Cerebellar direct current stimulation modulates pain perception in humans

Restorative Neurology and Neuroscience

Volumn 33, Issue 5, 2015, Pages 597-609

  Bocci, Tommaso ^a,b   Santarcangelo, Enrica ^a   Vannini, Beatrice ^a   Torzini, Antonio ^a,b   Carli, Giancarlo ^b   Ferrucci, Roberta ^c   Priori, Alberto ^c   Valeriani, Massimiliano ^d,e   Sartucci, Ferdinando ^a  

^a UNIVERSITY OF PISA   (Italy)

^b UNIVERSITY OF SIENA   (Italy)

^c UNIVERSITY OF MILAN   (Italy)

^d BAMBINO GESÙ CHILDREN S HOSPITAL   (Italy)

^e AALBORG UNIVERSITY   (Denmark)

Author keywords

cerebellar direct current stimulation; laser evoked potentials; Pain cerebellum; pain modulation; tDCS

Indexed keywords

ADULT; ARTICLE; CLINICAL ARTICLE; ELECTROPHYSIOLOGICAL PROCEDURES; EVOKED MUSCLE RESPONSE; EVOKED RESPONSE; FEMALE; HUMAN; LASER; LATENT PERIOD; MALE; NOCICEPTION; NORMAL HUMAN; PAIN INTENSITY; PERCEPTIVE THRESHOLD; POLARIZATION; PRIORITY JOURNAL; TRANSCRANIAL CEREBELLAR DIRECT CURRENT STIMULATION; TRANSCRANIAL DIRECT CURRENT STIMULATION; TRANSCRANIAL MAGNETIC STIMULATION; VISUAL ANALOG SCALE; ANALGESIA; CEREBELLUM; PATHOPHYSIOLOGY; PHYSIOLOGY; PROCEDURES; PSYCHOPHYSICS;

ADULT; CEREBELLUM; EVOKED POTENTIALS; FEMALE; HUMANS; LASERS; MALE; PAIN MANAGEMENT; PAIN PERCEPTION; PSYCHOPHYSICS; TRANSCRANIAL DIRECT CURRENT STIMULATION;

EID: 84941898966     PISSN: 09226028     EISSN: 18783627     Source Type: Journal    
DOI: 10.3233/RNN-140453     Document Type: Article

References (84)

