TMS motor mapping: method overview, research and clinical application
https://doi.org/10.17650/2222-8721-2022-12-4-10-19
Abstract
Cortical representations of muscles can be probed non‑invasively using transcranial magnetic stimulation (TMS) motor mapping. TMS mapping can be applied both in research and clinical settings to assess motor cortex reorganization under the influence of various factors, to clarify pathophysiological mechanisms of motor system damage in various diseases, and to develop novel biomarkers of this damage. The article discusses the main methodological aspects of TMS motor mapping: choosing stimulation intensity and interstimulus interval, using of grid, neuronavigation and robotic systems, determining of a target muscle, etc. Special attention is paid to the cortical motor representation parameters such as the “hot spot” and center of gravity localization, area, etc. and their reproducibility under various mapping protocols. A review of publications on the use of TMS motor mapping application in brain tumors, stroke and amyotrophic lateral sclerosis is presented. The most significant practical impact of TMS motor mapping of the cortex is seen in brain tumors when used for presurgical localization of eloquent motor areas, as it is associated with the improvement of functional outcomes and progression‑free survival.
About the Authors
A. G. PoydashevaRussian Federation
Alexandra Georgievna Poydasheva
80 Volokolamskoe Shosse, Moscow 125367
I. S. Bakulin
Russian Federation
80 Volokolamskoe Shosse, Moscow 125367
D. Yu. Lagoda
Russian Federation
80 Volokolamskoe Shosse, Moscow 125367
N. A. Suponeva
Russian Federation
80 Volokolamskoe Shosse, Moscow 125367
M. A. Piradov
Russian Federation
80 Volokolamskoe Shosse, Moscow 125367
References
1. Ebbesen C.L., Brecht M. Motor cortex – to act or not to act? Nat Rev Neurosci 2017;18(11):694–705. DOI: 10.1038/nrn.2017.119
2. Harris L.J., Almerigi J.B. Probing the human brain with stimulating electrodes: the story of Roberts Bartholow’s (1874) experiment on Mary Rafferty. Brain Cogn 2009;70(1):92–115. DOI: 10.1016/j.bandc.2009.01.008
3. Penfield W., Boldrey E. Somatic motor and sensory representation in the cerebral cortex of man as studied by electrical stimulation. Brain 1937;60:389–440.
4. Merton P.A., Morton H.B. Stimulation of the cerebral cortex in the intact human subject. Nature 1980;285(5762):227. DOI: 10.1038/285227a0
5. Barker A.T., Jalinous R., Freeston I.L. Non-invasive magnetic stimulation of human motor cortex. Lancet 1985;1(8437):1106–7. DOI: 10.1016/s0140-6736(85)92413-4
6. Cohen L.G., Bandinelli S., Topka H.R. et al. Topographic maps of human motor cortex in normal and pathological conditions: mirror movements, amputations and spinal cord injuries. Electroencephalogr Clin Neurophysiol Suppl 1991;43:36–50.
7. Ruohonen J., Karhu J. Navigated transcranial magnetic stimulation. Neurophysiol Clin 2010;40(1):7–17. DOI: 10.1016/j.neucli.2010.01.006
8. Nicolini C., Harasym D., Turco C.V. et al. Human motor cortical organization is influenced by handedness. Cortex 2019;115:172–83. DOI: 10.1016/j.cortex.2019.01.017
9. Raffin E., Siebner H.R. Use-dependent plasticity in human primary motor hand area: synergistic interplay between training and immobilization. Cereb Cortex 2019;29(1):356–71. DOI: 10.1093/cercor/bhy226
10. Krieg S.M., Lioumis P., Mäkelä J.P. et al. Protocol for motor and language mapping by navigated TMS in patients and healthy volunteers; workshop report. Acta Neurochir (Wien) 2017;159(7):1187–95. DOI: 10.1007/s00701-017-3187-z
11. Lüdemann-Podubecká J., Nowak D.A. Mapping cortical hand motor representation using TMS: A method to assess brain plasticity and a surrogate marker for recovery of function after stroke? Neurosci Biobehav Rev 2016;69:239–51. DOI: 10.1016/j.neubiorev.2016.07.006
12. Sondergaard R.E., Martino D., Kiss Z.H.T. et al. TMS Motor Mapping Methodology and Reliability: A Structured Review Front Neurosci 2021;15:709368. DOI: 10.3389/fnins.2021.709368
13. Portney L.G., Watkins M.P. Foundations of clinical research: applications to practice. Upper Saddle River: Pearson/Prentice Hall, 2009. 892 p.
