Thirty years of transcranial magnetic stimulation: where do we stand?

Experimental Brain Research

Volumn 235, Issue 4, 2017, Pages 973-984

  Ziemann, Ulf ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Corticospinal excitability; Human; Motor cortex; Plasticity; Transcranial magnetic stimulation; Treatment

Indexed keywords

ANTICONVULSIVE AGENT; BACLOFEN; CARBAMAZEPINE; GABAPENTIN; LAMOTRIGINE; LOSIGAMONE; VIGABATRIN;

BRAIN; BRAIN DISEASE; BRAIN MAPPING; CEREBROVASCULAR ACCIDENT; CLINICAL RESEARCH; COGNITION; CORTICAL EXCITABILITY; EVOKED CORTICAL RESPONSE; FACILITATION; FREQUENCY MODULATION; FUNCTIONAL CONNECTIVITY; HIGH FREQUENCY OSCILLATION; HUMAN; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MOTOR CORTEX; MOTOR EVOKED POTENTIAL; MOVEMENT THERAPY; NERVE CELL PLASTICITY; NERVE STIMULATION; NEUROREHABILITATION; NON INVASIVE PROCEDURE; PRIORITY JOURNAL; PUBLICATION; PYRAMIDAL TRACT; REPETITIVE TRANSCRANIAL MAGNETIC STIMULATION; REVIEW; STROKE PATIENT; THETA BURST STIMULATION; THETA RHYTHM; TRANSCRANIAL MAGNETIC STIMULATION; BIBLIOGRAPHIC DATABASE; HISTORY; PHYSIOLOGY; STATISTICS AND NUMERICAL DATA;

BRAIN; DATABASES, BIBLIOGRAPHIC; EVOKED POTENTIALS, MOTOR; HISTORY, 20TH CENTURY; HISTORY, 21ST CENTURY; HUMANS; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 85010767241     PISSN: 00144819     EISSN: 14321106     Source Type: Journal    
DOI: 10.1007/s00221-016-4865-4     Document Type: Review

References (50)

