The effect of long-term TENS on persistent neuroplastic changes in the human cerebral cortex

Human Brain Mapping

Volumn 32, Issue 6, 2011, Pages 872-882

  Meesen, Raf L J ^a,b,c   Cuypers, Koen ^a,c   Rothwell, John C ^d   Swinnen, Stephan P ^b   Levin, Oron ^b  

^a University College Limburg   (Belgium)

^b UNIVERSITY OF LEUVEN   (Belgium)

^c HASSELT UNIVERSITY   (Belgium)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Corticomotor representations; Neuroplasticity; Somatosensory stimulation; Transcranial magnetic stimulation (TMS)

Indexed keywords

ADULT; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; FEMALE; FOREARM; HUMAN; HUMAN EXPERIMENT; LONG TERM CARE; MALE; MOTOR CORTEX; MUSCLE EXAMINATION; NERVE STIMULATION; NORMAL HUMAN; PRIORITY JOURNAL; PYRAMIDAL TRACT; SOMATOSENSORY STIMULATION; TOPOGRAPHY; TRANSCRANIAL MAGNETIC STIMULATION; TRANSCUTANEOUS ELECTRICAL NERVE STIMULATION;

ADOLESCENT; ADULT; CEREBRAL CORTEX; ELECTROMYOGRAPHY; EVOKED POTENTIALS, MOTOR; FEMALE; FOREARM; HAND; HUMANS; MALE; MIDDLE AGED; NEURONAL PLASTICITY; TIME; TRANSCUTANEOUS ELECTRIC NERVE STIMULATION; YOUNG ADULT;

EID: 79955704905     PISSN: 10659471     EISSN: 10970193     Source Type: Journal    
DOI: 10.1002/hbm.21075     Document Type: Article

References (69)

