Precise motor mapping with transcranial magnetic stimulation

Konstantin Weise, Ole Numssen, Benjamin Kalloch, Anna Leah Zier, Axel Thielscher, Jens Haueisen, Gesa Hartwigsen, Thomas R. Knösche

Published: 2022-12-01 DOI: 10.1038/s41596-022-00776-6

Transcranial Magnetic Stimulation

Motor Mapping

Cortical Electric Fields

MEPs

Numerical Modeling

AI 解读

暂无数据

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References

Weise, K., Numssen, O., Thielscher, A., Hartwigsen, G. & Knösche, T. R. A novel approach to localize cortical TMS effects. NeuroImage 209, 116486 (2020).
Numssen, O. et al. Efficient high-resolution TMS mapping of the human motor cortex by nonlinear regression. NeuroImage 245, 118654 (2021).
Goetz, S. M., Mahdi Alavi, S. M., Deng, Z.-D. & Peterchev, A. V. Statistical model of motor-evoked potentials. IEEE Trans. Neural Syst. Rehab. Eng. 27, 1539–1545 (2019).
Di Lazzaro, V. et al. Comparison of descending volleys evoked by transcranial magnetic and electric stimulation in conscious humans. Electroencephalogr. Clin. Neurophysiol. Electromyogr. Mot. Control. 109, 397–401 (1998).
Thielscher, A. & Wichmann, F. A. Determining the cortical target of transcranial magnetic stimulation. NeuroImage 47, 1319–1330 (2009).
Aberra, A. S., Wang, B., Grill, W. M. & Peterchev, A. V. Simulation of transcranial magnetic stimulation in head model with morphologically-realistic cortical neurons. Brain Stimul. 13, 175–189 (2020).
Siebner, H. R. Does TMS of the precentral motor hand knob primarily stimulate the dorsal premotor cortex or the primary motor hand area? Brain Stimul. 13, 517–518 (2020).
Devanne, H., Lavoie, B. A. & Capaday, C. Input-output properties and gain changes in the human corticospinal pathway. Exp. Brain Res. 114, 329–338 (1997).
Capaday, C. Neurophysiological methods for studies of the motor system in freely moving human subjects. J. Neurosci. Methods 74, 201–218 (1997).
Ridding, M. C. & Rothwell, J. C. Stimulus/response curves as a method of measuring motor cortical excitability in man. Electroencephalogr. Clin. Neurophysiol. Electromyogr. Mot. Control 105, 340–344 (1997).
Rösler, J. et al. Language mapping in healthy volunteers and brain tumor patients with a novel navigated TMS system: evidence of tumor-induced plasticity. Clin. Neurophysiol. 125, 526–536 (2014).
Shamov, T., Spiriev, T., Tzvetanov, P. & Petkov, A. The combination of neuronavigation with transcranial magnetic stimulation for treatment of opercular gliomas of the dominant brain hemisphere. Clin. Neurol. Neurosurg. 112, 672–677 (2010).
Pelletier, I., Sauerwein, H. C., Lepore, F., Saint-Amour, D. & Lassonde, M. Non-invasive alternatives to the Wada test in the presurgical evaluation of language and memory functions in epilepsy patients. Epileptic Disord. 9, 111–126 (2007).
Zmeykina, E., Mittner, M., Paulus, W. & Turi, Z. Weak rTMS-induced electric fields produce neural entrainment in humans. Sci. Rep. 10, 11994 (2020).
Thielscher, A., Reichenbach, A., Uğurbil, K. & Uludağ, K. The cortical site of visual suppression by transcranial magnetic stimulation. Cereb. Cortex 20, 328–338 (2010).
Rushworth, M. F., Ellison, A. & Walsh, V. Complementary localization and lateralization of orienting and motor attention. Nat. Neurosci. 4, 656–661 (2001).
Rosanova, M. et al. Natural frequencies of human corticothalamic circuits. J. Neurosci. 29, 7679–7685 (2009).
Chung, S. W. et al. Impact of different intensities of intermittent theta burst stimulation on the cortical properties during TMS–EEG and working memory performance. Hum. Brain Mapp. 39, 783–802 (2018).
