. Canny ML, Thompson JM, Wheeler MJ. Reliability of the box and block test of manual dexterity for use with patients with fibromyalgia. American Journal of Occupational Therapy. 2009; 63(4): 506–510. doi: 10.5014/ajot.63.4.506 19708480
42. Nijs J, Roussel N, Van Oosterwijck J, De Kooning M, Ickmans K, Struyf F,et al. Fear of movement and avoidance behaviour toward physical activity in chronic-fatigue syndrome and fibromyalgia: state of the art and implications for clinical practice. Clin Rheumatol. 2013; 32(8): 1121–1129. doi: 10.1007/s10067-013-2277-4 23639990
43. Leavitt F, Katz RS. Cognitive dysfunction in fibromyalgia: slow access to the mental lexicon. Psychol Rep. 2014; 115(3): 828–839. doi: 10.2466/04.15.PR0.115c32z1 25539171
44. Togo F, Lange G, Natelson BH, Quigley KS. Attention network test: assessment of cognitive function in chronic fatigue syndrome. J Neuropsychol. 2015; 9(1): 1–9. doi: 10.1111/jnp.12030 24112872
45. Rasouli O, Fors EA, Borchgrevink PC, Öhberg F, Stensdotter AK. Gross and fine motor function in fibromyalgia and chronic fatigue syndrome. Journal of pain research. 2017; 10: 303–309. doi: 10.2147/JPR.S127038 28223840
46. Clauw DJ. Fibromyalgia: a clinical review. Jama. 2014; 311(15): 1547–1555. doi: 10.1001/jama.2014.3266 24737367
47. Chang WJ, O’Connell NE, Beckenkamp PR, Alhassani G, Liston MB, Schabrun SM. Altered Primary Motor Cortex Structure, Organization, and Function in Chronic Pain: A Systematic Review and Meta-Analysis. The Journal of Pain. 2018; 19(4): 341–359.
48. Mercier C, Léonard G. Interactions between pain and the motor cortex: insights from research on phantom limb pain and complex regional pain syndrome. Physiotherapy Canada. Physiotherapie Canada. 2011; 63(3): 305–314. doi: 10.3138/ptc.2010-08p 22654236
49. Lefaucheur JP, Drouot X, Ménard-Lefaucheur I, Keravel Y, Nguyen JP. Motor cortex rTMS restores defective intracortical inhibition in chronic neuropathic pain. Neurology. 2006; 67(9): 1568–1574. doi: 10.1212/01.wnl.0000242731.10074.3c 17101886
50. Maihӧfner C, Baron R, DeCol R, Binder A, Birklein F, Deuschl G, et al. The motor system shows adaptive changes in complex regional pain syndrome. Brain. 2007; 130(10): 2671–2687.
51. Parker RS, Lewis GN, Rice DA, McNair PJ. Is Motor Cortical Excitability Altered in People with Chronic Pain? A Systematic Review and Meta-Analysis, Brain Stimulation. 2016; 9(4): 488–500. doi: 10.1016/j.brs.2016.03.020 27133804
52. Cha M, Um SW, Kwon M, Nam TS, Lee BH. Repetitive motor cortex stimulation reinforces the pain modulation circuits of peripheral neuropathic pain. Scientific Reports. 2017; 7(1): 7986. doi: 10.1038/s41598-017-08208-2 28801619
53. Farina S, Tinazzi M, Le Pera D, Valeriani M. Pain-related modulation of the human motor cortex. Neurological Research. 2003; 25:(2): 130–142. doi: 10.1179/016164103101201283 12635511
54. Zhao X, Xu M, Jorgenson K, Kong J. Neurochemical changes in patients with chronic low back pain detected by proton magnetic resonance spectroscopy: a systematic review. Neuroimage Clin. 2016; 13: 33–38. doi: 10.1016/j.nicl.2016.11.006 27920977
55. de Tommaso M, Nolano M, Iannone F, Vecchio E, Ricci K, Lorenzo M, et al.. Update on laser evoked potential findings in fibromyalgia patients in light of clinical and skin biopsy features. J Neurol. 2014; 261(3): 461–472. doi: 10.1007/s00415-013-7211-9 24366650
56. Martìnez-Lavin M. Fibromyalgia and small fiber neuropathy: the plot thickens! Clin Rheumatol. 2018; 37(12): 3167–3171. doi: 10.1007/s10067-018-4300-2 30238382
57. Garcia-Larrea L, Frot M, Valeriani M. Brain generators of laser-evoked potentials: from dipole to finctional significance. Neurophysiol Clin. 2003; 33(6): 279–292. doi: 10.1016/j.neucli.2003.10.008 14678842
58. Le Pera D, Brancucci A, De Armas L, Del Percio C, Miliucci R, Babiloni C, et al. Inhibitory effect of voluntary movement preparation on cutaneous heat pain and laser-evoked potentials. Eur J Neurosci. 2007; 25(6): 1900–1907. doi: 10.1111/j.1460-9568.2007.05389.x 17432974
59. Mouraux A, Diukova A, Lee MC, Wise RG, Iannetti GD. A multisensory investigation of the functional significance of the “pain matrix”. Neuorimage. 2011; 54(3): 2237–2249.
60. Garcia-Larrea L, Peyron R. Motor cortex stimulation for neuropathic pain: From phenomenology to mechanisms. Neuroimage. 2007; 37 (Suppl 1): S71–79.
61. Passard A, Attal N, Benadhira R, Brasseur L, Saba G, Sichere P, at al.. Effects of unilateral repetitive transcranial magnetic stimulation of the motor cortex on chronic widespread pain in fibromyalgia. Brain. 2007; 130(10): 2611–2670.
62. Brighina F, Curatolo M, Cosentino G, de Tommaso M, Battaglia G, Sarzi-Puttini PC, et al.Brain modulation by electric currents in fibromyalgia: a structured review on non-invasive approach with transcranial electrical stimulation. Front Hum Neurosci. 2019; 11: 14–40.
63. O’Connell NE, Marston L, Spencer S, DeSouza LH, Wand BM. Non-invasive brain stimulation techniques for chronic pain. Cochrane Database of Systematic Reviews. 2018; 3: CD008208. doi: 10.1002/14651858.CD008208.pub4 29547226
64. de Tommaso M, Brighina F, Fierro B, Francesco VD, Santostasi R, Sciruicchio V, et al.Effects of high-frequency repetitive trasncranial magnetic stimulation of primary motor cortex on laser-evoked potentials in migraine. J Headache Pain. 2010; 11(6): 505–512. doi: 10.1007/s10194-010-0247-7 20714776
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