14. Weiss C., Nettekoven C., Rehme A.K. et al. Mapping the hand, foot and face representations in the primary motor cortex – retest reliability of neuronavigated TMS versus functional MRI. Neuroimage 2013;66:531–42. DOI: 10.1016/j.neuroimage.2012. 10.046
15. Opitz A., Legon W., Rowlands A. et al. Physiological observations validate finite element models for estimating subject-specific electric field distributions induced by transcranial magnetic stimulation of the human motor cortex. Neuroimage 2013;81:253–64. DOI: 10.1016/j.neuroimage.2013.04.067
16. Malcolm M.P., Triggs W.J., Light K.E. et al. Reliability of motor cortex transcranial magnetic stimulation in four muscle representations. Clin Neurophysiol 2006;117(5):1037–46. DOI: 10.1016/j.clinph.2006.02.005
17. Cavaleri R., Schabrun S.M., Chipchase L.S. The reliability and validity of rapid transcranial magnetic stimulation mapping. Brain Stimul 2018;11(6):1291–5. DOI: 10.1016/j.brs.2018.07.043
18. Пойдашева А.Г., Бакулин И.С., Чернявский А.Ю. и др. Картирование корковых представительств мышц с помощью навигационной транскраниальной магнитной стимуляции: возможности применения в клинической практике. Медицинский алфавит 2017;2(22):21–5 Poydasheva A.G., Bakulin I.S., Chernyavskiy A.Yu. et al. Motor cortex mapping with navigated transcranial magnetic stimulation and its clinical application. Meditsinskiy Alfavit = Medical Alphabet 2017;2(22):21–5. (In Russ.)
19. Jonker Z.D., van der Vliet R., Hauwert C.M. et al. TMS motor mapping: Comparing the absolute reliability of digital reconstruction methods to the golden standard. Brain Stimul 2019;12(2):309–13. DOI: 10.1016/j.brs.2018.11.005
20. McGregor K.M., Carpenter H., Kleim E. et al. Motor map reliability and aging: a TMS/fMRI study. Exp Brain Res 2012;219(1):97–106. DOI: 10.1007/s00221-012-3070-3
21. Van de Ruit M., Perenboom M.J., Grey M.J. TMS brain mapping in less than two minutes. Brain Stimul 2015;8(2):231–9. DOI: 10.1016/j.brs.2014.10.020
22. Sinitsyn D.O., Chernyavskiy A.Y., Poydasheva A.G. et al. Optimization of the navigated TMS mapping algorithm for accurate estimation of cortical muscle representation characteristics. Brain Sci 2019;9(4):88. DOI: 10.3390/brainsci9040088
23. Wassermann E.M., McShane L.M., Hallett M. et al. Noninvasive mapping of muscle representations in human motor cortex. Electroencephalogr Clin Neurophysiol 1992;85(1):1–8. DOI: 10.1016/0168-5597(92)90094-r
24. Julkunen P., Järnefelt G., Savolainen P. et al. Facilitatory effect of paired-pulse stimulation by transcranial magnetic stimulation with biphasic wave-form. Med Eng Phys 2016;38(8):813–7. DOI: 10.1016/j.medengphy.2016.04.025
25. Grab J.G., Zewdie E., Carlson H.L. et al. Robotic TMS mapping of motor cortex in the developing brain. J Neurosci Methods 2018;309:41–54. DOI: 10.1016/j.jneumeth.2018.08.007
26. Giuffre A., Kahl C.K., Zewdie E. et al. Reliability of robotic transcranial magnetic stimulation motor mapping. J Neurophysiol 2021;125(1):74–85. DOI: 10.1152/jn.00527.2020
27. Novikov P.A., Nazarova M.A., Nikulin V.V. TMSmap – software for quantitative analysis of TMS mapping results. Front Hum Neurosci 2018;12:239. DOI: 10.3389/fnhum.2018.00239
28. Gerber M.B., McLean A.C., Stephen S.J. et al. NeuroMeasure: A Software Package for Quantification of Cortical Motor Maps Using Frameless Stereotaxic Transcranial Magnetic Stimulation. Front Neuroinform 2019;13:23. DOI: 10.3389/fninf.2019.00023
29. Ngomo S., Leonard G., Moffet H. et al. Comparison of transcranial magnetic stimulation measures obtained at rest and under active conditions and their reliability. J Neurosci Methods 2012;205(1):65–71. DOI: 10.1016/j.jneumeth.2011.12.012