Neggers, S. F. W. et al. A stereotactic method for image-guided transcranial magnetic stimulation validated with fMRI and motor-evoked potentials. NeuroImage 21, 1805–1817 (2004).
Kleim, J. A., Kleim, E. D. & Cramer, S. C. Systematic assessment of training-induced changes in corticospinal output to hand using frameless stereotaxic transcranial magnetic stimulation. Nat. Protoc. 2, 1675 (2007).
Sparing, R., Buelte, D., Meister, I. G., Pauš, T. & Fink, G. R. Transcranial magnetic stimulation and the challenge of coil placement: a comparison of conventional and stereotaxic neuronavigational strategies. Hum. Brain Mapp. 29, 82–96 (2008).
Ngomo, S., Leonard, G., Moffet, H. & Mercier, C. Comparison of transcranial magnetic stimulation measures obtained at rest and under active conditions and their reliability. J. Neurosci. Methods 205, 65–71 (2012).
van de Ruit, M., Perenboom, M. J. & Grey, M. J. TMS brain mapping in less than two minutes. Brain Stimul. 8, 231–239 (2015).
Wassermann, E. M. et al. Locating the motor cortex on the MRI with transcranial magnetic stimulation and PET. NeuroImage 3, 1–9 (1996).
Classen, J. et al. Multimodal output mapping of human central motor representation on different spatial scales. J. Physiol. 512, 163–179 (1998).
Krieg, S. et al. Optimal timing of pulse onset for language mapping with navigated repetitive transcranial magnetic stimulation. NeuroImage 100, 219–236 (2014).
Sondergaard, R. E., Martino, D., Kiss, Z. H. T. & Condliffe, E. G. TMS motor mapping methodology and reliability: a structured review. Front. Neurosci. 15, 1–13 (2021).
Kraus, D. & Gharabaghi, A. Projecting navigated TMS sites on the gyral anatomy decreases inter-subject variability of cortical motor maps. Brain Stimul. 8, 831–837 (2015).
Kraus, D. & Gharabaghi, A. Neuromuscular plasticity: disentangling stable and variable motor maps in the human sensorimotor cortex. Neural Plast. 2016, 7365609 (2016).
Mathew, J., Kubler, A., Bauer, R. & Gharabaghi, A. Probing corticospinal recruitment patterns and functional synergies with transcranial magnetic stimulation. Front. Cell. Neurosci. 10, 175 (2016).
Sollmann, N., Krieg, S. M., Säisänen, L. & Julkunen, P. Mapping of motor function with neuronavigated transcranial magnetic stimulation: a review on clinical application in brain tumors and methods for ensuring feasible accuracy. Brain Sci. 11, 897 (2021).
Julkunen, P. et al. Comparison of navigated and non-navigated transcranial magnetic stimulation for motor cortex mapping, motor threshold and motor evoked potentials. NeuroImage 44, 790–795 (2009).
Ruohonen, J. & Karhu, J. Navigated transcranial magnetic stimulation. Clin. Neurophysiol. 40, 7–17 (2010).
Opitz, A., Zafar, N., Bockermann, V., Rohde, V. & Paulus, W. Validating computationally predicted TMS stimulation areas using direct electrical stimulation in patients with brain tumors near precentral regions. NeuroImage Clin. 4, 500–507 (2014).
Mandija, S., Petrov, P. I., Neggers, S. F., Luijten, P. R. & van den Berg, C. A. MR‐based measurements and simulations of the magnetic field created by a realistic transcranial magnetic stimulation (TMS) coil and stimulator. NMR Biomed. 29, 1590–1600 (2016).
Opitz, 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 81, 253–264 (2013).
Aonuma, S. et al. A high-resolution computational localization method for transcranial magnetic stimulation mapping. NeuroImage 172, 85–93 (2018).