1. Avenanti A, Coccia M, Ladavas E, Provinciali L, Ceravolo MG (2012) Low-frequency rTMS promotes use-dependent motor plasticity in chronic stroke: A randomized trial. Neurology 78:256–264
2. Barker AT, Jalinous R, Freeston IL (1985) Non-invasive magnetic stimulation of human motor cortex [letter]. Lancet 1: 1106–1107
3. Bolognini N, Ro T (2010) Transcranial magnetic stimulation: disrupting neural activity to alter and assess brain function. J Neurosci 30:9647–9650
4. Byblow WD, Stinear CM, Barber PA, Petoe MA, Ackerley SJ (2015) Proportional recovery after stroke depends on corticomotor integrity. Ann Neurol 78:848–859
5. Cantone M, Di Pino G, Capone F, Piombo M, Chiarello D, Cheeran B, Pennisi G, Di Lazzaro V (2014) The contribution of transcranial magnetic stimulation in the diagnosis and in the management of dementia. Clin Neurophysiol 125:1509–1532
6. Chen R, Classen J, Gerloff C, Celnik P, Wassermann EM, Hallett M, Cohen LG (1997) Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology 48:1398–1403
7. Cohen LG, Celnik P, Pascual-Leone A, Corwell B, Faiz L, Dambrosia J, Honda M, Sadato N, Gerloff C, Catala MD, Hallett M (1997) Functional relevance of cross-modal plasticity in the blind. Nature 389:180–183
8. Day BL, Dressler D, Maertens de Noordhout A, Marsden CD, Nakashima K, Rothwell JC, Thompson PD (1989) Electric and magnetic stimulation of human motor cortex: surface EMG and single motor unit responses. J Physiol (Lond) 412: 449–473
9. de Goede AA, Ter Braack EM, van Putten MJ (2016) Single and paired pulse transcranial magnetic stimulation in drug naive epilepsy. Clin Neurophysiol 127:3140–3155
10. Deng ZD, Lisanby SH, Peterchev AV (2014) Coil design considerations for deep transcranial magnetic stimulation. Clin Neurophysiol
11. Di Lazzaro V, Oliviero A, Profice P, Pennisi MA, Di Giovanni S, Zito G, Tonali P, Rothwell JC (2000) Muscarinic receptor blockade has differential effects on the excitability of intracortical circuits in human motor cortex. Exp Brain Res 135:455–461
12. Downar J, Geraci J, Salomons TV, Dunlop K, Wheeler S, McAndrews MP, Bakker N, Blumberger DM, Daskalakis ZJ, Kennedy SH, Flint AJ, Giacobbe P (2014) Anhedonia and reward-circuit connectivity distinguish nonresponders from responders to dorsomedial prefrontal repetitive transcranial magnetic stimulation in major depression. Biol Psychiatry 76:176–185
13. Fadiga L, Fogassi L, Pavesi G, Rizzolatti G (1995) Motor facilitation during action observation: a magnetic stimulation study. J Neurophysiol 73:2608–2611
14. George MS, Lisanby SH, Avery D, McDonald WM, Durkalski V, Pavlicova M, Anderson B, Nahas Z, Bulow P, Zarkowski P, Holtzheimer PE 3rd, Schwartz T, Sackeim HA (2010) Daily left prefrontal transcranial magnetic stimulation therapy for major depressive disorder: a sham-controlled randomized trial. Arch Gen Psychiatry 67:507–516
15. Gharabaghi A, Kraus D, Leao MT, Spuler M, Walter A, Bogdan M, Rosenstiel W, Naros G, Ziemann U (2014) Coupling brain-machine interfaces with cortical stimulation for brain-state dependent stimulation: enhancing motor cortex excitability for neurorehabilitation. Front Hum Neurosci 8: 122
16. Hess G, Donoghue JP (1996a) Long-term depression of horizontal connections in rat motor cortex. Eur J Neurosci 8:658–665
17. Hess G, Donoghue JP (1996b) Long-term potentiation and long-term depression of horizontal connections in rat motor cortex. Acta Neurobiol Exp 56:397–405
18. Huang Y-Z, Edwards MJ, Rounis E, Bhatia KP, Rothwell JC (2005) Theta Burst Stimulation of the Human Motor Cortex. Neuron 45:201–206
19. Ilic TV, Meintzschel F, Cleff U, Ruge D, Kessler KR, Ziemann U (2002) Short-interval paired-pulse inhibition and facilitation of human motor cortex: the dimension of stimulus intensity. J Physiol 545.1: 153–167
20. Kujirai T, Caramia MD, Rothwell JC, Day BL, Thompson PD, Ferbert A, Wroe S, Asselman P, Marsden CD (1993) Corticocortical inhibition in human motor cortex. J Physiol (Lond) 471: 501–519
21. Lefaucheur JP, Menard-Lefaucheur I, Goujon C, Keravel Y, Nguyen JP (2011) Predictive value of rTMS in the identification of responders to epidural motor cortex stimulation therapy for pain. J Pain 12:1102–1111
22. Lefaucheur JP, Andre-Obadia N, Antal A, Ayache SS, Baeken C, Benninger DH, Cantello RM, Cincotta M, de Carvalho M, De Ridder D, Devanne H, Di Lazzaro V, Filipovic SR, Hummel FC, Jaaskelainen SK, Kimiskidis VK, Koch G, Langguth B, Nyffeler T, Oliviero A, Padberg F, Poulet E, Rossi S, Rossini PM, Rothwell JC, Schonfeldt-Lecuona C, Siebner HR, Slotema CW, Stagg CJ, Valls-Sole J, Ziemann U, Paulus W, Garcia-Larrea L (2014) Evidence-based guidelines on the therapeutic use of repetitive transcranial magnetic stimulation (rTMS). Clin Neurophysiol 125:2150–2206
23. Levkovitz Y, Isserles M, Padberg F, Lisanby SH, Bystritsky A, Xia G, Tendler A, Daskalakis ZJ, Winston JL, Dannon P, Hafez HM, Reti IM, Morales OG, Schlaepfer TE, Hollander E, Berman JA, Husain MM, Sofer U, Stein A, Adler S, Deutsch L, Deutsch F, Roth Y, George MS, Zangen A (2015) Efficacy and safety of deep transcranial magnetic stimulation for major depression: a prospective multicenter randomized controlled trial. World. Psychiatry 14:64–73
