Ongoing cumulative effects of single TMS pulses on corticospinal excitability: An intra- and inter-block investigation

Clinical Neurophysiology

Volumn 127, Issue 1, 2016, Pages 621-628

  Pellicciari, Maria Concetta ^a   Miniussi, Carlo ^a,b   Ferrari, Clarissa ^a   Koch, Giacomo ^c,d   Bortoletto, Marta ^a  

^a IRCCS ISTITUTO CENTRO SAN GIOVANNI DI DIO FATEBENEFRATELLI   (Italy)

^b UNIVERSITY OF BRESCIA   (Italy)

^c IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^d TOR VERGATA UNIVERSITY HOSPITAL   (Italy)

Author keywords

Corticospinal excitability; Motor evoked potentials (MEP); Random and fixed inter trial interval; Single pulse; Transcranial magnetic stimulation (TMS)

Indexed keywords

ADULT; ANALYSIS OF VARIANCE; ARTICLE; CONTROLLED STUDY; EXCITABILITY; FEMALE; HUMAN; HUMAN EXPERIMENT; MALE; MOTOR ACTIVITY; MOTOR CORTEX; MOTOR EVOKED POTENTIAL; NORMAL HUMAN; PRIORITY JOURNAL; PYRAMIDAL TRACT; TRANSCRANIAL MAGNETIC STIMULATION; ELECTROMYOGRAPHY; PHYSIOLOGY; PROCEDURES; TRENDS; YOUNG ADULT;

ADULT; ELECTROMYOGRAPHY; EVOKED POTENTIALS, MOTOR; FEMALE; HUMANS; MALE; MOTOR CORTEX; PYRAMIDAL TRACTS; TRANSCRANIAL MAGNETIC STIMULATION; YOUNG ADULT;

EID: 84925832567     PISSN: 13882457     EISSN: 18728952     Source Type: Journal    
DOI: 10.1016/j.clinph.2015.03.002     Document Type: Article

References (57)