1. Absinta, M., Rocca, M.A., Colombo, B., Falini, A., Comi, G., & Filippi, M. (2012). Selective decreased grey matter volume of the pain-matrix network in cluster headache. Cephalalgia, 32(2), 109-115
2. Agostino, R., Cruccu, G., Iannetti, G., Romaniello, A., Truini, A., & Manfredi, M. (2000). Topographical distribution of pinprick and warmth thresholds to CO2 laser stimulation on the human skin. Neurosci Lett, 285(2), 115-118
3. Antal, A., Brepohl, N., Poreisz, C., Boros, K., Csifcsak, G., & Paulus, W. (2008). Transcranial direct current stimulation over somatosensory cortex decreases experimentally induced acute pain perception. Clin J Pain, 24(1), 56-63
4. Antal, A., & Paulus, W. (2010). Effects of transcranial theta-burst stimulation on acute pain perception. Restor Neurol Neurosci, 28(4), 477-484
5. Apkarian, A.V., Bushnell, M.C., Treede, R.D., & Zubieta, J.K. (2005). Human brain mechanisms of pain perception and regulation in health and disease. Eur J Pain, 9(4), 463-484
6. Balsters, J.H., Whelan, C.D., Robertson, I.H., & Ramnani, N. (2013). Cerebellum and cognition: Evidence for the encoding of higher order rules. Cereb Cortex, 23(6), 1433-1443
7. Battaglia, F., Quartarone, A., Ghilardi, M.F., Dattola, R., Bagnato, S., Rizzo, V., Morgante, L., & Girlanda, P. (2006). Unilateral cerebellar stroke disrupts movement preparation and motor imagery. Clin Neurophysiol, 117(5), 1009-1016
8. Bingel, U., Quante, M., Knab, R., Bromm, B., Weiller, C., & Buchel, C. (2002). Subcortical structures involved in pain processing: Evidence from single-trial fMRI. Pain, 99(1-2), 313-321
9. Boggio, P.S., Zaghi, S., & Fregni, F. (2009). Modulation of emotions associated with images of human pain using anodal transcranial direct current stimulation (tDCS). Neuropsychologia, 47(1), 212-217
10. Boggio, P.S., Zaghi, S., Lopes, M., & Fregni, F. (2008). Modulatory effects of anodal transcranial direct current stimulation on perception and pain thresholds in healthy volunteers. Eur J Neurol, 15(10), 1124-1130
11. Borsook, D., Moulton, E.A., Tully, S., Schmahmann, J.D., & Becerra, L. (2008). Human cerebellar responses to brush and heat stimuli in healthy and neuropathic pain subjects. Cerebellum, 7(3), 252-272
12. Ceko, M., Seminowicz, D.A., Bushnell, M.C., & Olausson, H.W. (2013). Anatomical and functional enhancements of the insula after loss of large primary somatosensory fibers. Cereb Cortex, 23(9), 2017-2024
13. Cruccu, G., Aminoff, M.J., Curio, G., Guerit, J.M., Kakigi, R., Mauguiere, F., Rossini, P.M., Treede, R.D., & Garcia-Larrea, L. (2008). Recommendations for the clinical use of somatosensory-evoked potentials. Clin Neurophysiol, 119(8), 1705-1719
14. Cruccu, G., Romaniello, A., Amantini, A., Lombardi, M., Innocenti, P., & Manfredi, M. (1999). Assessment of trigeminal smallfiber function: Brain and reflex responses evoked by CO2-laser stimulation. Muscle Nerve, 22(4), 508-516
15. Dasilva, A.F., Mendonca, M.E., Zaghi, S., Lopes, M., Dossantos, M.F., Spierings, E.L., Bajwa, Z., Datta, A., Bikson, M., & Fregni, F. (2012). tDCS-induced analgesia and electrical fields in pain-related neural networks in chronic migraine. Headache, 52(8), 1283-1295
16. Duerden, E.G., & Albanese, M.C. (2013). Localization of painrelated brain activation: A meta-Analysis of neuroimaging data. Hum Brain Mapp, 34(1), 109-149
17. Ekerot, C.F., Garwicz, M., & Schouenborg, J. (1991a). The postsynaptic dorsal column pathway mediates cutaneous nociceptive information to cerebellar climbing fibres in the cat. J Physiol, 441, 275-284
