Brain Topography

, Volume 31, Issue 2, pp 288–299 | Cite as

Reorganization of Motor Representations in Patients with Brain Lesions: A Navigated Transcranial Magnetic Stimulation Study

  • Lucia Bulubas
  • Nico Sollmann
  • Noriko Tanigawa
  • Claus Zimmer
  • Bernhard Meyer
  • Sandro M. Krieg
Original Paper


This is an explorative study applying presurgical navigated transcranial magnetic stimulation (nTMS) to investigate the spatial distributions of motor sites to reveal tumor-induced brain plasticity in patients with brain tumors. We analyzed nTMS-based motor maps derived from presurgical mapping of 100 patients with motor eloquently located brain tumors (tumors in the frontal lobe, the precentral gyrus [PrG], the postcentral gyrus [PoG], the remaining parietal lobe, or the temporal lobe). Based on these motor maps, we systematically investigated changes in motor evoked potential (MEP) counts among 4 gyri (PrG, PoG, medial frontal gyrus, and superior frontal gyrus) between subgroups of patients according to the tumor location in order to depict the tumor’s influence on reorganization. When comparing patients with different tumor locations, high MEP counts were elicited less frequently by stimulating the PrG in patients with tumors directly affecting the PrG (p < 0.05). Still, in more than 50% of these patients, the MEP counts elicited by stimulating the PrG were higher than average, indicating robust motor representations within the primary motor cortex. In contrast, patients with PoG and parietal tumors primarily showed high MEP counts when stimulating the PoG (p < 0.10). The functional reorganization is not likely to induce a shift of motor function from the PrG to adjacent regions but rather leads to a reorganization within anatomical constraints, such as of the PoG. Thus, presurgical nTMS-based motor mapping sensitively depicted the tumor-induced plasticity of the motor cortex.


Brain tumor Cortical mapping Motor evoked potentials Navigated transcranial magnetic stimulation Presurgical motor mapping 





Abductor digiti minimi muscle


Analysis of variance


Abductor pollicis brevis muscle


British Medical Research Council


Direct cortical stimulation




Flexor carpi radialis muscle


High-grade glioma


Low-grade glioma


Motor evoked potential


Middle frontal gyrus


Magnetic resonance imaging


Navigated transcranial magnetic stimulation


Premotor cortex


Postcentral gyrus


Precentral gyrus


Resting motor threshold


Superior frontal gyrus


Upper extremity



LB and NS gratefully acknowledge the support of the Graduate School’s Faculty Graduate Center of Medicine at our university. Moreover, the study was supported by grants of the Wilhelm Sander foundation.


The study was financed by institutional grants from the Department of Neurosurgery, the Section of Neuroradiology, and the Wilhelm Sander foundation.

Compliance with Ethical Standards

Conflict of interest

SK and BM are consultants for Brainlab AG (Munich, Germany). SK is a consultant for Nexstim Plc. (Helsinki, Finland). The authors declare that they have no conflict of interest.

Ethical Approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

Informed Consent

Informed consent was obtained from all individual participants included in the study.