1. Allen E.A., Pasley B.N., Duong T., Freeman R.D. Transcranial magnetic stimulation elicits coupled neural and hemodynamic consequences. Science 2007, 317:1918-1921.
2. Arai N., Okabe S., Furubayashi T., Terao Y., Yuasa K., Ugawa Y. Comparison between short train, monophasic and biphasic repetitive transcranial magnetic stimulation (rTMS) of the human motor cortex. Clin Neurophysiol 2005, 116:605-613.
3. Bailey N.W., Thomson R.H., Hoy K.E., Hernandez-Pavon J.C., Fitzgerald P.B., Ugawa Y. Commentary regarding: TDCS increases cortical excitability: direct evidence from TMS-EEG. Cortex 2014 Nov 15, S0010-9452(14)00352-9.
4. Bastani A., Jaberzadeh S. A higher number of TMS-elicited MEP from a combined hotspot improves intra- and inter-session reliability of the upper limb muscles in healthy individuals. PLoS One 2012, 7:e47582.
5. Bestmann S. The physiological basis of transcranial magnetic stimulation. Trends Cogn Sci 2008, 12:81-83.
6. Bohning D.E., Shastri A., McConnell K.A., Nahas Z., Lorberbaum J.P., Roberts D.R., et al. A combined TMS/fMRI study of intensity-dependent TMS over motor cortex. Biol Psychiatry 1999, 45:385-394.
7. Bohning D.E., Shastri A., Wassermann E.M., Ziemann U., Lorberbaum J.P., Nahas Z., Lomarev M.P., George M.S. BOLD-f MRI response to single-pulse transcranial magnetic stimulation (TMS). J Magn Reson Imaging 2000, 11:569-574.
8. Carducci F., Brusco R. Accuracy of an individualized MR-based head model for navigated brain stimulation. Psychiatry Res 2012, 203:105-108.
9. Carroll T.J., Selvanayagam V.S., Riek S., Semmler J.G. Neural adaptations to strength training: moving beyond transcranial magnetic stimulation and reflex studies. Acta Physiol (Oxford) 2011, 202:119-140.
10. Chaieb L., Antal A., Paulus W. Transcranial alternating current stimulation in the low kHz range increases motor cortex excitability. Restor Neurol Neurosci 2011, 29:167-175.
11. Chen R., Classen J., Gerloff C., Celnik P., Wassermann E.M., Hallett M., Cohen L.G. Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology 1997, 48:1398-1403.
12. Chen A.C., Oathes D.J., Chang C., Bradley T., Zhou Z.W., Williams L.M., et al. Causal interactions between fronto-parietal central executive and default-mode networks in humans. Proc Natl Acad Sci U S A 2013, 110:19944-19949.
13. Christie A., Fling B., Crews R.T., Mulwitz L.A., Kamen G. Reliability of motor-evoked potentials in the ADM muscle of older adults. J Neurosci Methods 2007, 164:320-324.
14. Cincotta M., Giovannelli F., Borgheresi A., Balestrieri F., Toscani L., Zaccara G., et al. Optically tracked neuronavigation increases the stability of hand-held focal coil positioning: evidence from "transcranial" magnetic stimulation-induced electrical field measurements. Brain Stimul 2010, 3:119-123.
15. Cuypers K., Thijs H., Meesen R.L. Optimization of the transcranial magnetic stimulation protocol by defining a reliable estimate for corticospinal excitability. PLoS One 2014, 9:e86380.
16. Daskalakis Z., Moller B., Christensen B.K., et al. The effects of repetitive transcranial magnetic stimulation on cortical inhibition in healthy human subjects. Exp Brain Res 2006, 174:403-412.
17. Delvendahl I., Gattinger N., Berger T., Gleich B., Siebner H.R., Mall V. The role of pulse shape in motor cortex transcranial magnetic stimulation using full-sine stimuli. PLoSOne 2014, 16(9):e115247.
18. Denslow S., Lomarev M., Bohning D.E., Mu Q., George M.S. A high resolution assessment of the repeatability of relative location and intensity of transcranial magnetic stimulation-induced and volitionally induced blood oxygen level-dependent response in the motor cortex. Cogn Behav Neurol 2004, 17:163-173.
19. Di Lazzaro V., Oliviero A., Mazzone P., Insola A., Pilato F., Saturno E., et al. Comparison of descending volleys evoked by monophasic and biphasic magnetic stimulation of the motor cortex in conscious humans. Exp Brain Res 2001, 141:121-127.
20. Doeltgen S.H., Ridding M.C., O'Beirne G.A., Dalrymple-Alford J., Huckabee M.L. Test-retest reliability of motor evoked potentials (MEPs) at the submental muscle group during volitional swallowing. J Neurosci Methods 2009, 178:134-137.
21. Fitzgerald P.B., Fountain S., Daskalakis Z.J. A comprehensive review of the effects of rTMS on motor cortical excitability and inhibition. Clin Neurophysiol 2006, 117:2584-2596.
22. Fox J. Applied regression, linear models, and related methods 1997, Sage Publications, Thousand Oaks (CA).
23. Funke K., Benali A. Cortical cellular actions of transcranial magnetic stimulation. Restor Neurol Neurosci 2010, 28:399-417.
24. Furubayashi T., Mochizuki H., Terao Y., Arai N., Hanajima R., Hamada M., et al. Cortical hemoglobin concentration changes underneath the coil after single-pulse transcranial magnetic stimulation: a near-infrared spectroscopy study. J Neurophysiol 2013, 109:1626-1637.
25. Heide G., Witte O.W., Ziemann U. Physiology of modulation of motor cortex excitability by low-frequency suprathreshold repetitive transcranial magnetic stimulation. Exp Brain Res 2006, 171:26-34.
26. Hanakawa T., Mima T., Matsumoto R., Abe M., Inouchi M., Urayama S., et al. Stimulus-response profile during single-pulse transcranial magnetic stimulation to the primary motor cortex. Cereb Cortex 2009, 19:2605-2615.
27. Hoogendam J.M., Ramakers G.M., Di Lazzaro V. Physiology of repetitive transcranial magnetic stimulation of the human brain. Brain Stimul 2010, 3:95-118.
28. Ilmoniemi R.J., Virtanen J., Ruohonen J., Karhu J., Aronen H.J., Näätänen R., et al. Neuronal responses to magnetic stimulation reveal cortical reactivity and connectivity. NeuroReport 1997, 8:3537-3540.