1. Armutlu K, Meric A, Kirdi N, Yakut E, Karabudak R (2003): The effect of transcutaneous electrical nerve stimulation on spasticity in multiple sclerosis patients: A pilot study. Neurorehabil Neural Repair 17: 79-82.
2. Bending J, Cleeves L (1990): Effect of electrical nerve stimulation on dystonic tremor. Lancet 336: 1385-1386.
3. Carel C, Loubinoux I, Boulanouar K, Manelfe C, Rascol O, Celsis P, Chollet F (2000): Neural substrate for the effects of passive training on sensorimotor cortical representation: A study with functional magnetic resonance imaging in healthy subjects. J Cereb Blood Flow Metab 20: 478-484.
4. Caria MA, Kaneko T, Kimura A, Asanuma H (1997): Functional organization of the projection from area 2 to area 4gamma in the cat. J Neurophysiol 77: 3107-3114.
5. Classen J, Liepert J, Wise SP, Hallett M, Cohen LG (1998): Rapid plasticity of human cortical movement representation induced by practice. J Neurophysiol 79: 1117-1123.
6. Cohen LG, Bandinelli S, Findley TW, Hallett M (1991): Motor reorganization after upper limb amputation in man. A study with focal magnetic stimulation. Brain 114 (Part 1B): 615-627.
7. Conforto AB, Ferreiro KN, Tomasi C, dos Santos RL, Moreira VL, Marie SK, Baltieri SC, Scaff M, Cohen LG (2010): Effects of somatosensory stimulation on motor function after subacute stroke. Neurorehabil Neural Repair 24: 263-272.
8. Cuypers K, Levin O, Thijs H, Swinnen SP, Meesen RLJ: Long-term TENS treatment improves tactile sensitivity in MS patients. Neurorehabil Neural Repair (in press).
9. Deletis V, Schild JH, Beric A, Dimitrijevic MR (1992): Facilitation of motor evoked potentials by somatosensory afferent stimulation. Electroencephalogr Clin Neurophysiol 85: 302-310.
10. Duclos C, Roll R, Kavounoudias A, Roll JP (2007): Cerebral correlates of the "Kohnstamm phenomenon": An fMRI study. Neuroimage 34: 774-783.
11. Fernandez-del-Olmo M, varez-Sauco M, Koch G, Franca M, Marquez G, Sanchez JA, Acero RM, Rothwell JC (2008): How repeatable are the physiological effects of TENS? Clin Neurophysiol 119: 1834-1839.
12. Foley-Nolan D, Kinirons M, Coughlan RJ, O'Connor P (1990): Post whiplash dystonia well controlled by transcutaneous electrical nervous stimulation (TENS): Case report. J Trauma 30: 909-910.
13. Forner-Cordero A, Steyvers M, Levin O, Alaerts K, Swinnen SP (2008): Changes in corticomotor excitability following prolonged muscle tendon vibration. Behav Brain Res 190: 41-49.
14. Fraser C, Power M, Hamdy S, Rothwell J, Hobday D, Hollander I, Tyrell P, Hobson A, Williams S, Thompson D (2002): Driving plasticity in human adult motor cortex is associated with improved motor function after brain injury. Neuron 34: 831-840.
15. Fuhr P, Cohen LG, Dang N, Findley TW, Haghighi S, Oro J, Hallett M (1992): Physiological analysis of motor reorganization following lower limb amputation. Electroencephalogr Clin Neurophysiol 85: 53-60.
16. Fung J, Barbeau H (1994): Effects of conditioning cutaneomuscular stimulation on the soleus H-reflex in normal and spastic paretic subjects during walking and standing. J Neurophysiol 72: 2090-2104.
17. Ghosh S, Porter R (1988): Corticocortical synaptic influences on morphologically identified pyramidal neurones in the motor cortex of the monkey. J Physiol 400: 617-629.
18. Goulet C, Arsenault AB, Bourbonnais D, Laramee MT, Lepage Y (1996): Effects of transcutaneous electrical nerve stimulation on H-reflex and spinal spasticity. Scand J Rehabil Med 28: 169-176.
19. Hamdy S, Rothwell JC, Aziz Q, Singh KD, Thompson DG (1998): Long-term reorganization of human motor cortex driven by short-term sensory stimulation. Nat Neurosci 1: 64-68.
20. Harms KJ, Rioult-Pedotti MS, Carter DR, Dunaevsky A (2008): Transient spine expansion and learning-induced plasticity in layer 1 primary motor cortex. J Neurosci 28: 5686-5690.
21. Huerta MF, Pons TP (1990): Primary motor cortex receives input from area 3a in macaques. Brain Res 537: 367-371.
22. Kimura I, Ayyar DR, Lippmann SM (1983): Electrophysiological verification of the ulnar to median nerve communications in the hand and forearm. Tohoku J Exp Med 141: 269-274.
23. Krause T, Kurth R, Ruben J, Schwiemann J, Villringer K, Deuchert M, Moosmann M, Brandt S, Wolf K, Curio G, Villringer A (2001): Representational overlap of adjacent fingers in multiple areas of human primary somatosensory cortex depends on electrical stimulus intensity: An fMRI study. Brain Res 899: 36-46.