18. Ekerot, C.F., Garwicz, M., & Schouenborg, J. (1991b). Topography and nociceptive receptive fields of climbing fibres projecting to the cerebellar anterior lobe in the cat. J Physiol, 441, 257-274
19. Ekerot, C.F., Gustavsson, P., Oscarsson, O., & Schouenborg, J. (1987a). Climbing fibres projecting to cat cerebellar anterior lobe activated by cutaneous A and C fibres. J Physiol, 386, 529-538
20. Ekerot, C.F., Oscarsson, O., & Schouenborg, J. (1987b). Stimulation of cat cutaneous nociceptive C fibres causing tonic and synchronous activity in climbing fibres. J Physiol, 386, 539-546
21. Ferrucci, R., Brunoni, A.R., Parazzini, M., Vergari, M., Rossi, E., Fumagalli, M., Mameli, F., Rosa, M., Giannicola, G., Zago, S., & Priori, A. (2013). Modulating human procedural learning by cerebellar transcranial direct current stimulation. Cerebellum, 12(4), 485-492
22. Ferrucci, R., Giannicola, G., Rosa, M., Fumagalli, M., Boggio, P.S., Hallett, M., Zago, S., & Priori, A. (2012). Cerebellum and processing of negative facial emotions: Cerebellar transcranial DC stimulation specifically enhances the emotional recognition of facial anger and sadness. Cogn Emot, 26(5), 786-799
23. Ferrucci, R., Marceglia, S., Vergari, M., Cogiamanian, F., Mrakic-Sposta, S., Mameli, F., Zago, S., Barbieri, S., & Priori, A. (2008). Cerebellar transcranial direct current stimulation impairs the practice-dependent proficiency increase in working memory. J Cogn Neurosci, 20(9), 1687-1697
24. Fregni, F., Freedman, S., & Pascual-Leone, A. (2007). Recent advances in the treatment of chronic pain with non-invasive brain stimulation techniques. Lancet Neurol, 6(2), 188-191
25. Galea, J.M., Jayaram, G., Ajagbe, L., & Celnik, P. (2009). Modulation of cerebellar excitability by polarity-specific noninvasive direct current stimulation. J Neurosci, 29(28), 9115-9122
26. Galea, J.M., Vazquez, A., Pasricha, N., de Xivry, J.J., & Celnik, P. (2011). Dissociating the roles of the cerebellum and motor cortex during adaptive learning: The motor cortex retains what the cerebellum learns. Cereb Cortex, 21(8), 1761-1770
27. Gandiga, P.C., Hummel, F.C., & Cohen, L.G. (2006). Transcranial DC stimulation (tDCS): A tool for double-blind sham-controlled clinical studies in brain stimulation. Clin Neurophysiol, 117(4), 845-850
28. Garcia-Larrea, L., Peyron, R., Laurent, B., & Mauguiere, F. (1997). Association and dissociation between laser-evoked potentials and pain perception. Neuroreport, 8(17), 3785-3789
29. Grimaldi, G., Argyropoulos, G.P., Boehringer, A., Celnik, P., Edwards, M.J., Ferrucci, R., Galea, J.M., Groiss, S.J., Hiraoka, K., Kassavetis, P., Lesage, E., Manto, M., Miall, R.C., Priori, A., Sadnicka, A., Ugawa, Y., & Ziemann, U. (2014). Non-invasive cerebellar stimulation-A consensus paper. Cerebellum, 13(1), 121-138
30. Groppa, S., Oliviero, A., Eisen, A., Quartarone, A., Cohen, L.G., Mall, V., Kaelin-Lang, A., Mima, T., Rossi, S., Thickbroom, G.W., Rossini, P.M., Ziemann, U., Valls-Sole, J., & Siebner, H.R. (2012). A practical guide to diagnostic transcranial magnetic stimulation: Report of an IFCN committee. Clin Neurophysiol, 123(5), 858-882
31. Hamada, M., Strigaro, G., Murase, N., Sadnicka, A., Galea, J.M., Edwards, M.J., & Rothwell, J.C. (2012). Cerebellar modulation of human associative plasticity. J Physiol, 590(Pt 10), 2365-2374
32. Hess, C.W., Mills, K.R., & Murray, N.M. (1987). Responses in small hand muscles from magnetic stimulation of the human brain. J Physiol, 388, 397-419
