Movement observation-induced modulation of pain perception and motor cortex excitability

Clinical Neurophysiology

Volumn 126, Issue 6, 2015, Pages 1204-1211

  Volz, Magdalena Sarah ^a,b   Suarez Contreras, Vanessa ^a   Portilla, Andrea L Santos ^a   Illigens, Ben ^a   Bermpohl, Felix ^b   Fregni, Felipe ^a,c  

^a HARVARD MEDICAL SCHOOL   (United States)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Corticospinal excitability; M1; Motor cortex; Movement observation; Pain

Indexed keywords

ADULT; ALGOMETER; ANXIETY; ARTICLE; BODY MOVEMENT; CONTROLLED STUDY; EXPLORATORY RESEARCH; HAND MOVEMENT; HUMAN; HUMAN EXPERIMENT; MALE; MOTOR PERFORMANCE; NERVE EXCITABILITY; NERVE STIMULATOR; NEUROMODULATION; NOCICEPTION; NORMAL HUMAN; PRESSURE PAIN THRESHOLD; PRIMARY MOTOR CORTEX; PRIORITY JOURNAL; PURDUE PEGBOARD TEST; PYRAMIDAL TRACT; TRANSCRANIAL MAGNETIC STIMULATION; VISUAL ANALOG SCALE; ADOLESCENT; DOUBLE BLIND PROCEDURE; EVOKED MUSCLE RESPONSE; HAND; MIDDLE AGED; MOTOR CORTEX; MOVEMENT (PHYSIOLOGY); PAIN THRESHOLD; PHOTOSTIMULATION; PHYSIOLOGY; PROCEDURES; RANDOMIZED CONTROLLED TRIAL; YOUNG ADULT;

ADOLESCENT; ADULT; DOUBLE-BLIND METHOD; EVOKED POTENTIALS, MOTOR; HAND; HUMANS; MALE; MIDDLE AGED; MOTOR CORTEX; MOVEMENT; PAIN PERCEPTION; PAIN THRESHOLD; PHOTIC STIMULATION; TRANSCRANIAL MAGNETIC STIMULATION; YOUNG ADULT;

EID: 84928730719     PISSN: 13882457     EISSN: 18728952     Source Type: Journal    
DOI: 10.1016/j.clinph.2014.09.022     Document Type: Article

References (70)

