Skip to main content
SpringerLink
Log in

Improvement of tactile perception and enhancement of cortical excitability through intermittent theta burst rTMS over human primary somatosensory cortex

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

An Erratum to this article was published on 12 October 2007

Abstract

Adopting the patterns of theta burst stimulation (TBS) used in brain-slice preparations, a novel and rapid method of conditioning the human brain has recently been introduced. Using short bursts of high-frequency (50 Hz) repetitive transcranial magnetic stimulation (rTMS) has been shown to induce lasting changes in brain physiology of the motor cortex. In the present study, we tested whether a few minutes of intermittent theta burst stimulation (iTBS) over left primary somatosensory cortex (SI) evokes excitability changes within the stimulated brain area and whether such changes are accompanied by changes in tactile discrimination behavior. As a measure of altered perception we assessed tactile discrimination thresholds on the right and left index fingers (d2) before and after iTBS. We found an improved discrimination performance on the right d2 that was present for at least 30 min after termination of iTBS. Similar improvements were found for the ring finger, while left d2 remained unaffected in all cases. As a control, iTBS over the tibialis anterior muscle representation within primary motor cortex had no effects on tactile discrimination. Recording somatosensory evoked potentials over left SI after median nerve stimulation revealed a reduction in paired-pulse inhibition after iTBS that was associated but not correlated with improved discrimination performance. No excitability changes could be found for SI contralateral to iTBS. Testing the performance of simple motor tasks revealed no alterations after iTBS was applied over left SI. Our results demonstrate that iTBS protocols resembling those used in slice preparations for the induction of long-term potentiation are also effective in driving lasting improvements of the perception of touch in human subjects together with an enhancement of cortical excitability.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Allison T, McCarthy G, Wood CC, Jones SJ (1991) Potentials evoked in human and monkey cerebral cortex by stimulation of the median nerve. A review of scalp and intracranial recordings. Brain 114(Pt 6):2465–2503

    Article  PubMed  Google Scholar 

  • Andres FG, Mima T, Schulman AE, Dichgans J, Hallett M, Gerloff C (1999) Functional coupling of human cortical sensorimotor areas during bimanual skill acquisition. Brain 122(Pt 5):855–870

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Bliss TV, Lomo T (1973) Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol 232:331–356

    PubMed  CAS  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

    PubMed  CAS  Google Scholar 

  • Di Lazzaro V, Oliviero A, Mazzone P, Pilato F, Saturno E, Dileone M, Insola A, Tonali PA, Rothwell JC (2002) Short-term reduction of intracortical inhibition in the human motor cortex induced by repetitive transcranial magnetic stimulation. Exp Brain Res 147:108–113

    Article  PubMed  CAS  Google Scholar 

  • Dinse HR, Ragert P, Pleger B, Schwenkreis P, Tegenthoff M (2003) Pharmacological modulation of perceptual learning and associated cortical reorganization. Science 301:91–94

    Article  PubMed  CAS  Google Scholar 

  • Dinse HR, Kleibel N, Kalisch T, Ragert P, Tegenthoff M (2006) Tactile coactivation resets age-related decline of human tactile discrimination. Ann Neurol 60:88–94

    Article  PubMed  Google Scholar 

  • Evers S, Bockermann I, Nyhuis PW (2001) The impact of transcranial magnetic stimulation on cognitive processing: an event-related potential study. Neuroreport 12:2915–2918

    Article  PubMed  CAS  Google Scholar 

  • Fitzgerald PB, Fountain S, Daskalakis ZJ (2006) A comprehensive review of the effects of rTMS on motor cortical excitability and inhibition. Clin Neurophysiol 117:2584–2596

    Article  PubMed  Google Scholar 

  • Frasson E, Priori A, Bertolasi L, Mauguiere F, Fiaschi A, Tinazzi M (2001) Somatosensory disinhibition in dystonia. Mov Disord 16:674–682

    Article  PubMed  CAS  Google Scholar 

  • Godde B, Stauffenberg B, Spengler F, Dinse HR (2000) Tactile coactivation-induced changes in spatial discrimination performance. J Neurosci 20:1597–1604

    PubMed  CAS  Google Scholar 

  • Hanajima R, Ugawa Y, Machii K, Mochizuki H, Terao Y, Enomoto H, Furubayashi T, Shiio Y, Uesugi H, Kanazawa I (2001) Interhemispheric facilitation of the hand motor area in humans. J Physiol 531:849–859

    Article  PubMed  CAS  Google Scholar 

  • Huang YZ, Rothwell JC (2004) The effect of short-duration bursts of high-frequency, low-intensity transcranial magnetic stimulation on the human motor cortex. Clin Neurophysiol 115:1069–1075

    Article  PubMed  Google Scholar 

  • Huang YZ, Edwards MJ, Rounis E, Bhatia KP, Rothwell JC (2005) Theta burst stimulation of the human motor cortex. Neuron 45:201–206