Niyazov, D. M., Butler, A. J., Kadah, Y. M., Epstein, C. M. & Hu, X. P. Functional magnetic resonance imaging and transcranial magnetic stimulation: effects of motor imagery, movement and coil orientation. Clin. Neurophysiol. 116, 1601–1610 (2005).
Laakso, I., Murakami, T., Hirata, A. & Ugawa, Y. Where and what TMS activates: experiments and modeling. Brain Stimul. 11, 166–174 (2018).
Windhoff, M., Opitz, A. & Thielscher, A. Electric field calculations in brain stimulation based on finite elements: an optimized processing pipeline for the generation and usage of accurate individual head models. Hum. Brain Mapp. 34, 923–935 (2013).
Nielsen, J. D. et al. Automatic skull segmentation from MR images for realistic volume conductor models of the head: assessment of the state-of-the-art. NeuroImage 174, 587–598 (2018).
Puonti, O. et al. Accurate and robust whole-head segmentation from magnetic resonance images for individualized head modeling. NeuroImage 219, 117044 (2020).
Huang, Y. et al. Automated MRI segmentation for individualized modeling of current flow in the human head. J. Neural Eng. 10, 066004 (2013).
Huang, Y., Datta, A., Bikson, M. & Parra, L. C. Realistic volumetric-approach to simulate transcranial electric stimulation—ROAST—a fully automated open-source pipeline. J. Neural Eng. 16, 056006 (2019).
Rashed, E. A., Gomez-Tames, J. & Hirata, A. Development of accurate human head models for personalized electromagnetic dosimetry using deep learning. NeuroImage 202, 116132 (2019).
Fortunati, V. et al. Automatic tissue segmentation of head and neck MR images for hyperthermia treatment planning. Phys. Med. Biol. 60, 6547 (2015).
Thielscher, A., Antunes A., Saturnino, G. B. Field modeling for transcranial magnetic stimulation: a useful tool to understand the physiological effects of TMS? 37th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC), (2015); http://doi.org/10.1109/embc.2015.7318340
Saturnino, G. B., Madsen, K. H. & Thielscher, A. Electric field simulations for transcranial brain stimulation using FEM: an efficient implementation and error analysis. J. Neural Eng. 16, 066032 (2019).
Opitz, A., Windhoff, M., Heidemann, R. M., Turner, R. & Thielscher, A. How the brain tissue shapes the electric field induced by transcranial magnetic stimulation. NeuroImage 58, 849–859 (2011).
Rossi, S. et al. Safety and recommendations for TMS use in healthy subjects and patient populations, with updates on training, ethical and regulatory issues: expert guidelines. Clin. Neurophysiol. 132, 269–306 (2021).
Numssen, O., et al. Precise motor mapping with transcranial magnetic stimulation—data and code. osf.io http://doi.org/10.17605/OSF.IO/MYRQN (2021).
Bikson, M. et al. Guidelines for TMS/tES clinical services and research through the COVID-19 pandemic. Brain Stimul. 13, 1124–1149 (2020).
Pascual-Leone A, Davey NJ, Rothwell J, Wasserman EM, Puri BK (Eds.). Handbook of transcranial magnetic stimulation (Arnold, 2002).
Sommer, M. et al. Half sine, monophasic and biphasic transcranial magnetic stimulation of the human motor cortex. Clin. Neurophysiol. 117, 838–844 (2006).
Kammer, T., Beck, S., Thielscher, A., Laubis-Herrmann, U. & Topka, H. Motor thresholds in humans: a transcranial magnetic stimulation study comparing different pulse waveforms, current directions and stimulator types. Clin. Neurophysiol., 112, 250–258 (2001).
Li, X., Morgan, P. S., Ashburner, J., Smith, J. & Rorden, C. The first step for neuroimaging data analysis: DICOM to NIfTI conversion. J. Neurosci. Methods 264, 47–56 (2016).