1. Anderson W.S., Weiss N., Lawson H.C., Ohara S., Rowland L., Lenz F.A. Demonstration of motor imagery movement and phantom movement-related neuronal activity in human thalamus. Neuroreport 2010, 22:88-92.
2. Ansari A.H., Oghabian M.A., Hossein-Zadeh G.A. Assessment of functional and structural connectivity between motor cortex and thalamus using fMRI and DWI. Conf Proc IEEE Eng Med Biol Soc 2012, 2011:5056-5059.
3. Battaglia F., Lisanby S.H., Freedberg D. Corticomotor excitability during observation and imagination of a work of art. Front Hum Neurosci 2011, 5:79.
4. Beck A.T., Steer R.A. Internal consistencies of the original and revised Beck Depression Inventory. J Clin Psychol 1984, 40:1365-1367.
5. Bermpohl F., Fregni F., Boggio P.S., Thut G., Northoff G., Otachi P.T., et al. Effect of low-frequency transcranial magnetic stimulation on an affective go/no-go task in patients with major depression: role of stimulation site and depression severity. Psychiatry Res 2006, 141:1-13.
6. Biagi L., Cioni G., Fogassi L., Guzzetta A., Tosetti M. Anterior intraparietal cortex codes complexity of observed hand movements. Brain Res Bull 2010, 81(4-5):434-440.
7. Bolognini N., Olgiati E., Maravita A., Ferraro F., Fregni F. Motor and parietal cortex stimulation for phantom limb pain and sensations. Pain 2013, 154:1274-1280.
8. Borroni P., Baldissera F. Activation of motor pathways during observation and execution of hand movements. Soc Neurosci 2008, 3:276-288.
9. Castillo Saavedra L., Mendonca M., Fregni F. Role of the primary motor cortex in the maintenance and treatment of pain in fibromyalgia. Med Hypotheses 2014, 83:332-336.
10. Chesterton L.S., Barlas P., Foster N.E., Lundeberg T., Wright C.C., Baxter G.D. Sensory stimulation (TENS): effects of parameter manipulation on mechanical pain thresholds in healthy human subjects. Pain 2002, 99:253-262.
11. Decety J., Grezes J., Costes N., Perani D., Jeannerod M., Procyk E., et al. Brain activity during observation of actions. Influence of action content and subject's strategy. Brain 1997, 120:1763-1777.
12. Desy M.C., Theoret H. Modulation of motor cortex excitability by physical similarity with an observed hand action. PLoS One 2007, 2:e971.
13. Di Lazzaro V., Pilato F., Saturno E., Oliviero A., Dileone M., Mazzone P., et al. Theta-burst repetitive transcranial magnetic stimulation suppresses specific excitatory circuits in the human motor cortex. J Physiol 2005, 565:945-950.
14. Dube J.A., Mercier C. Effect of pain and pain expectation on primary motor cortex excitability. Clin Neurophysiol 2011, 122:2318-2323.
15. Fadiga L., Fogassi L., Pavesi G., Rizzolatti G. Motor facilitation during action observation: a magnetic stimulation study. J Neurophysiol 1995, 73:2608-2611.
16. Fecteau S., Lassonde M., Theoret H. Modulation of motor cortex excitability during action observation in disconnected hemispheres. Neuroreport 2005, 16:1591-1594.
17. Feurra M., Bianco G., Polizzotto N.R., Innocenti I., Rossi A., Rossi S. Cortico-cortical connectivity between right parietal and bilateral primary motor cortices during imagined and observed actions: a combined TMS/tDCS study. Front Neural Circuits 2011, 5:10.
18. Fourkas A.D., Avenanti A., Urgesi C., Aglioti S.M. Corticospinal facilitation during first and third person imagery. Exp Brain Res 2006, 168:143-151.
19. Fregni F., Boggio P.S., Lima M.C., Ferreira M.J., Wagner T., Rigonatti S.P., 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 2006, 122:197-209.
20. 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.
21. Fregni F., Gimenes R., Valle A.C., Ferreira M.J., Rocha R.R., 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.
22. Fregni F., Valle A.C., Otachi P., Thut G., Rigonatti S.P., Marcolin M.A., et al. Homeostatic effects of plasma valproate levels on corticospinal excitability changes induced by 1Hz rTMS in patients with juvenile myoclonic epilepsy. Clin Neurophysiol 2006, 117:1217-1227.
23. Funase K., Tabira T., Higashi T., Liang N., Kasai T. Increased corticospinal excitability during direct observation of self-movement and indirect observation with a mirror box. Neurosci Lett 2007, 419:108-112.