24. Kurth R, Villringer K, Curio G, Wolf KJ, Krause T, Repenthin J, Schwiemann J, Deuchert M, Villringer A (2000): fMRI shows multiple somatotopic digit representations in human primary somatosensory cortex. Neuroreport 11: 1487-1491.
25. Levin MF, Hui-Chan CW (1992): Relief of hemiparetic spasticity by TENS is associated with improvement in reflex and voluntary motor functions. Electroencephalogr Clin Neurophysiol 85: 131-142.
26. Lewis GN, Byblow WD (2004): The effects of repetitive proprioceptive stimulation on corticomotor representation in intact and hemiplegic individuals. Clin Neurophysiol 115: 765-773.
27. Liepert J, Bauder H, Wolfgang HR, Miltner WH, Taub E, Weiller C (2000): Treatment-induced cortical reorganization after stroke in humans. Stroke 31: 1210-1216.
28. Lucier GE, Ruegg DC, Wiesendanger M (1975): Responses of neurones in motor cortex and in area 3A to controlled stretches of forelimb muscles in cebus monkeys. J Physiol 251: 833-853.
29. Mace MJ, Levin O, Alaerts K, Rothwell JC, Swinnen SP (2008): Corticospinal facilitation following prolonged proprioceptive stimulation by means of passive wrist movement. J Clin Neurophysiol 25: 202-209.
30. Matteis M, Vernieri F, Troisi E, Pasqualetti P, Tibuzzi F, Caltagirone C, Silvestrini M (2003): Early cerebral hemodynamic changes during passive movements and motor recovery after stroke. J Neurol 250: 810-817.
31. Miller L, Mattison P, Paul L, Wood L (2007): The effects of transcutaneous electrical nerve stimulation (TENS) on spasticity in multiple sclerosis. Mult Scler 13: 527-533.
32. Murphy JT, Wong YC, Kwan HC (1975): Afferent-efferent linkages in motor cortex for single forelimb muscles. J Neurophysiol 38: 990-1014.
33. Naito E, Ehrsson HH, Geyer S, Zilles K, Roland PE (1999): Illusory arm movements activate cortical motor areas: A positron emission tomography study. J Neurosci 19: 6134-6144.
34. Nelles G, Spiekramann G, Jueptner M, Leonhardt G, Muller S, Gerhard H, Diener HC (1999): Evolution of functional reorganization in hemiplegic stroke: A serial positron emission tomographic activation study. Ann Neurol 46: 901-909.
35. Nelles G, Jentzen W, Jueptner M, Muller S, Diener HC (2001): Arm training induced brain plasticity in stroke studied with serial positron emission tomography. Neuroimage 13: 1146-1154.
36. Ng SS, Hui-Chan CW (2007): Transcutaneous electrical nerve stimulation combined with task-related training improves lower limb functions in subjects with chronic stroke. Stroke 38: 2953-2959.
37. Nudo RJ, Wise BM, SiFuentes F, Milliken GW (1996): Neural substrates for the effects of rehabilitative training on motor recovery after ischemic infarct. Science 272: 1791-1794.
38. Oldfield RC (1971): The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia 9: 97-113.
39. Pascual-Leone A, Cammarota A, Wassermann EM, Brasil-Neto JP, Cohen LG, Hallett M (1993): Modulation of motor cortical outputs to the reading hand of braille readers. Ann Neurol 34: 33-37.
40. Pascual-Leone A, Grafman J, Hallett M (1994): Modulation of cortical motor output maps during development of implicit and explicit knowledge. Science 263: 1287-1289.
41. Pascual-Leone A, Nguyet D, Cohen LG, Brasil-Neto JP, Cammarota A, Hallett M (1995): Modulation of muscle responses evoked by transcranial magnetic stimulation during the acquisition of new fine motor skills. J Neurophysiol 74: 1037-1045.
42. Quartarone A, Bagnato S, Rizzo V, Siebner HR, Dattola V, Scalfari A, Morgante F, Battaglia F, Romano M, Girlanda P (2003): Abnormal associative plasticity of the human motor cortex in writer's cramp. Brain 126: 2586-2596.
43. Quartarone A, Rizzo V, Bagnato S, Morgante F, Sant'Angelo A, Girlanda P, Siebner HR (2006): Rapid-rate paired associative stimulation of the median nerve and motor cortex can produce long-lasting changes in motor cortical excitability in humans. J Physiol 575: 657-670.
44. Radovanovic S, Korotkov A, Ljubisavljevic M, Lyskov E, Thunberg J, Kataeva G, Danko S, Roudas M, Pakhomov S, Medvedev S, Johansson H (2002): Comparison of brain activity during different types of proprioceptive inputs: A positron emission tomography study. Exp Brain Res 143: 276-285.
45. Ridding MC, Rothwell JC (1997): Stimulus/response curves as a method of measuring motor cortical excitability in man. Electroencephalogr Clin Neurophysiol 105: 340-344.
46. Ridding MC, McKay DR, Thompson PD, Miles TS (2001): Changes in corticomotor representations induced by prolonged peripheral nerve stimulation in humans. Clin Neurophysiol 112: 1461-1469.