  1. Almairac F, Herbet G, Moritz-Gasser S, Duffau H (2014) Parietal network underlying movement control: disturbances during subcortical electrostimulation. Neurosurg Rev 37:513–516. doi: 10.1007/s10143-014-0530-1 (discussion 516-517)CrossRefPubMedGoogle Scholar
  2. Bulubas L et al (2016) Motor areas of the frontal cortex in patients with motor eloquent brain lesions. J Neurosurg 125:1431–1442. doi: 10.3171/2015.11.JNS152103 CrossRefPubMedGoogle Scholar
  3. Capelle L et al (2013) Spontaneous and therapeutic prognostic factors in adult hemispheric World Health Organization Grade II gliomas: a series of 1097 cases: clinical article. J Neurosurg 118:1157–1168. doi: 10.3171/2013.1.JNS121 CrossRefPubMedGoogle Scholar
  4. Cicinelli P, Traversa R, Rossini PM (1997) Post-stroke reorganization of brain motor output to the hand: a 2–4 month follow-up with focal magnetic transcranial stimulation. Electroencephalogr Clin Neurophysiol 105:438–450CrossRefPubMedGoogle Scholar
  5. Conway N et al (2017) Cortical plasticity of motor-eloquent areas measured by navigated transcranial magnetic stimulation in patients with glioma. J Neurosurg:1–11 doi: 10.3171/2016.9.JNS161595
  6. Desmurget M, Bonnetblanc F, Duffau H (2007) Contrasting acute and slow-growing lesions: a new door to. Brain Plast Brain 130:898–914. doi: 10.1093/brain/awl300 Google Scholar
  7. Duffau H (2005) Lessons from brain mapping in surgery for low-grade glioma: insights into associations between tumour and brain plasticity. Lancet Neurol 4:476–486. doi: 10.1016/S1474-4422(05)70140-X CrossRefPubMedGoogle Scholar
  8. Duffau H (2006) Brain plasticity: from pathophysiological mechanisms to therapeutic applications. J Clin Neurosci 13:885–897. doi: 10.1016/j.jocn.2005.11.045 CrossRefPubMedGoogle Scholar
  9. Duffau H (2014) The huge plastic potential of adult brain and the role of connectomics: new insights provided by serial mappings in glioma surgery. Cortex 58:325–337. doi: 10.1016/j.cortex.2013.08.005 CrossRefPubMedGoogle Scholar
  10. Duffau H, Denvil D, Capelle L (2002) Long term reshaping of language, sensory, and motor maps after glioma resection: a new parameter to integrate in the surgical strategy. J Neurol Neurosurg Psychiatr 72:511–516Google Scholar
  11. Fridman EA, Hanakawa T, Chung M, Hummel F, Leiguarda RC, Cohen LG (2004) Reorganization of the human ipsilesional premotor cortex after stroke. Brain 127:747–758. doi: 10.1093/brain/awh082 CrossRefPubMedGoogle Scholar
  12. Hayashi Y, Nakada M, Kinoshita M, Hamada J (2014) Functional reorganization in the patient with progressing glioma of the pure primary motor cortex: a case report with special reference to the topographic central sulcus defined by somatosensory-evoked potential. World Neurosurg 82:536 e531–534 doi: 10.1016/j.wneu.2013.01.084
  13. Herbet G, Maheu M, Costi E, Lafargue G, Duffau H (2016) Mapping neuroplastic potential in brain-damaged patients. Brain 139:829–844. doi: 10.1093/brain/awv394 CrossRefPubMedGoogle Scholar
  14. Ius T, Angelini E, Thiebaut de Schotten M, Mandonnet E, Duffau H (2011) Evidence for potentials and limitations of brain plasticity using an atlas of functional resectability of WHO grade II gliomas: towards a “minimal common brain”. Neuroimage 56:992–1000. doi: 10.1016/j.neuroimage.2011.03.022 CrossRefPubMedGoogle Scholar
  15. Kelly-Hayes M, Beiser A, Kase CS, Scaramucci A, D’Agostino RB, Wolf PA (2003) The influence of gender and age on disability following ischemic stroke: the Framingham study. J Stroke Cerebrovasc Dis 12:119–126. doi: 10.1016/s1052-3057(03)00042-9 CrossRefPubMedGoogle Scholar
  16. Kombos T, Suess O, Kern BC, Funk T, Hoell T, Kopetsch O, Brock M (1999) Comparison between monopolar and bipolar electrical stimulation of the motor cortex. Acta Neurochir 141:1295–1301. doi: 10.1007/s007010050433 CrossRefPubMedGoogle Scholar
  17. Krieg SM, Shiban E, Buchmann N, Gempt J, Foerschler A, Meyer B, Ringel F (2012) Utility of presurgical navigated transcranial magnetic brain stimulation for the resection of tumors in eloquent motor areas. J Neurosurg 116:994–1001. doi: 10.3171/2011.12.JNS111524 CrossRefPubMedGoogle Scholar
  18. Krieg SM et al (2015) Changing the clinical course of glioma patients by preoperative motor mapping with navigated transcranial magnetic brain stimulation. BMC Cancer 15:231. doi: 10.1186/s12885-015-1258-1 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Krieg SM et al (2017) Protocol for motor and language mapping by navigated TMS in patients and healthy volunteers; workshop report. Acta Neurochir. doi: 10.1007/s00701-017-3187-z PubMedGoogle Scholar
  20. Liu Y, Rouiller EM (1999) Mechanisms of recovery of dexterity following unilateral lesion of the sensorimotor cortex in adult monkeys. Exp Brain Res 128:149–159CrossRefPubMedGoogle Scholar
  21. Mesulam MM (1998) From sensation to cognition. Brain 121(6):1013–1052CrossRefPubMedGoogle Scholar
  22. Moser T et al (2016) Resection of nTMS-positive prerolandic motor areas causes permanent impairment of motor function. Neurosurgery. doi: 10.1093/neuros/nyw169 Google Scholar
