J Clin Neurol.  2013 Apr;9(2):75-82. 10.3988/jcn.2013.9.2.75.

Cortico-Cortical Modulation Induced by 1-Hz Repetitive Transcranial Magnetic Stimulation of the Temporal Cortex

• Lee M
• Kim SE
• Kim WS
• Han J
• Kim HJ
• Kim BS
• Kim JY
• Hong SB
• Kim BG
• Lee HW

• KMID: 2179164
• DOI: http://doi.org/10.3988/jcn.2013.9.2.75

Abstract

BACKGROUND AND PURPOSE
Repetitive transcranial magnetic stimulation (rTMS) has potential as a noninvasive neuromodulation treatment method for various neuropsychiatric disorders, and repeated sessions of rTMS are more likely to enhance the therapeutic efficacy. This study investigated neurophysiologic and spatiodynamic changes induced by repeated 1-Hz rTMS of the temporal cortex using transcranial magnetic stimulation (TMS) indices and fluorodeoxyglucose positron emission tomography (FDG-PET).
METHODS
Twenty-seven healthy subjects underwent daily 1-Hz active or sham rTMS of the right temporal cortex for 5 consecutive days. TMS indices of motor cortical excitability were measured in both hemispheres daily before and after each rTMS session, and 2 weeks after the last stimulation. FDG-PET was performed at baseline and after the 5 days of rTMS sessions.
RESULTS
All subjects tolerated all of the sessions well, with only three of them (11.1%) reporting mild transient side effects (i.e., headache, tinnitus, or local irritation). One-Hz rTMS decreased motor evoked potential amplitudes and delayed cortical silent periods in the stimulated hemisphere. Statistical parametric mapping of FDG-PET data revealed a focal reduction of glucose metabolism in the stimulated temporal area and an increase in the bilateral precentral, ipsilateral superior and middle frontal, prefrontal and cingulate gyri.
CONCLUSIONS
Repeated rTMS sessions for 5 consecutive days were tolerated in all subjects, with only occasional minor side effects. Focal 1-Hz rTMS of the temporal cortex induces cortico-cortical modulation with widespread functional changes in brain neural networks via long-range neural connections.

Keyword

repetitive transcranial magnetic stimulation (rTMS); cortical excitability; fluorodeoxyglucose positron emission tomography (FDG-PET); cortico-cortical modulation

MeSH Terms

Brain
Evoked Potentials, Motor
Glucose
Headache
Positron-Emission Tomography
Salicylamides
Tinnitus
Transcranial Magnetic Stimulation
Glucose
Salicylamides

Figure

• 

  Fig. 1 Schematic demonstration of the experimental design. All subjects received daily 1-Hz rTMS of the right temporal cortex for 30 min (1800 pulses) over 5 consecutive days. TMS indices of cortical excitability were measured before and after daily rTMS and 2 weeks after the last rTMS session. FDG-PET images were obtained at baseline before the first session and after the last session on the fifth day of rTMS. FDG-PET: fluorodeoxyglucose positron emission tomography, rTMS: repetitive transcranial magnetic stimulation, TMS: transcranial magnetic stimulation.

• 

  Fig. 2 SPM analysis of FDG-PET data at the baseline before the first session and after the last session of rTMS. A: Glucose metabolism decreased focally at the stimulated temporal area (uncorrected p<0.0001), but no difference was observed in the primary motor cortex despite the changes in TMS indices of motor excitability. B: Glucose metabolism was markedly increased in the bilateral precentral, ipsilateral superior and middle frontal, prefrontal and cingulate gyri, which are cortical areas remote from the stimulated site (uncorrected p<0.0001). FDG-PET: fluorodeoxyglucose positron emission tomography, rTMS: repetitive transcranial magnetic stimulation, SPM: statistical parametric mapping, TMS: transcranial magnetic stimulation.

Reference

1. Merton PA, Morton HB. Stimulation of the cerebral cortex in the intact human subject. Nature. 1980. 285:227.

2. Pascual-Leone A, Rubio B, Pallardó F, Catalá MD. Rapid-rate transcranial magnetic stimulation of left dorsolateral prefrontal cortex in drug-resistant depression. Lancet. 1996. 348:233–237.

3. George MS, Nahas Z, Molloy M, Speer AM, Oliver NC, Li XB, et al. A controlled trial of daily left prefrontal cortex TMS for treating depression. Biol Psychiatry. 2000. 48:962–970.

4. Theodore WH, Hunter K, Chen R, Vega-Bermudez F, Boroojerdi B, Reeves-Tyer P, et al. Transcranial magnetic stimulation for the treatment of seizures: a controlled study. Neurology. 2002. 59:560–562.

5. Cantello R, Rossi S, Varrasi C, Ulivelli M, Civardi C, Bartalini S, et al. Slow repetitive TMS for drug-resistant epilepsy: clinical and EEG findings of a placebo-controlled trial. Epilepsia. 2007. 48:366–374.

6. Chen R, Classen J, Gerloff C, Celnik P, Wassermann EM, Hallett M, et al. Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology. 1997. 48:1398–1403.

7. Gerschlager W, Siebner HR, Rothwell JC. Decreased corticospinal excitability after subthreshold 1 Hz rTMS over lateral premotor cortex. Neurology. 2001. 57:449–455.

8. Kreuzer PM, Landgrebe M, Schecklmann M, Poeppl TB, Vielsmeier V, Hajak G, et al. Can temporal repetitive transcranial magnetic stimulation be enhanced by targeting affective components of tinnitus with frontal rTMS? A randomized controlled pilot trial. Front Syst Neurosci. 2011. 5:88.