24. 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
25. Liston C, Chen AC, Zebley BD, Drysdale AT, Gordon R, Leuchter B, Voss HU, Casey BJ, Etkin A, Dubin MJ (2014) Default mode network mechanisms of transcranial magnetic stimulation in depression. Biol Psychiatry 76:517–526
26. Lopez-Alonso V, Cheeran B, Rio-Rodriguez D, Fernandez-Del-Olmo M (2014) Inter-individual variability in response to non-invasive brain stimulation paradigms. Brain Stimul 7:372–380
27. McDonnell MN, Orekhov Y, Ziemann U (2006) The role of GABA(B) receptors in intracortical inhibition in the human motor cortex. Exp Brain Res 173:86–93
28. Menon P, Geevasinga N, Yiannikas C, Howell J, Kiernan MC, Vucic S (2015) Sensitivity and specificity of threshold tracking transcranial magnetic stimulation for diagnosis of amyotrophic lateral sclerosis: a prospective study. Lancet Neurol
29. Merton PA, Hill DK, Morton HB, Marsden CD (1982) Scope of a technique for electrical stimulation of human brain, spinal cord, and muscle. The Lancet 2:597–600
30. Merzenich MM, Kaas JH (1982) Reorganization of mammalian somatosensory cortex following peripheral nerve injury. Trends Neurosci 2:434–436
31. O’Reardon JP, Solvason HB, Janicak PG, Sampson S, Isenberg KE, Nahas Z, McDonald WM, Avery D, Fitzgerald PB, Loo C, Demitrack MA, George MS, Sackeim HA (2007) Efficacy and safety of transcranial magnetic stimulation in the acute treatment of major depression: a multisite randomized controlled trial. Biol Psychiatry 62:1208–1216
32. Pascual-Leone A, Valls-Sole J, Wassermann EM, Hallett M (1994) Responses to rapid-rate transcranial magnetic stimulation of the human motor cortex. Brain 117:847–858
33. 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
34. Pascual-Leone A, Rubio B, Pallardo F, Catala MD (1996) Rapid-rate transcranial magnetic stimulation of left dorsolateral prefrontal cortex in drug-resistant depression. The Lancet 348:233–237
35. Pons TP, Garraghty PE, Ommaya AK, Kaas JH, Taub E, Mishkin M (1991) Massive cortical reorganization after sensory deafferentation in adult macaques. Science 252:1857–1860
36. Premoli I, Castellanos N, Rivolta D, Belardinelli P, Bajo R, Zipser C, Espenhahn S, Heidegger T, Müller-Dahlhaus F, Ziemann U (2014) TMS-EEG signatures of GABAergic neurotransmission in the human cortex. J Neurosci 34:5603–5612
37. Rizzolatti G, Craighero L (2004) The mirror-neuron system. Annu Rev Neurosci 27:169–192
38. Rossi S, Hallett M, Rossini PM, Pascual-Leone A (2009) Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin Neurophysiol 120:2008–2039
39. Salomons TV, Dunlop K, Kennedy SH, Flint A, Geraci J, Giacobbe P, Downar J (2014) Resting-state cortico-thalamic-striatal connectivity predicts response to dorsomedial prefrontal rTMS in major depressive disorder. Neuropsychopharmacology 39:488–498
40. Sanger TD, Garg RR, Chen R (2001) Interactions between two different inhibitory systems in the human motor cortex. J Physiol 530.2: 307–317
41. Schneider AL, Schneider TL, Stark H (2008) Repetitive transcranial magnetic stimulation (rTMS) as an augmentation treatment for the negative symptoms of schizophrenia: a 4-week randomized placebo controlled study. Brain Stimul 1:106–111
42. Stetkarova I, Kofler M (2013) Differential effect of baclofen on cortical and spinal inhibitory circuits. Clin Neurophysiol 124:339–345
43. Suppa A, Huang YZ, Funke K, Ridding MC, Cheeran B, Di Lazzaro V, Ziemann U, Rothwell JC (2016) Ten years of theta burst stimulation in humans: established knowledge, unknowns and prospects. Brain Stimul 9:323–335
44. Wagle Shukla A, Vaillancourt DE (2014) Treatment and physiology in Parkinson’s disease and dystonia: using transcranial magnetic stimulation to uncover the mechanisms of action. Curr Neurol Neurosci Rep 14:449
45. Wang JX, Rogers LM, Gross EZ, Ryals AJ, Dokucu ME, Brandstatt KL, Hermiller MS, Voss JL (2014) Targeted enhancement of cortical-hippocampal brain networks and associative memory. Science 345:1054–1057
46. Wassermann EM (1998) Risk and safety of repetitive transcranial magnetic stimulation: Report and recommendations from the international workshop on the safety of repetitive transcranial magnetic stimulation June 5–7, 1996. Electroencephalogr Clin Neurophysiol 108: 1–16
47. Ziemann U, Lönnecker S, Steinhoff BJ, Paulus W (1996) Effects of antiepileptic drugs on motor cortex excitability in humans: a transcranial magnetic stimulation study. Ann Neurol 40:367–378
48. Ziemann U, Corwell B, Cohen LG (1998) Modulation of plasticity in human motor cortex after forearm ischemic nerve block. J Neurosci 18:1115–1123
49. Ziemann U, Paulus W, Nitsche MA, Pascual-Leone A, Byblow WD, Berardelli A, Siebner HR, Classen J, Cohen LG, Rothwell JC (2008) Consensus: Motor cortex plasticity protocols. Brain Stimul 1:164–182
50. Ziemann U, Reis J, Schwenkreis P, Rosanova M, Strafella A, Badawy R, Müller-Dahlhaus F (2015) TMS and drugs revisited 2014. Clin Neurophysiol 126:1847–1868