30. Sollmann N., Zhang H., Kelm A. et al. Paired-pulse navigated TMS is more effective than single-pulse navigated TMS for mapping upper extremity muscles in brain tumor patients. Clin Neurophysiol 2020;131(12):2887–98. DOI: 10.1016/j.clinph.2020.09.025
31. Davies J.L. Using transcranial magnetic stimulation to map the cortical representation of lower-limb muscles. Clin Neurophysiol Pract 2020;5:87–99. DOI: 10.1016/j.cnp.2020.04.001
32. Cavaleri R., Schabrun S.M., Chipchase L.S. The number of stimuli required to reliably assess corticomotor excitability and primary motor cortical representations using transcranial magnetic stimulation (TMS): a systematic review and meta-analysis. Syst Rev 2017;6(1):48. DOI: 10.1186/s13643-017-0440-8
33. Ammann C., Guida P., Caballero-Insaurriaga J. et al. A framework to assess the impact of number of trials on the amplitude of motor evoked potentials. Sci Rep 2020;10(1):21422. DOI: 10.1038/s41598-020-77383-6
34. Chernyavskiy A.Y., Sinitsyn D.O., Poydasheva A.G. et al. Accuracy of estimating the area of cortical muscle representations from TMS mapping data using voronoi diagrams. Brain Topogr 2019;32(5):859–72. DOI: 10.1007/s10548-019-00714-y
35. Faghihpirayesh R., Imbiriba T., Yarossi M. et al. Motor Cortex Mapping using Active Gaussian Processes. Int Conf Pervasive Technol Relat Assist Environ 2020;2020:14. DOI: 10.1145/3389189.3389202
36. Haddad A.F., Young J.S., Berger M.S. et al. Preoperative applications of navigated transcranial magnetic stimulation. Front Neurol 2021;11:628903. DOI: 10.3389/fneur.2020.628903
37. Picht T., Schmidt S., Brandt S. et al. Preoperative functional mapping for rolandic brain tumor surgery: comparison of navigated transcranial magnetic stimulation to direct cortical stimulation. Neurosurgery 2011;69(3):581–8; discussion 588. DOI: 10.1227/NEU.0b013e3182181b89
38. Frey D., Schilt S., Strack V. et al. Navigated transcranial magnetic stimulation improves the treatment outcome in patients with brain tumors in motor eloquent locations. Neuro Oncol 2014;16(10):1365–72. DOI: 10.1093/neuonc/nou110
39. Krieg S.M., Picht T., Sollmann N. et al. Resection of motor eloquent metastases aided by preoperative nTMS-based motor maps-comparison of two observational cohorts. Front Oncol 2016;6:261. DOI: 10.3389/fonc.2016.00261
40. Rosenstock T., Grittner U., Acker G. et al. Risk stratification in motor area-related glioma surgery based on navigated transcranial magnetic stimulation data. J Neurosurg 2017;126(4):1227–37. DOI: 10.3171/2016.4.JNS152896
41. Münnich T., Klein J., Hattingen E. et al. Tractography verified by intraoperative magnetic resonance imaging and subcortical stimulation during tumor resection near the corticospinal tract. Oper Neurosurg (Hagerstown) 2019;16(2):197–210. DOI: 10.1093/ons/opy062
42. Sollmann N., Zhang H., Fratini A. et al. Risk assessment by presurgical tractography using navigated TMS maps in patients with highly motor- or language-eloquent brain tumors. Cancers (Basel) 2020;12(5):1264. DOI: 10.3390/cancers12051264
43. Bulubas L., Sollmann N., Tanigawa N. et al. Reorganization of motor representations in patients with brain lesions: a navigated transcranial magnetic stimulation study. Brain Topogr 2018;31(2):288–99. DOI: 10.1007/s10548-017-0589-4
44. Tarapore P.E., Picht T., Bulubas L. et al. Safety and tolerability of navigated TMS for preoperative mapping in neurosurgical patients. Clin Neurophysiol 2016;127(3):1895–900. DOI: 10.1016/j.clinph.2015.11.042
45. Di Pino G., Di Lazzaro V. The balance recovery bimodal model in stroke patients between evidence and speculation: Do recent studies support it? Clin Neurophysiol 2020;131(10):2488–90. DOI: 10.1016/j.clinph.2020.07.004