24. Gangitano M., Mottaghy F.M., Pascual-Leone A. Modulation of premotor mirror neuron activity during observation of unpredictable grasping movements. Eur J Neurosci 2004, 20:2193-2202.
25. Gangitano M., Mottaghy F.M., Pascual-Leone A. Phase-specific modulation of cortical motor output during movement observation. Neuroreport 2001, 12:1489-1492.
26. Gopin C.B., Burdick K.E., Derosse P., Goldberg T.E., Malhotra A.K. Emotional modulation of response inhibition in stable patients with bipolar I disorder: a comparison with healthy and schizophrenia subjects. Bipolar Disord 2011, 13:164-172.
27. Heide G., Witte O.W., Ziemann U. Physiology of modulation of motor cortex excitability by low-frequency suprathreshold repetitive transcranial magnetic stimulation. Exp Brain Res 2006, 171:26-34.
28. Hodges P.W., Smeets R.J. Interaction between pain, movement and physical activity: short-term benefits, long-term consequences, and targets for treatment. Clin J Pain 2014, [Epub ahead of print].
29. Hurlow A., Bennett M.I., Robb K.A., Johnson M.I., Simpson K.H., Oxberry S.G. Transcutaneous electric nerve stimulation (TENS) for cancer pain in adults. Cochrane Database Syst Rev 2012, 3:CD006276.
30. Izumi S.F.T., Ikai T., Andrews J., Daum M., Chino N. Facilitatory effect of thinking about movement on motor-evoked potentials to transcranial magnetic stimulation of the brain. Am J Phys Med Rehabil 1995, 74:207-213.
31. Kallioniemi E., Saisanen L., Kononen M., Awiszus F., Julkunen P. On the estimation of silent period thresholds in transcranial magnetic stimulation. Clin Neurophysiol 2014, 125:2247-2252.
32. Kasai T.K.S., Kawanishi M., Yahagi S. Evidence for facilitation of motor evoked potentials (MEPs) induced by motor imagery. Brain Res 1997, 744:147-150.
33. Kobayashi M., Pascual-Leone A. Transcranial magnetic stimulation in neurology. Lancet Neurol 2003, 2:145-156.
34. Kwon Y., Ko M., Ahn S., Kim Y., Song J., Lee C., et al. Primary motor cortex activation by transcranial direct current stimulation in the human brain. Neurosci Lett 2008, 11:56-59.
35. Lefaucheur J., Antal A., Ahdab R., Ciampi de Andrade D., Fregni F., Khedr E., et al. The use of repetitive transcranial magnetic stimulation (rTMS) and transcranial direct current stimulation (tDCS) to relieve pain. Brain Stimul 2008, 1:337-344.
36. Lefaucheur J.P., Drouot X., Ménard-Lefaucheur I., Keravel Y., Nguyen J.P. Motor cortex rTMS restores defective intracortical inhibition in chronic neuropathic pain. Neurology 2006, 67:1568-1574.
37. Longo M.R., Iannetti G.D., Mancini F., Driver J., Haggard P. Linking pain and the body: neural correlates of visually induced analgesia. J Neurosci 2012, 32:2601-2607.
38. Maeda F., Kleiner-Fisman G., Pascual-Leone A. Motor facilitation while observing hand actions: specificity of the effect and role of observer's orientation. J Neurophysiol 2002, 87:1329-1335.
39. Matthys K., Smits M., Van der Geest J., Van der Lugt A., Seurinck R. Mirror-induced visual illusion of hand movements: a functional magnetic resonance imaging study. Arch Phys Med Rehabil 2009, 90:675-681.
40. Mhalla A., Baudic S., Ciampi de Andrade D., Gautron M., Perrot S., Teixeira M.J., et al. Long-term maintenance of the analgesic effects of transcranial magnetic stimulation in fibromyalgia. Pain 2011, 152:1478-1485.
41. Misra G., Coombes S.A. Neuroimaging evidence of motor control and pain processing in the human midcingulate cortex. Cereb Cortex 2014, 10.1093/cercor/bhu001.
42. Muller K., Bacht K., Prochnow D., Schramm S., Seitz R.J. Activation of thalamus in motor imagery results from gating by hypnosis. Neuroimage 2012, 66C:361-367.
43. Murakami T., Restle J., Ziemann U. Observation-execution matching and action inhibition in human primary motor cortex during viewing of speech-related lip movements or listening to speech. Neuropsychologia 2011, 49:2045-2054.
44. Oldfield R.C. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 1971, 9:97-113.
45. Ossipov M.H., Dussor G.O., Porreca F. Central modulation of pain. J Clin Invest 2010, 120:3779-3787.
46. 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.
47. Pell G., Roth Y., Zangen A. Modulation of cortical excitability induced by repetitive transcranial magnetic stimulation: influence of timing and geometrical parameters and underlying mechanisms. Prog Neurobiol 2011, 93:59-98.
