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

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Abstract

Transcranial magnetic stimulation (TMS) has been first described 30 years ago, and since then has gained enormous attention by neurologists, psychiatrists, neurosurgeons, clinical neurophysiologists, psychologists, and neuroscientist alike. In the early days, it was primarily used to test integrity of the corticospinal tract. Beyond further developments of TMS in diagnostics, mapping and monitoring of the motor system, major other applications expanded into using TMS as research tool in the cognitive neurosciences, and as therapeutic tool in neurological and psychiatric disease by virtue of inducing long-term change in excitability and connectivity of the stimulated brain networks. This mini-review will highlight these developments by reviewing the 10 most frequently cited TMS publications. Despite the tremendous popularity and success of TMS as a non-invasive technique to stimulate the human brain, several aims remain unresolved. This review will end with highlighting those 10 most frequently cited papers that have been published in 2014–2016 to indicate the currently hottest topics in TMS research and major avenues of development.

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References

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Barker AT, Jalinous R, Freeston IL (1985) Non-invasive magnetic stimulation of human motor cortex [letter]. Lancet 1: 1106–1107

    Article  CAS  PubMed  Google Scholar 

  • Bolognini N, Ro T (2010) Transcranial magnetic stimulation: disrupting neural activity to alter and assess brain function. J Neurosci 30:9647–9650

    Article  CAS  PubMed  Google Scholar 

  • Byblow WD, Stinear CM, Barber PA, Petoe MA, Ackerley SJ (2015) Proportional recovery after stroke depends on corticomotor integrity. Ann Neurol 78:848–859

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Deng ZD, Lisanby SH, Peterchev AV (2014) Coil design considerations for deep transcranial magnetic stimulation. Clin Neurophysiol

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Fadiga L, Fogassi L, Pavesi G, Rizzolatti G (1995) Motor facilitation during action observation: a magnetic stimulation study. J Neurophysiol 73:2608–2611

    CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

  • Hess G, Donoghue JP (1996a) Long-term depression of horizontal connections in rat motor cortex. Eur J Neurosci 8:658–665

  • 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

  • Huang Y-Z, Edwards MJ, Rounis E, Bhatia KP, Rothwell JC (2005) Theta Burst Stimulation of the Human Motor Cortex. Neuron 45:201–206

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

  • 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

    Article  CAS  Google Scholar 

  • Merzenich MM, Kaas JH (1982) Reorganization of mammalian somatosensory cortex following peripheral nerve injury. Trends Neurosci 2:434–436

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Rizzolatti G, Craighero L (2004) The mirror-neuron system. Annu Rev Neurosci 27:169–192

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Sanger TD, Garg RR, Chen R (2001) Interactions between two different inhibitory systems in the human motor cortex. J Physiol 530.2: 307–317

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Stetkarova I, Kofler M (2013) Differential effect of baclofen on cortical and spinal inhibitory circuits. Clin Neurophysiol 124:339–345

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Ziemann U, Corwell B, Cohen LG (1998) Modulation of plasticity in human motor cortex after forearm ischemic nerve block. J Neurosci 18:1115–1123

    CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

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Correspondence to Ulf Ziemann.

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This mini-review will highlight the 10 most frequently cited TMS papers (source: Web of ScienceTM, Thomson Reuters; effective date: July 30, 2016). Only original articles, letters and case reports were included in this survey. Reviews, guidelines, consensus papers, and articles on other non-invasive brain stimulation techniques such as transcranial direct current stimulation are not considered here.

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Ziemann, U. Thirty years of transcranial magnetic stimulation: where do we stand?. Exp Brain Res 235, 973–984 (2017). https://doi.org/10.1007/s00221-016-4865-4

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