46. Plow E.B., Sankarasubramanian V., Cunningham D.A. et al. Models to tailor brain stimulation therapies in stroke. Neural Plast 2016;2016:4071620. DOI: 10.1155/2016/4071620
47. Veldema J., Bösl K., Nowak D.A. Motor recovery of the affected hand in subacute stroke correlates with changes of contralesional cortical hand motor representation. Neural Plast 2017;2017:6171903. DOI: 10.1155/2017/6171903
48. Liepert J., Miltner W.H., Bauder H. et al. Motor cortex plasticity during constraint-induced movement therapy in stroke patients. Neurosci Lett 1998;250(1):5–8. DOI: 10.1016/s0304-3940(98)00386-3
49. Sankarasubramanian V., Machado A.G., Conforto A.B. et al. Inhibition versus facilitation of contralesional motor cortices in stroke: deriving a model to tailor brain stimulation. Clin Neurophysiol 2017;128(6):892–902. DOI: 10.1016/j.clinph.2017.03.030
50. Назарова М.А. Мультимодальная оценка реорганизации двигательной системы руки после полушарного инсульта: МРТ–ТМС исследование. Автореф. дис. … канд. мед. наук. М., 2015. 122 с. Nazarova M.A. Multimodal assessment of the reorganization of the motor system of the hand after a hemispheric stroke: an MRI–TMS study. Author’s abstract of thesis … of candidate of medical sciences. Moscow, 2015. 122 p. (In Russ.)
51. De Carvalho M. Electrodiagnosis of amyotrophic lateral sclerosis: a review of existing guidelines. J Clin Neurophysiol 2020;37(4):294–8. DOI: 10.1097/WNP.0000000000000682
52. Chervyakov A.V., Bakulin I.S., Savitskaya N.G. et al. Navigated transcranial magnetic stimulation in amyotrophic lateral sclerosis. Muscle Nerve 2015;51(1):125–31.
53. Бакулин И.С., Пойдашева А.Г., Чернявский А.Ю. и др. Методика выявления поражения верхнего мотонейрона при боковом амиотрофическом склерозе с помощью транскраниальной магнитной стимуляции. Анналы клинической и экспериментальной неврологии 2018;12(2):45–54. DOI: 10.25692/ACEN.2018.2.7 Bakulin I.S., Poydasheva A.G., Chernyavsky A.Yu. et al. Methods of detecting lesions of upper motor neuron in amyotrophic lateral sclerosis using transcranial magnetic stimulation. Annaly klinicheskoy i eksperimentalnoy nevrologii = Annals of Clinical and Experimental Neurology 2018;12(2):45–54. (In Russ.)]. DOI: 10.25692/ACEN.2018.2.7
54. Бакулин И.С., Синицын Д.О., Пойдашева А.Г. и др. Навигационное ТМС-картирование с «сеточным» алгоритмом в оценке реорганизации корковых представительств мышц при боковом амиотрофическом склерозе. Анналы клинической и экспериментальной неврологии 2019;13(3):55–62. DOI: 10.25692/ACEN.2019.3.7 Bakulin I.S., Sinitsyn D.O., Poydasheva A.G. et al. Navigated TMS mapping using the grid-based algorithm to evaluate the reorganization of cortical muscle representation in amyotrophic lateral sclerosis. Annaly klinicheskoy i eksperimentalnoy nevrologii = Annals of Clinical and Experimental Neurology 2019;13(3): 55–62. (In Russ.)]. DOI: 10.25692/ACEN.2019.3.7
55. Zdunczyk A., Schwarzer V., Mikhailov M. et al. The corticospinal reserve capacity: reorganization of motor area and excitability as a novel pathophysiological concept in cervical myelopathy. Neurosurgery 2018;83(4):810–8. DOI: 10.1093/neuros/nyx437
56. Schieber M.H., Hibbard L.S. How somatotopic is the motor cortex hand area? Science 1993;261(5120):489–92. DOI: 10.1126/science.8332915
57. Kaas J.H. Evolution of columns, modules, and domains in the neocortex of primates. Proc Natl Acad Sci USA 2012;109(Suppl 1): 10655–60. DOI: 10.1073/pnas.1201892109
Review
For citations:
Poydasheva A.G., Bakulin I.S., Lagoda D.Yu., Suponeva N.A., Piradov M.A. TMS motor mapping: method overview, research and clinical application. Neuromuscular Diseases. 2022;12(4):10-19. (In Russ.) https://doi.org/10.17650/2222-8721-2022-12-4-10-19