29. Julkunen P., Saisanen L., Hukkanen T., Danner N., Kononen M. Does second-scale intertrial interval affect motor evoked potentials induced by single-pulse transcranial magnetic stimulation?. Brain Stimul 2012, 5:526-532.
30. Kamen G. Reliability of motor-evoked potentials during resting and active contraction conditions. Med Sci Sport Exerc 2004, 36:1574-1579.
31. Kawasaki M., Uno Y., Mori J., Kobata K., Kitajo K. Transcranial magnetic stimulation-induced global propagation of transient phase resetting associated with directional information flow. Front Hum Neurosci 2014, 8:173.
32. Kiers L., Cros D., Chiappa K.H., Fang J. Variability of motor potentials evoked by transcranial magnetic stimulation. Electroencephalogr Clin Neurophysiol 1993, 89:415-423.
33. McDonald J.H. Handbook of biological statistics 2009, Sparky House Publishing, Maryland, Baltimore, p. 173-81.
34. Moliadze V., Zhao Y., Eysel U., Funke K. Effect of transcranial magnetic stimulation on single-unit activity in the cat primary visual cortex. J Physiol 2003, 553:665-679.
35. Nielsen J.F. Logarithmic distribution of amplitudes of compound muscle action potentials evoked by transcranial magnetic stimulation. J Clin Neurophysiol 1996, 13:423-434.
36. Noguchi Y., Watanabe E., Sakai K.L. An event-related optical topography study of cortical activation induced by single-pulse transcranial magnetic stimulation. NeuroImage 2003, 19:156-162.
37. Oldfield R.C. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 1971, 9:97-113.
38. Pal P.K., Hanajima R., Gunraj C.A., et al. Effect of low-frequency repetitive transcranial magnetic stimulation on interhemispheric inhibition. J Neurophysiol 2005, 94:1668-1675.
39. Paus P., Sipila P.K., Strafella A.P. Synchronization of neuronal activity in the human primary motor cortex by transcranial magnetic stimulation: an EEG study. J Neurophysiol 2001, 86:1983-1990.
40. Pell G.S., Roth Y., Zangen A. Modulation of cortical excitability induced by repetitive transcranial magnetic stimulation: influence of timing and geometrical parameters and underlying mechanisms. Prog Neurobiol 2011, 93:59-98.
41. Ramsay J.O., Silverman B.W. Functional data analysis 2005, Springer, New York.
42. Rosanova M., Casali A., Bellina V., Resta F., Mariotti M., Massimini M. Natural frequencies of human corticothalamic circuits. J Neurosci 2009, 29:7679-7685.
43. Rosanova M., Casali A., Bellina V., Resta F., Mariotti M., Massimini M., et al. Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin Neurophysiol 2009, 120:2008-2039. Safety of TMS Consensus Group.
44. Rossini P.M., Barker A.T., Berardelli A., Caramia M.D., Caruso G., Cracco R.Q., 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.
45. Rossini P.M., Burke D., Chen R., Cohen L.G., Daskalakis Z., Di Iorio R., et al. Non-invasive electrical and magnetic stimulation of the brain, spinal cord, roots and peripheral nerves: basic principles and procedures for routine clinical and research application. An updated report from an I.F.C.N. Committee. Clin Neurophysiol 2015, 126:1071-1107.
46. Rothkegel H., Sommer M., Paulus W. Breaks during 5 Hz rTMS are essential for facilitatory after effects. Clin Neurophysiol 2010, 121:426-430.
47. Rothwell J.C., Hallett M., Berardelli A., Eisen A., Rossini P., Paulus W. Magnetic stimulation: motor evoked potentials. The International Federation of Clinical Neurophysiology. Electroencephalogr Clin Neurophysiol Suppl 1999, 52:97-103.
48. Schmidt S., Cichy R.M., Kraft A., Brocke J., Irlbacher K., Brandt S.A. An initial transient-state and reliable measures of corticospinal excitability in TMS studies. Clin Neurophysiol 2009, 120:987-993.
49. Sale M.V., Ridding M.C., Nordstrom M.A. Factors influencing the magnitude and reproducibility of corticomotor excitability changes induced by paired associative stimulation. Exp Brain Res 2007, 181:615-626.
50. Shitara H., Shinozaki T., Takagishi K., Honda M., Hanakawa T. Time course and spatial distribution of fMRI signal changes during single-pulse transcranial magnetic stimulation to the primary motor cortex. NeuroImage 2011, 56:1469-1479.
51. Sommer M., Alfaro A., Rummel M., Speck S., Lang N., Tings T., et al. Half sine, monophasic and biphasic transcranial magnetic stimulation of the human motor cortex. Clin Neurophysiol 2006, 117:838-844.
52. Stamoulis C., Oberman L.M., Praeg E., Bashir S., Pascual-Leone A. Single pulse TMS-induced modulations of resting brain neurodynamics encoded in EEG phase. Brain Topogr 2011, 24:105-113.
53. Thomson R.H., Maller J.J., Daskalakis Z.J., Fitzgerald P.B. Blood oxygenation changes resulting from trains of low frequency transcranial magnetic stimulation. Cortex 2012, 48:487-491.
54. Todd G., Butler J.E., Gandevia S.C., Taylor J.L. Decreased input to the motor cortex increases motor cortical excitability. Clin Neurophysiol 2006, 117:2496-2503.
55. Van Der Werf Y.D., Paus T. The neural response to transcranial magnetic stimulation of the human motor cortex. I. Intracortical and cortico-cortical contributions. Exp Brain Res 2006, 175:231-245.
56. Wagner T., Rushmore J., Eden U., Valero-Cabre A. Biophysical foundations underlying TMS: setting the stage for an effective use of neurostimulation in the cognitive neurosciences. Cortex 2009, 45:1025-1034.
57. Ziemann U., Paulus W., Nitsche M.A., Pascual-Leone A., Byblow W.D., Berardelli A., Siebner H.R., Classen J., Cohen L.G., Rothwell J.C. Consensus: Motor cortex plasticity protocols. Brain Stimul 2008, 1:164-182.