Dale, A. M., Fischl, B. & Sereno, M. I. Cortical surface-based analysis. I. Segmentation and surface reconstruction. NeuroImage 9, 179–194 (1999).
Fischl, B., Sereno, M. I. & Dale, A. M. Cortical surface-based analysis. II: Inflation, flattening, and a surface-based coordinate system. NeuroImage 9, 195–207 (1999).
Ahrens, James, Geveci, Berk, Law, Charles, ParaView: An End-User Tool for Large Data Visualization, Visualization Handbook (Elsevier, 2005). (ISBN-13: 978-0123875822)
Ayachit, Utkarsh, The ParaView Guide: A Parallel Visualization Application (Kitware, 2015). (ISBN 978-1930934306)
Geuzaine, C. & Remacle, J.-F. Gmsh: a three-dimensional finite element mesh generator with built-in pre- and post-processing facilities. Int. J. Numer. Methods Eng. 79, 1309–1331 (2009).
Saturnino, G. B., Thielscher, A., Madsen, K. H., Knösche, T. R. & Weise, K. A principled approach to conductivity uncertainty analysis in electric field calculations. NeuroImage 188, 821–834 (2019).
Mayka, M. A., Corcos, D. M., Leurgans, S. E. & Vaillancourt, D. E. Three-dimensional s and boundaries of motor and premotor cortices as defined by functional brain imaging: a meta-analysis. NeuroImage 31, 1453–1474 (2006).
Awiszus F, Chapter 2 TMS and threshold hunting. In Transcranial Magnetic Stimulation and Transcranial Direct Current Stimulation, Proceedings of the 2nd International Transcranial Magnetic Stimulation (TMS) and Transcranial Direct Current Stimulation (tDCS) Symposium (pp. 13–23).
Julkunen, P., Säisänen, L., Hukkanen, T., Danner, N. & Könönen, M. Does second-scale intertrial interval affect motor evoked potentials induced by single-pulse transcranial magnetic stimulation? Brain Stimul. 5, 526–532 (2012).
Brasil‐Neto, J. P., Cohen, L. G. & Hallett, M. Central fatigue as revealed by postexercise decrement of motor evoked potentials. Muscle Nerve. 17, 713–719 (1994).
Rossini, P. M. 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 IFCN Committee. Clin. Neurophysiol. 126, 1071–1107 (2015).
Möller, C., Arai, N., Lücke, J. & Ziemann, U. Hysteresis effects on the input–output curve of motor evoked potentials. Clin. Neurophysiol. 120, 1003–1008 (2009).
Schmidt, S. et al. An initial transient-state and reliable measures of corticospinal excitability in TMS studies. Clin. Neurophysiol. 120, 987–993 (2009).
Brasil-Neto, J. P. et al. Optimal focal transcranial magnetic activation of the human motor cortex: effects of coil orientation, shape of the induced current pulse, and stimulus intensity. J. Clin. Neurophysiol. 9, 132–136 (1992). (PMID: 1552001).
Mills, K. R., Boniface, S. J. & Schubert, M. Magnetic brain stimulation with a double coil: the importance of coil orientation. Electroencephalogr. Clin. Neurophysiol. Evoked Potentials 85, 17–21 (1992).
Bungert, A., Antunes, A., Espenhahn, S. & Thielscher, A. Where does TMS stimulate the motor cortex? Combining electrophysiological measurements and realistic field estimates to reveal the affected cortex position. Cereb. Cortex 27, 5083–5094 (2017).
Pellegrini, M., Zoghi, M. & Jaberzadeh, S. The effect of transcranial magnetic stimulation test intensity on the amplitude, variability and reliability of motor evoked potentials. Brain Res. 1700, 190–198 (2018).
Gray H. Anatomy of the Human Body (Lea & Febiger, 1918).

Precise motor mapping with transcranial magnetic stimulation

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