33. Hull, C.A., Chu, Y., Thanawala, M., & Regehr, W.G. (2013). Hyperpolarization induces a long-term increase in the spontaneous firing rate of cerebellar Golgi cells. J Neurosci, 33(14), 5895-5902
34. Ihle, K., Rodriguez-Raecke, R., & Luedtke, K., May, A. (2014). tDCS modulates cortical nociceptive processing but has little to no impact on pain perception. Pain, 155(10), 2080-2087
35. Ito, M. (2006). Cerebellar circuitry as a neuronal machine. Prog Neurobiol, 78(3-5), 272-303
36. Iyer, M.B., Mattu, U., Grafman, J., Lomarev, M., Sato, S., & Wassermann, E.M. (2005). Safety and cognitive effect of frontal DC brain polarization in healthy individuals. Neurology, 64(5), 872-875
37. Kelly, R.M., & Strick, P.L. (2003). Cerebellar loops with motor cortex and prefrontal cortex of a nonhuman primate. J Neurosci, 23(23), 8432-8444
38. Lefaucheur, J.P., Andre-Obadia, N., Antal, A., Ayache, S.S., Baeken, C., Benninger, D.H., Cantello, R.M., Cincotta, M., de Carvalho, M., De Ridder, D., Devanne, H., Di Lazzaro, V., Filipovic, S.R., Hummel, F.C., Jaaskelainen, S.K., Kimiskidis, V.K., Koch, G., Langguth, B., Nyffeler, T., Oliviero, A., Padberg, F., Poulet, E., Rossi, S., Rossini, P.M., Rothwell, J.C., Schonfeldt-Lecuona, C., Siebner, H.R., Slotema, C.W., Stagg, C.J., Valls-Sole, J., Ziemann, U., Paulus, W., & Garcia-Larrea, L. (2014). Evidencebased guidelines on the therapeutic use of repetitive transcranial magnetic stimulation (rTMS). Clin Neurophysiol, 125(11), 2150-2206
39. Lefaucheur, J.P., Brusa, A., Creange, A., Drouot, X., & Jarry, G. (2002). Clinical application of laser evoked potentials using the Nd: YAG laser. Neurophysiol Clin, 32(2), 91-98
40. Lefaucheur, J.P., Debray, S., & Jarry, G. (2001). Laser evoked potentials using the Nd: YAG laser. Muscle Nerve, 24(4), 496-501
41. Lefaucheur, J.P., Drouot, X., Menard-Lefaucheur, I., Keravel, Y., & Nguyen, J.P. (2006). Motor cortex rTMS restores defective intracortical inhibition in chronic neuropathic pain. Neurology, 67(9), 1568-1574
42. Longo, M.R., Iannetti, G.D., Mancini, F., Driver, J., & Haggard, P. (2012). Linking pain and the body: Neural correlates of visually induced analgesia. J Neurosci, 32(8), 2601-2607
43. Lorenz, J., & Garcia-Larrea, L. (2003). Contribution of attentional and cognitive factors to laser evoked brain potentials. Neurophysiol Clin, 33(6), 293-301
44. 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(Pt 5), 1079-1091
45. Luedtke, K., May, A., & Jurgens, T.P. (2012). No effect of a single session of transcranial direct current stimulation on experimentally induced pain in patients with chronic low back pain-An exploratory study. PLoS One, 7(11), e48857
46. Mendonca, M.E., Santana, M.B., Baptista, A.F., Datta, A., Bikson, M., Fregni, F., & Araujo, C.P. (2011). Transcranial DC stimulation in fibromyalgia: Optimized cortical target supported by high-resolution computational models. J Pain, 12(5), 610-617
47. Moriguchi, Y., Decety, J., Ohnishi, T., Maeda, M., Mori, T., Nemoto, K., Matsuda, H., & Komaki, G. (2007). Empathy and judging others pain: An fMRI study of alexithymia. Cereb Cortex, 17(9), 2223-2234
48. Moulton, E.A., Elman, I., Pendse, G., Schmahmann, J., Becerra, L., & Borsook, D. (2011). Aversion-related circuitry in the cerebellum: Responses to noxious heat and unpleasant images. J Neurosci, 31(10), 3795-3804
49. Moulton, E.A., Schmahmann, J.D., Becerra, L., & Borsook, D. (2010). The cerebellum and pain: Passive integrator or active participator?. Brain Res Rev, 65(1), 14-27
50. Mouraux, A., & Plaghki, L. (2006). Are the processes reflected by late and ultra-late laser evoked potentials specific of nociception?. Suppl Clin Neurophysiol, 59, 197-204