47. Rioult-Pedotti MS, Donoghue JP, Dunaevsky A (2007): Plasticity of the synaptic modification range. J Neurophysiol 98: 3688-3695.
48. Rosenkranz K, Rothwell JC (2003): Differential effect of muscle vibration on intracortical inhibitory circuits in humans. J Physiol 551: 649-660.
49. Rosenkranz K, Rothwell JC (2006): Differences between the effects of three plasticity inducing protocols on the organization of the human motor cortex. Eur J Neurosci 23: 822-829.
50. Rosenkranz K, Kacar A, Rothwell JC (2007): Differential modulation of motor cortical plasticity and excitability in early and late phases of human motor learning. J Neurosci 27: 12058-12066.
51. Rosenkranz K, Butler K, Williamon A, Cordivari C, Lees AJ, Rothwell JC (2008): Sensorimotor reorganization by proprioceptive training in musician's dystonia and writer's cramp. Neurology 70: 304-315.
52. Roth BJ, Saypol JM, Hallett M, Cohen LG (1991): A theoretical calculation of the electric field induced in the cortex during magnetic stimulation. Electroencephalogr Clin Neurophysiol 81: 47-56.
53. Sato K, Nariai T, Tanaka Y, Maehara T, Miyakawa N, Sasaki S, Momose-Sato Y, Ohno K (2005): Functional representation of the finger and face in the human somatosensory cortex: intraoperative intrinsic optical imaging. Neuroimage 25: 1292-1301.
54. Siebner HR, Rothwell J (2003): Transcranial magnetic stimulation: new insights into representational cortical plasticity. Exp Brain Res 148: 1-16.
55. Skeil D, Thorpe AC (2001): Transcutaneous electrical nerve stimulation in the treatment of neurological patients with urinary symptoms. BJU Int 88: 899-908.
56. Sonde L, Gip C, Fernaeus SE, Nilsson CG, Viitanen M (1998): Stimulation with low frequency (1.7 Hz) transcutaneous electric nerve stimulation (low-tens) increases motor function of the post-stroke paretic arm. Scand J Rehabil Med 30: 95-99.
57. Steyvers M, Levin O, Van Baelen M, Swinnen SP (2003a): Corticospinal excitability changes following prolonged muscle tendon vibration. Neuroreport 14: 1901-1905.
58. Steyvers M, Levin O, Verschueren SM, Swinnen SP (2003b): Frequency-dependent effects of muscle tendon vibration on corticospinal excitability: A TMS study. Exp Brain Res 151: 9-14.
59. Thickbroom GW, Sammut R, Mastaglia FL (1998): Magnetic stimulation mapping of motor cortex: Factors contributing to map area. Electroencephalogr Clin Neurophysiol 109: 79-84.
60. Thickbroom GW, Byrnes ML, Mastaglia FL (1999): Methodology and application of TMS mapping. Electroencephalogr Clin Neurophysiol Suppl 51: 48-54.
61. Tinazzi M, Zarattini S, Valeriani M, Romito S, Farina S, Moretto G, Smania N, Fiaschi A, Abbruzzese G (2005): Long-lasting modulation of human motor cortex following prolonged transcutaneous electrical nerve stimulation (TENS) of forearm muscles: Evidence of reciprocal inhibition and facilitation. Exp Brain Res 161: 457-464.
62. Tinazzi M, Zarattini S, Valeriani M, Stanzani C, Moretto G, Smania N, Fiaschi A, Abbruzzese G (2006): Effects of transcutaneous electrical nerve stimulation on motor cortex excitability in writer's cramp: Neurophysiological and clinical correlations. Mov Disord 21: 1908-1913.
63. Toglia JU, Izzo K (1985): Treatment of myoclonic dystonia with transcutaneous electrical nerve stimulation. Ital J Neurol Sci 6: 75-78.
64. Wassermann EM (1998): Risk and safety of repetitive transcranial magnetic stimulation: Report and suggested guidelines from the international workshop on the safety of repetitive transcranial magnetic stimulation, June 5-7, 1996. Electroencephalogr Clin Neurophysiol 108: 1-16.
65. Wassermann EM, McShane LM, Hallett M, Cohen LG (1992): Noninvasive mapping of muscle representations in human motor cortex. Electroencephalogr Clin Neurophysiol 85: 1-8.
66. Wilson SA, Thickbroom GW, Mastaglia FL (1993): Transcranial magnetic stimulation mapping of the motor cortex in normal subjects. The representation of two intrinsic hand muscles. J Neurol Sci 118: 134-144.
67. Wilson SA, Day BL, Thickbroom GW, Mastaglia FL (1996): Spatial differences in the sites of direct and indirect activation of corticospinal neurones by magnetic stimulation. Electroencephalogr Clin Neurophysiol 101: 255-261.
68. Zarzecki P, Shinoda Y, Asanuma H (1978): Projection from area 3a to the motor cortex by neurons activated from group I muscle afferents. Exp Brain Res 33: 269-282.
69. Ziemann U, Rothwell JC, Ridding MC (1996): Interaction between intracortical inhibition and facilitation in human motor cortex. J Physiol 496 (Part 3): 873-881.