9. Kim WS, Lee M, Han JM, Kim SE, Kim HJ, Kim BS, et al. Acute and chronic effects of repeated 1 Hz rTMS on the temporal cortex. Neuroreport. 2012. 23:540–545.

10. Siebner H, Peller M, Bartenstein P, Willoch F, Rossmeier C, Schwaiger M, et al. Activation of frontal premotor areas during suprathreshold transcranial magnetic stimulation of the left primary sensorimotor cortex: a glucose metabolic PET study. Hum Brain Mapp. 2001. 12:157–167.

11. Speer AM, Willis MW, Herscovitch P, Daube-Witherspoon M, Shelton JR, Benson BE, et al. Intensity-dependent regional cerebral blood flow during 1-Hz repetitive transcranial magnetic stimulation (rTMS) in healthy volunteers studied with H215O positron emission tomography: II. Effects of prefrontal cortex rTMS. Biol Psychiatry. 2003. 54:826–832.

12. Takano B, Drzezga A, Peller M, Sax I, Schwaiger M, Lee L, et al. Short-term modulation of regional excitability and blood flow in human motor cortex following rapid-rate transcranial magnetic stimulation. Neuroimage. 2004. 23:849–859.

13. Fox P, Ingham R, George MS, Mayberg H, Ingham J, Roby J, et al. Imaging human intra-cerebral connectivity by PET during TMS. Neuroreport. 1997. 8:2787–2791.

14. Hayashi T, Ohnishi T, Okabe S, Teramoto N, Nonaka Y, Watabe H, et al. Long-term effect of motor cortical repetitive transcranial magnetic stimulation [correction]. Ann Neurol. 2004. 56:77–85.

15. Ohn SH, Chang WH, Park CH, Kim ST, Lee JI, Pascual-Leone A, et al. Neural correlates of the antinociceptive effects of repetitive transcranial magnetic stimulation on central pain after stroke. Neurorehabil Neural Repair. 2012. 26:344–352.

16. Brasil-Neto JP, Cohen LG, Pascual-Leone A, Jabir FK, Wall RT, Hallett M. Rapid reversible modulation of human motor outputs after transient deafferentation of the forearm: a study with transcranial magnetic stimulation. Neurology. 1992. 42:1302–1306.

17. Rossini PM, Barker AT, Berardelli A, Caramia MD, Caruso G, Cracco RQ, et al. Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application. Report of an IFCN committee. Electroencephalogr Clin Neurophysiol. 1994. 91:79–92.

18. Lee HW, Seo HJ, Cohen LG, Bagic A, Theodore WH. Cortical excitability during prolonged antiepileptic drug treatment and drug withdrawal. Clin Neurophysiol. 2005. 116:1105–1112.

19. Lee M, Kim SE, Kim WS, Lee J, Yoo HK, Park KD, et al. Interaction of motor training and intermittent theta burst stimulation in modulating motor cortical plasticity: influence of BDNF Val66Met polymorphism. PLoS One. 2013. 8:e57690.

20. Kujirai T, Caramia MD, Rothwell JC, Day BL, Thompson PD, Ferbert A, et al. Corticocortical inhibition in human motor cortex. J Physiol. 1993. 471:501–519.

21. Di Lazzaro V, Oliviero A, Saturno E, Pilato F, Insola A, Mazzone P, et al. The effect on corticospinal volleys of reversing the direction of current induced in the motor cortex by transcranial magnetic stimulation. Exp Brain Res. 2001. 138:268–273.

22. Okamoto M, Dan H, Sakamoto K, Takeo K, Shimizu K, Kohno S, et al. Three-dimensional probabilistic anatomical cranio-cerebral correlation via the international 10-20 system oriented for transcranial functional brain mapping. Neuroimage. 2004. 21:99–111.

23. Esser SK, Huber R, Massimini M, Peterson MJ, Ferrarelli F, Tononi G. A direct demonstration of cortical LTP in humans: a combined TMS/EEG study. Brain Res Bull. 2006. 69:86–94.

24. Kim HJ, Lee M, Cho HJ, Park KD, Choi KG, Lee HW. Changes in neuronal activity after low frequency repetitive transcranial magnetic stimulation. J Korean Neurol Assoc. 2005. 23:627–634.

25. Rossi S, Hallett M, Rossini PM, Pascual-Leone A. Safety of TMS Consensus Group. Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin Neurophysiol. 2009. 120:2008–2039.

26. Boroojerdi B, Battaglia F, Muellbacher W, Cohen LG. Mechanisms influencing stimulus-response properties of the human corticospinal system. Clin Neurophysiol. 2001. 112:931–937.

27. Sanger TD, Garg RR, Chen R. Interactions between two different inhibitory systems in the human motor cortex. J Physiol. 2001. 530:307–317.

28. Hallett M. Transcranial magnetic stimulation: a revolution in clinical neurophysiology. J Clin Neurophysiol. 2002. 19:253–254.

29. Ziemann U, Lönnecker S, Steinhoff BJ, Paulus W. Effects of antiepileptic drugs on motor cortex excitability in humans: a transcranial magnetic stimulation study. Ann Neurol. 1996. 40:367–378.

30. Paus T, Castro-Alamancos MA, Petrides M. Cortico-cortical connectivity of the human mid-dorsolateral frontal cortex and its modulation by repetitive transcranial magnetic stimulation. Eur J Neurosci. 2001. 14:1405–1411.

31. Thut G, Pascual-Leone A. A review of combined TMS-EEG studies to characterize lasting effects of repetitive TMS and assess their usefulness in cognitive and clinical neuroscience. Brain Topogr. 2010. 22:219–232.