51. Mylius, V., Jung, M., Menzler, K., Haag, A., Khader, P.H., Oertel, W.H., Rosenow, F., & Lefaucheur, J.P. (2012). Effects of transcranial direct current stimulation on pain perception and working memory. Eur J Pain, 16(7), 974-982
52. Ni, Z., Gunraj, C. & Chen, R. (2007). Short interval intracortical inhibition and facilitation during the silent period in human. J Physiol, 583(Pt 3), 971-982
53. Nitsche, M.A., Liebetanz, D. Lang, N., Antal, A., Tergau, F., & Paulus, W. (2003). Safety criteria for transcranial direct current stimulation (tDCS) in humans. Clin Neurophysiol, 114(11), 2220-2222; author reply 2222-2223
54. Opsommer, E., Guerit, J.M., & Plaghki, L. (2003). Exogenous and endogenous components of ultralate (C-fibre) evoked potentials following CO2 laser stimuli to tiny skin surface areas in healthy subjects. Neurophysiol Clin, 33(2), 78-85
55. Parazzini, M., Fiocchi, S., Liorni, I., Priori, A., & Ravazzani, P. (2014). Computational modeling of transcranial direct current stimulation in the child brain: Implications for the treatment of refractory childhood focal epilepsy. Int J Neural Syst, 24(2), 1430006
56. Parazzini, M., Rossi, E., Ferrucci, R., Fiocchi, S., Liorni, I., Priori, A., & Ravazzani, P. (2013). Computational model of cerebellar transcranial direct current stimulation. Conf Proc IEEE Eng Med Biol Soc, 2013, 237-240
57. Parazzini, M., Rossi, E., Ferrucci, R., Liorni, I., Priori, A., & Ravazzani. P. (2014). Modelling the electric field and the current density generated by cerebellar transcranial DC stimulation in humans. Clin Neurophysiol, 125(3), 577-584
58. Perini, I., Bergstrand, S., & Morrison, I. (2013). Where pain meets action in the human brain. J Neurosci, 33(40), 15930-15939
59. Ploghaus, A., Tracey, I., Gati, J.S., Clare, S., Menon, R.S., Matthews, P.M., & Rawlins, J.N. (1999). Dissociating pain from its anticipation in the human brain. Science, 284(5422), 1979-1981
60. Priori, A., Ciocca, M., Parazzini, M., Vergari, M., & Ferrucci. R. (2014). Transcranial cerebellar direct current stimulation and transcutaneous spinal cord direct current stimulation as innovative tools for neuroscientists. J Physiol 592(Pt 16), 3345-3369
61. Purpura, D.P., & McMurtry, J.C. (1965). Intracellular activities and evoked potential changes during polarization of motor cortex. J Neurophysiol, 28, 166-185
62. Qiu, Y., Inui, K., Wang, X., Tran, T.D., & Kakigi, R. (2002). Effects of attention, distraction and sleep on CO(2) laser evoked potentials related to C-fibers in humans. Clin Neurophysiol, 113(10), 1579-1585
63. Reidler, J.S., Mendonca, M.E., Santana, M.B., Wang, X., Lenkinski, R., Motta, A.F., Marchand, S., Latif, L., & Fregni, F. (2012). Effects of motor cortex modulation and descending inhibitory systems on pain thresholds in healthy subjects. J Pain, 13(5), 450-458
64. Riedl, V., Valet, M., Woller, A., Sorg, C., Vogel, D., Sprenger, T., Boecker, H., Wohlschlager, A.M., & Tolle, T.R. (2011). Repeated pain induces adaptations of intrinsic brain activity to reflect past and predict future pain. Neuroimage, 57(1), 206-213
65. Rocca, M.A., Valsasina, P., Absinta, M., Colombo, B., Barcella, V., Falini, A., Comi, G., & Filippi, M. (2010). Central nervous system dysregulation extends beyond the pain-matrix network in cluster headache. Cephalalgia, 30(11), 1383-1391
66. Rossi, S., Hallett, M., Rossini, P.M., & Pascual-Leone, A. (2009). Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin Neurophysiol, 120(12), 2008-2039