  23. Pascual-Leone A et al (2011) Characterizing brain cortical plasticity and network dynamics across the age-span in health and disease with TMS-EEG and TMS-fMRI. Brain Topogr 24:302–315. doi: 10.1007/s10548-011-0196-8 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Picht T et al (2011) Preoperative functional mapping for rolandic brain tumor surgery: comparison of navigated transcranial magnetic stimulation to direct. Cortic Stimul Neurosurg 69:581–588. doi: 10.1227/NEU.0b013e3182181b89 (discussion 588)Google Scholar
  25. Picht T, Strack V, Schulz J, Zdunczyk A, Frey D, Schmidt S, Vajkoczy P (2012) Assessing the functional status of the motor system in brain tumor patients using transcranial magnetic stimulation. Acta Neurochir 154:2075–2081. doi: 10.1007/s00701-012-1494-y CrossRefPubMedGoogle Scholar
  26. Robles SG, Gatignol P, Lehericy S, Duffau H (2008) Long-term brain plasticity allowing a multistage surgical approach to World Health Organization Grade II gliomas in eloquent areas. J Neurosurg 109:615–624. doi: 10.3171/JNS/2008/109/10/0615 CrossRefPubMedGoogle Scholar
  27. Rosenstock T, Grittner U, Acker G, Schwarzer V, Kulchytska N, Vajkoczy P, Picht T (2016) Risk stratification in motor area-related glioma surgery based on navigated transcranial magnetic stimulation data. J Neurosurg. doi: 10.3171/2016.4.JNS152896 PubMedGoogle Scholar
  28. Rossini PM et al (1994) 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 91:79–92CrossRefPubMedGoogle Scholar
  29. Rossini PM et al (2015) 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 126:1071–1107. doi: 10.1016/j.clinph.2015.02.001 CrossRefPubMedGoogle Scholar
  30. Saisanen L et al (2008) Motor potentials evoked by navigated transcranial magnetic stimulation in healthy subjects. J Clin Neurophysiol 25:367–372. doi: 10.1097/WNP.0b013e31818e7944 CrossRefPubMedGoogle Scholar
  31. Seitz RJ, Huang Y, Knorr U, Tellmann L, Herzog H, Freund HJ (1995) Large-scale plasticity of the human motor cortex. Neuroreport 6:742–744CrossRefPubMedGoogle Scholar
  32. Seitz RJ, Hoflich P, Binkofski F, Tellmann L, Herzog H, Freund HJ (1998) Role of the premotor cortex in recovery from middle cerebral artery infarction. Arch Neurol 55:1081–1088CrossRefPubMedGoogle Scholar
  33. Sollmann N et al (2017a) Clinical factors underlying the inter-individual variability of the resting motor threshold in navigated transcranial magnetic stimulation motor mapping. Brain Topogr 30:98–121. doi: 10.1007/s10548-016-0536-9)CrossRefPubMedGoogle Scholar
  34. Sollmann N, Bulubas L, Tanigawa N, Zimmer C, Meyer B, Krieg SM (2017b) The variability of motor evoked potential latencies in neurosurgical motor mapping by preoperative navigated transcranial magnetic stimulation. BMC Neurosci 18:5. doi: 10.1186/s12868-016-0321-4)CrossRefPubMedPubMedCentralGoogle Scholar
  35. Southwell DG, Hervey-Jumper SL, Perry DW, Berger MS (2016) Intraoperative mapping during repeat awake craniotomy reveals the functional plasticity of adult cortex. J Neurosurg 124:1460–1469. doi: 10.3171/2015.5.JNS142833 CrossRefPubMedGoogle Scholar
  36. Tarapore PE, Tate MC, Findlay AM, Honma SM, Mizuiri D, Berger MS, Nagarajan SS (2012) Preoperative multimodal motor mapping: a comparison of magnetoencephalography imaging, navigated transcranial magnetic stimulation, and direct cortical stimulation. J Neurosurg 117:354–362. doi: 10.3171/2012.5.JNS112124 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Tarapore PE et al (2016a) Safety and tolerability of navigated TMS for preoperative mapping in neurosurgical patients. Clin Neurophysiol 127:1895–1900. doi: 10.1016/j.clinph.2015.11.042 a)CrossRefPubMedGoogle Scholar
  38. Tarapore PE et al (2016b) Safety and tolerability of navigated TMS in healthy volunteers. Clin. neurophysiol. 127:1916–1918. doi: 10.1016/j.clinph.2015.11.043 b)CrossRefPubMedGoogle Scholar
  39. Teitti S et al (2008) Non-primary motor areas in the human frontal lobe are connected directly to hand muscles. Neuroimage 40:1243–1250 doi: 10.1016/j.neuroimage.2007.12.065 CrossRefPubMedGoogle Scholar
  40. Uematsu S et al (1992) Motor and sensory cortex in humans: topography studied with chronic subdural stimulation. Neurosurgery 31:59–71 (discussion 71-52)CrossRefPubMedGoogle Scholar
  41. van Geemen K, Herbet G, Moritz-Gasser S, Duffau H (2014) Limited plastic potential of the left ventral premotor cortex in speech articulation: evidence from intraoperative awake mapping in glioma patients. Hum Brain Mapp 35:1587–1596. doi: 10.1002/hbm.22275 CrossRefPubMedGoogle Scholar
  42. Weiller C, Ramsay SC, Wise RJ, Friston KJ, Frackowiak RS (1993) Individual patterns of functional reorganization in the human cerebral cortex after capsular infarction. Ann Neurol 33:181–189. doi: 10.1002/ana.410330208 CrossRefPubMedGoogle Scholar
  43. Wunderlich G, Knorr U, Herzog H, Kiwit JC, Freund HJ, Seitz RJ (1998) Precentral glioma location determines the displacement of cortical hand representation. Neurosurgery 42:18–26 (discussion 26-17)CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  1. 1.Department of NeurosurgeryKlinikum rechts der Isar, Technische Universität MünchenMunichGermany
  2. 2.TUM-Neuroimaging CenterKlinikum rechts der Isar, Technische Universität MünchenMunichGermany
  3. 3.Section of Neuroradiology, Department of RadiologyKlinikum rechts der Isar, Technische Universität MünchenMunichGermany
  4. 4.Faculty of Linguistics, Philology & PhoneticsUniversity of OxfordOxfordUK

Personalised recommendations