    Article  PubMed  CAS  Google Scholar 

  • Huang YZ, Chen RS, Rothwell JC, Wen HY (2007) The after-effect of human theta burst stimulation is NMDA receptor dependent. Clin Neurophysiol 118:1028–1032

    Article  PubMed  CAS  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 545:153–167

    Article  PubMed  CAS  Google Scholar 

  • Klimesch W, Sauseng P, Gerloff C (2003) Enhancing cognitive performance with repetitive transcranial magnetic stimulation at human individual alpha frequency. Eur J Neurosci 17:1129–1133

    Article  PubMed  Google Scholar 

  • Knecht S, Ellger T, Breitenstein C, Bernd Ringelstein E, Henningsen H (2003) Changing cortical excitability with low-frequency transcranial magnetic stimulation can induce sustained disruption of tactile perception. Biol Psychiatry 53:175–179

    Article  PubMed  Google Scholar 

  • Kobayashi M, Hutchinson S, Theoret H, Schlaug G, Pascual-Leone A (2004) Repetitive TMS of the motor cortex improves ipsilateral sequential simple finger movements. Neurology 62:91–98

    PubMed  CAS  Google Scholar 

  • Mochizuki H, Hanajima R, Kowa H, Motoyoshi Y, Ashida H, Kamakura K, Motoyoshi K, Ugawa Y (2001) Somatosensory evoked potential recovery in myotonic dystrophy. Clin Neurophysiol 112:793–799

    Article  PubMed  CAS  Google Scholar 

  • Muellbacher W, Ziemann U, Boroojerdi B, Hallett M (2000) Effects of low-frequency transcranial magnetic stimulation on motor excitability and basic motor behavior. Clin Neurophysiol 111:1002–1007

    Article  PubMed  CAS  Google Scholar 

  • Munchau A, Bloem BR, Irlbacher K, Trimble MR, Rothwell JC (2002) Functional connectivity of human premotor and motor cortex explored with repetitive transcranial magnetic stimulation. J Neurosci 22:554–561

    PubMed  CAS  Google Scholar 

  • Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113

    Article  PubMed  CAS  Google Scholar 

  • Peinemann A, Lehner C, Mentschel C, Munchau A, Conrad B, Siebner HR (2000) Subthreshold 5-Hz repetitive transcranial magnetic stimulation of the human primary motor cortex reduces intracortical paired-pulse inhibition. Neurosci Lett 296:21–24

    Article  PubMed  CAS  Google Scholar 

  • Pleger B, Foerster AF, Ragert P, Dinse HR, Schwenkreis P, Malin JP, Nicolas V, Tegenthoff M (2003a) Functional imaging of perceptual learning in human primary and secondary somatosensory cortex. Neuron 40:643–653

    Article  PubMed  CAS  Google Scholar 

  • Pleger B, Schwenkreis P, Dinse HR, Ragert P, Hoffken O, Malin JP, Tegenthoff M (2003b) Pharmacological suppression of plastic changes in human primary somatosensory cortex after motor learning. Exp Brain Res 148:525–532

    PubMed  Google Scholar 

  • Pleger B, Blankenburg F, Bestmann S, Ruff CC, Wiech K, Stephan KE, Friston KJ, Dolan RJ (2006) Repetitive transcranial magnetic stimulation-induced changes in sensorimotor coupling parallel improvements of somatosensation in humans. J Neurosci 15:1945–1952

    Article  Google Scholar 

  • Ragert P, Dinse HR, Pleger B, Wilimzig C, Frombach E, Schwenkreis P, Tegenthoff M (2003) Combination of 5 Hz repetitive transcranial magnetic stimulation (rTMS) and tactile coactivation boosts tactile discrimination in humans. Neurosci Lett 348:105–108

    Article  PubMed  CAS  Google Scholar 

  • Ragert P, Becker M, Tegenthoff M, Pleger B, Dinse HR (2004) Sustained increase of somatosensory cortex excitability by 5 Hz repetitive transcranial magnetic stimulation studied by paired median nerve stimulation in humans. Neurosci Lett 356:91–94

    Article  PubMed  CAS  Google Scholar 

  • Romero JR, Anschel D, Sparing R, Gangitano M, Pascual-Leone A (2002) Subthreshold low frequency repetitive transcranial magnetic stimulation selectively decreases facilitation in the motor cortex. Clin Neurophysiol 113:101–107

    Article  PubMed  Google Scholar 

  • Ruff RM, Parker SB (1993) Gender- and age-specific changes in motor speed and eye–hand coordination in adults: normative values for the Finger Tapping and Grooved Pegboard Tests. Percept Mot Skills 76:1219–1230

    PubMed  CAS  Google Scholar 

  • Samuel M, Williams SC, Leigh PN, Simmons A, Chakraborti S, Andrew CM, Friston KJ, Goldstein LH, Brooks DJ (1998) Exploring the temporal nature of hemodynamic responses of cortical motor areas using functional MRI. Neurology 51:1567–1575