67. Rossini, P.M., & Rossi, S. (2007).Transcranial magnetic stimulation: Diagnostic, therapeutic, and research potential. Neurology, 68(7), 484-488
68. Ruscheweyh, R., Kuhnel, M., Filippopulos, F., Blum, B., Eggert, T., & Straube, A. (2014). Altered experimental pain perception after cerebellar infarction. Pain, 155(7), 1303-1312
69. Schmahmann, J.D. (1991). An emerging concept. The cerebellar contribution to higher function. Arch Neurol, 48(11), 1178-1187
70. Singer, T., Seymour, B., ODoherty, J., Kaube, H., Dolan, R.J., & Frith, C.D. (2004). Empathy for pain involves the affective but not sensory components of pain. Science, 303(5661), 1157-1162
71. Smith, M.J., Keel, J.C., Greenberg, B.D., Adams, L.F., Schmidt, P.J., Rubinow, D.A., & Wassermann, E.M. (1999). Menstrual cycle effects on cortical excitability. Neurology, 53(9), 2069-2072
72. Stoodley, C.J., & Schmahmann, J.D. (2009). Functional topography in the human cerebellum: A meta-Analysis of neuroimaging studies. Neuroimage, 44(2), 489-501
73. Strick, P.L., Dum, R.P., & Fiez, J.A. (2009). Cerebellum and nonmotor function. Annu Rev Neurosci, 32, 413-434
74. Strigo, I.A., Duncan, G.H., Boivin, M., & Bushnell, M.C. (2003). Differentiation of visceral and cutaneous pain in the human brain. J Neurophysiol, 89(6), 3294-3303
75. Truini, A., Galeotti, F., Romaniello, A., Virtuoso, M., Iannetti, G.D., & Cruccu, G. (2005). Laser-evoked potentials: Normative values. Clin Neurophysiol, 116(4), 821-826
76. Truini, A., Panuccio, G., Galeotti, F., Maluccio, M.R., Sartucci, F., Avoli, M., & Cruccu, G. (2010). Laser-evoked potentials as a tool for assessing the efficacy of antinociceptive drugs. Eur J Pain, 14(2), 222-225
77. Truini, A., Vergari, M., Biasiotta, A., La Cesa, S., Gabriele, M., Di Stefano, G., Cambieri, C., Cruccu, G., Inghilleri, M., & Priori, A. (2011). Transcutaneous spinal direct current stimulation inhibits nociceptive spinal pathway conduction and increases pain tolerance in humans. Eur J Pain, 15(10), 1023-1027
78. Valeriani, M., Le Pera, D., Restuccia, D., de Armas, L., Miliucci, R., Betti, V., Vigevano, F., & Tonali, P. (2007). Parallel spinal pathways generate the middle-latency N1 and the late P2 components of the laser evoked potentials. Clin Neurophysiol, 118(5), 1097-1104
79. Valeriani, M., Pazzaglia, C., Cruccu, G., & Truini, A. (2012). Clinical usefulness of laser evoked potentials. Neurophysiol Clin, 42(5), 345-353
80. Volz, M.S., Mendonca, M., Pinheiro, F.S. Cui, H., Santana M., & Fregni, F. (2012). Dissociation of motor task-induced cortical excitability and pain perception changes in healthy volunteers. PLoS One 7(3), e34273
81. Wager, T.D., Rilling, J.K., Smith, E.E., Sokolik, A., Casey, K.L., Davidson, R.J., Kosslyn, S.M., Rose, R.M., & Cohen, J.D. (2004). Placebo-induced changes in FMRI in the anticipation and experience of pain. Science, 303(5661), 1162-1167
82. Zaghi, S., Thiele, B., Pimentel, D., Pimentel, T., & Fregni, F. (2011). Assessment and treatment of pain with noninvasive cortical stimulation. Restor Neurol Neurosci, 29(6), 439-451
83. Zubieta, J.K., Bueller, J.A., Jackson, L.R., Scott, D.J., Xu, Y., Koeppe, R.A., Nichols, T.E., & Stohler, C.S. (2005). Placebo effects mediated by endogenous opioid activity on mu-opioid receptors. J Neurosci, 25(34), 7754-7762
84. Zunhammer, M., Busch, V., Griesbach, F., Landgrebe, M., Hajak G., & Langguth, B. (2011). rTMS over the cerebellum modulates temperature detection and pain thresholds through peripheral mechanisms. Brain Stimul, 4(4), 210-7 e1