48. Peters M.L., Schmidt A.J., Van den Hout M.A., Koopmans R., Sluijter M.E. Chronic back pain, acute postoperative pain and the activation of diffuse noxious inhibitory controls (DNIC). Pain 1992, 50:177-187.
49. Ramachandran V.S., Altschuler E.L. The use of visual feedback, in particular mirror visual feedback, in restoring brain function. Brain 2009, 132:1693-1710.
50. Reyns N., Derambure P., Duhamel A., Bourriez J.L., Blond S., Houdayer E. Motor cortex stimulation modulates defective central beta rhythms in patients with neuropathic pain. Clin Neurophysiol 2012, 124:761-769.
51. Ribaud A., Tavares I., Viollet E., Julia M., Herisson C., Dupeyron A. Which physical activities and sports can be recommended to chronic low back pain patients after rehabilitation?. Ann Phys Rehabil Med 2013, 56:576-594.
52. Rizzolatti G., Fadiga L., Matelli M., Bettinardi V., Paulesu E., Perani D., et al. Localization of grasp representations in humans by PET: 1. Observation versus execution. Exp Brain Res 1996, 111:246-252.
53. Roosink M., Zijdewind I. Corticospinal excitability during observation and imagery of simple and complex hand tasks: implications for motor rehabilitation. Behav Brain Res 2010, 213:35-41.
54. Rossi S., Hallett M., Rossini P.M., Pascual-Leone A. Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin Neurophysiol 2009, 120:2008-2039.
55. Samargia S., Schmidt R., Kimberley T.J. Shortened cortical silent period in adductor spasmodic dysphonia: evidence for widespread cortical excitability. Neurosci Lett 2013, 560:12-15.
56. Smith M.J., Keel J.C., Greenberg B.D., Adams L.F., Schmidt P.J., Rubinow D.A., et al. Menstrual cycle effects on cortical excitability. Neurology 1999, 53:2069-2072.
57. Soler M.D., Kumru H., Pelayo R., Vidal J., Tormos J.M., Fregni F., et al. Effectiveness of transcranial direct current stimulation and visual illusion on neuropathic pain in spinal cord injury. Brain 2010, 133:2565-2577.
58. Stetkarova I., Leis A.A., Stokic D.S., Delapasse J.S., Tarkka I.M. Characteristics of the silent period after transcranial magnetic stimulation. Am J Phys Med Rehabil 1994, 73:98-102.
59. Strafella A.P., Paus T. Modulation of cortical excitability during action observation: a transcranial magnetic stimulation study. Neuroreport 2000, 11:2289-2292.
60. Theoret H., Halligan E., Kobayashi M., Fregni F., Tager-Flusberg H., Pascual-Leone A. Impaired motor facilitation during action observation in individuals with autism spectrum disorder. Curr Biol 2005, 15:R84-R85.
61. Tiffin J., Asher E.J. The Purdue pegboard; norms and studies of reliability and validity. J Appl Psychol 1948, 32:234-247.
62. Tsubokawa T., Katayama Y., Yamamoto T., et al. Deafferentation pain and stimulation of the thalamic sensory relay nucleus: clinical and experimental study. Appl Neurophysiol 1985, 48:166-171.
63. Tsubokawa T., Katayama Y., Yamamoto T., Hirayama T. Treatment of thalamic pain by chronic motor cortex stimulation. Pacing Clin Electrophysiol 1991, 14:131-134.
64. Tsubokawa T., Yamamoto T., Katayama Y., Hirayama T., Sibuya H. Thalamic relay nucleus stimulation for relief of intractable pain. Clinical results and beta-endorphin immunoreactivity in the cerebrospinal fluid. Pain 1984, 18:115-126.
65. Villanueva L. Diffuse Noxious Inhibitory Control (DNIC) as a tool for exploring dysfunction of endogenous pain modulatory systems. Pain 2009, 143:161-162.
66. Volz M.S., Suarez-Contreras V., Mendonca M.E., Pinheiro F.S., Merabet L.B., Fregni F. Effects of sensory behavioral tasks on pain threshold and cortical excitability. PLoS One 2013, 8:e52968.
67. Wagle-Shukla A., Ni Z., Gunraj C.A., Bahl N., Chen R. Effects of short interval intracortical inhibition and intracortical facilitation on short interval intracortical facilitation in human primary motor cortex. J Physiol 2009, 587:5665-5678.
68. Woolf C.J. Central sensitization: implications for the diagnosis and treatment of pain. Pain 2010, 152:S2-S15.
69. Xie Y., Huo F., Tang J. Cerebral cortex modulation of pain. Acta Pharmacol Sin 2009, 30:31-41.
70. Zaghi S., Thiele B., Pimentel D., Pimentel T., Fregni F. Assessment and treatment of pain with non-invasive cortical stimulation. Restor Neurol Neurosci 2011, 29:439-451.