    PubMed  CAS  Google Scholar 

  • Satow T, Mima T, Yamamoto J, Oga T, Begum T, Aso T, Hashimoto N, Rothwell JC, Shibasaki H (2003) Short-lasting impairment of tactile perception by 0.9Hz-rTMS of the sensorimotor cortex. Neurology 25:1045–1047

    Google Scholar 

  • Schambra HM, Sawaki L, Cohen LG (2003) Modulation of excitability of human motor cortex (M1) by 1 Hz transcranial magnetic stimulation of the contralateral M1. Clin Neurophysiol 114:130–133

    Article  PubMed  CAS  Google Scholar 

  • Schiene K, Bruehl C, Zilles K, Qu M, Hagemann G, Kraemer M, Witte OW (1996) Neuronal hyperexcitability, reduction of GABAA-receptor expression in the surround of cerebral photothrombosis. J Cereb Blood Flow Metab 16(5):906–914

    Article  PubMed  CAS  Google Scholar 

  • Schwenkreis P, Pleger B, Hoffken O, Malin JP, Tegenthoff M (2001) Repetitive training of a synchronised movement induces short-term plastic changes in the human primary somatosensory cortex. Neurosci Lett 312:99–102

    Article  PubMed  CAS  Google Scholar 

  • Seyal M, Siddiqui I, Hundal NS (1997) Suppression of spatial localization of a cutaneous stimulus following transcranial magnetic pulse stimulation of the sensorimotor cortex. Electroencephalogr Clin Neurophysiol 105:24–28

    Article  PubMed  CAS  Google Scholar 

  • Siebner HR, Peller M, Willoch F, Minoshima S, Boecker H, Auer C, Drzezga A, Conrad B, Bartenstein P (2000) Lasting cortical activation after repetitive TMS of the motor cortex: a glucose metabolic study. Neurology 54:956–963

    PubMed  CAS  Google Scholar 

  • Siebner HR, Rothwell J (2003) Transcranial magnetic stimulation: new insights into representational cortical plasticity. Exp Brain Res 148:1–16

    Article  PubMed  Google Scholar 

  • Stanton PK, Sejnowski TJ (1989) Associative long-term depression in the hippocampus induced by Hebbian covariance. Nature 339:215–218

    Article  PubMed  CAS  Google Scholar 

  • Tegenthoff M, Ragert P, Pleger B, Schwenkreis P, Forster AF, Nicolas V, Dinse HR (2005) Improvement of tactile discrimination performance and enlargement of cortical somatosensory maps after 5 Hz rTMS. PLoS Biol 3:e362

    Article  PubMed  Google Scholar 

  • Wassermann EM, Wedegaertner FR, Ziemann U, George MS, Chen R (1998) Crossed reduction of human motor cortex excitability by 1-Hz transcranial magnetic stimulation. Neurosci Lett 250:141–144

    Article  PubMed  CAS  Google Scholar 

  • Wolters A, Schmidt A, Schramm A, Zeller D, Naumann M, Kunesch E, Benecke R, Reiners K, Classen J (2005) Timing-dependent plasticity in human primary somatosensory cortex. J Physiol 565:1039–1052

    Article  PubMed  CAS  Google Scholar 

  • Wu T, Sommer M, Tergau F, Paulus W (2000) Lasting influence of repetitive transcranial magnetic stimulation on intracortical excitability in human subjects. Neurosci Lett 287:37–40

    Article  PubMed  CAS  Google Scholar 

  • Ziemann U, Lonnecker S, Steinhoff BJ, Paulus W (1996) The effect of lorazepam on the motor cortical excitability in man. Exp Brain Res 109:127–135

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by the Deutsche Forschungsgemeinschaft DFG (Ra 1391/1-1).

Author information

Author notes

  1. Patrick Ragert

    Present address: Human Cortical Physiology Section, National Institute of Neurological Disorders and Stroke, National Institute of Health, Bethesda, MD, USA

Authors and Affiliations

  1. Institute for Neuroinformatics, Theoretical Biology, Ruhr-University, 44780, Bochum, Germany

    Patrick Ragert, Stephanie Franzkowiak & Hubert R. Dinse

  2. Department of Neurology, BG-Kliniken Bergmannsheil, Ruhr-University, 44789, Bochum, Germany

    Patrick Ragert, Peter Schwenkreis & Martin Tegenthoff

Authors
  1. Patrick Ragert
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Stephanie Franzkowiak
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Peter Schwenkreis
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Martin Tegenthoff
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hubert R. Dinse
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Martin Tegenthoff.

Additional information

An erratum to this article can be found at http://dx.doi.org/10.1007/s00221-007-1122-x

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ragert, P., Franzkowiak, S., Schwenkreis, P. et al. Improvement of tactile perception and enhancement of cortical excitability through intermittent theta burst rTMS over human primary somatosensory cortex. Exp Brain Res 184, 1–11 (2008). https://doi.org/10.1007/s00221-007-1073-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-007-1073-2

Keywords

Search

Navigation