Acta Neurochirurgica

, Volume 152, Issue 2, pp 185–193 | Cite as

Direct electrical stimulation as an input gate into brain functional networks: principles, advantages and limitations

  • Emmanuel Mandonnet
  • Peter A. Winkler
  • Hugues Duffau
Review Article



While the fundamental and clinical contribution of direct electrical stimulation (DES) of the brain is now well acknowledged, its advantages and limitations have not been re-evaluated for a long time.


Here, we critically review exactly what DES can tell us about cerebral function.


First, we show that DES is highly sensitive for detecting the cortical and axonal eloquent structures. Moreover, DES also provides a unique opportunity to study brain connectivity, since each area responsive to stimulation is in fact an input gate into a large-scale network rather than an isolated discrete functional site. DES, however, also has a limitation: its specificity is suboptimal. Indeed, DES may lead to interpretations that a structure is crucial because of the induction of a transient functional response when stimulated, whereas (1) this effect is caused by the backward spreading of the electro-stimulation along the network to an essential area and/or (2) the stimulated region can be functionally compensated owing to long-term brain plasticity mechanisms.


In brief, although DES is still the gold standard for brain mapping, its combination with new methods such as perioperative neurofunctional imaging and biomathematical modeling is now mandatory, in order to clearly differentiate those networks that are actually indispensable to function from those that can be compensated.


Brain mapping Connectivity Direct electrical stimulation Neural networks Plasticity 


  1. 1.
    Agarwal VS, Thakor NV, Lesser RP, Gordon B, Nathan SS (1994) Modelling electrical stimulation of the human cerebral cortex. Annu Int Conf IEEE 1:185–186Google Scholar
  2. 2.
    Agnew WF, McCreery DB (1987) Considerations for safety in the use of extracranial stimulation for motor evoked potentials. Neurosurgery 20:143–147. doi:10.1097/00006123-198701000-00030 CrossRefPubMedGoogle Scholar
  3. 3.
    Bartels A, Zeki S (2005) The chronoarchitecture of the cerebral cortex. Philos Trans R Soc Lond B Biol Sci 360:733–750. doi:10.1098/rstb.2005.1627 CrossRefPubMedGoogle Scholar
  4. 4.
    Bartolomei F, Wendling F, Chauvel P (2008) The concept of an epileptogenic network in human partial epilepsies. Neurochirurgie 54:174–184. doi:10.1016/j.neuchi.2008.02.013 CrossRefPubMedGoogle Scholar
  5. 5.
    Bassett DS, Meyer-Lindenberg A, Achard S, Duke T, Bullmore E (2006) Adaptive reconfiguration of fractal small-world human brain functional networks. Proc Natl Acad Sci USA 103:19518–19523. doi:10.1073/pnas.0606005103 CrossRefPubMedGoogle Scholar
  6. 6.
    Berger MS, Rostomily RC (1997) Low grade gliomas: functional mapping resection strategies, extent of resection, and outcome. J Neurooncol 34:85–101. doi:10.1023/A:1005715405413 CrossRefPubMedGoogle Scholar
  7. 7.
    Butson CR, McIntyre CC (2006) Role of electrode design on the volume of tissue activated during deep brain stimulation. J Neural Eng 3:1–8. doi:10.1088/1741-2560/3/1/001 CrossRefPubMedGoogle Scholar
  8. 8.
    Cilia R, Landi A, Vergani F, Sganzerla E, Pezzoli G, Antonini A (2007) Extradural motor cortex stimulation in Parkinson's disease. Mov Disord 22:111–114. doi:10.1002/mds.21207 CrossRefPubMedGoogle Scholar
  9. 9.
    du Boisgueheneuc F, Levy R, Volle E, Seassau M, Duffau H, Kinkingnehun S, Samson Y, Zhang S, Dubois B (2006) Functions of the left superior frontal gyrus in humans: a lesion study. Brain 129:3315–3328. doi:10.1093/brain/awl244 CrossRefPubMedGoogle Scholar
  10. 10.
    Duffau H (2004) Intraoperative functional mapping using direct electrical stimulations. Methodological considerations. Neurochirurgie 50:474–483. doi:10.1016/S0028-3770(04)98328-2 CrossRefPubMedGoogle Scholar
  11. 11.
    Duffau H (2005) Intraoperative cortico-subcortical stimulations in surgery of low-grade gliomas. Expert Rev Neurother 5:473–485. doi:10.1586/14737175.5.4.473 CrossRefPubMedGoogle Scholar
  12. 12.
    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
  13. 13.
    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
  14. 14.
    Duffau H (2006) New concepts in surgery of WHO grade II gliomas: functional brain mapping, connectionism and plasticity——a review. J Neurooncol 79:77–115. doi:10.1007/s11060-005-9109-6 CrossRefPubMedGoogle Scholar
  15. 15.
    Duffau H, Capelle L, Denvil D, Sichez N, Gatignol P, Taillandier L, Lopes M, Mitchell MC, Roche S, Muller JC, Bitar A, Sichez JP, van Effenterre R (2003) Usefulness of intraoperative electrical subcortical mapping during surgery for low-grade gliomas located within eloquent brain regions: functional results in a consecutive series of 103 patients. J Neurosurg 98:764–778CrossRefPubMedGoogle Scholar
  16. 16.
    Duffau H, Capelle L, Sichez N, Denvil D, Lopes M, Sichez JP, Bitar A, Fohanno D (2002) Intraoperative mapping of the subcortical language pathways using direct stimulations. An anatomo-functional study. Brain 125:199–214. doi:10.1093/brain/awf016 CrossRefPubMedGoogle Scholar
  17. 17.
    Duffau H, Gatignol P, Mandonnet E, Peruzzi P, Tzourio-Mazoyer N, Capelle L (2005) New insights into the anatomo-functional connectivity of the semantic system: a study using cortico-subcortical electrostimulations. Brain 128:797–810. doi:10.1093/brain/awh423 CrossRefPubMedGoogle Scholar
  18. 18.
    Duffau H, Lopes M, Arthuis F, Bitar A, Sichez JP, Van Effenterre R, Capelle L (2005) Contribution of intraoperative electrical stimulations in surgery of low grade gliomas: a comparative study between two series without (1985–96) and with (1996–2003) functional mapping in the same institution. J Neurol Neurosurg Psychiatry 76:845–851. doi:10.1136/jnnp. 2004.048520 CrossRefPubMedGoogle Scholar
  19. 19.
    Duffau H, Peggy Gatignol ST, Mandonnet E, Capelle L, Taillandier L (2008) Intraoperative subcortical stimulation mapping of language pathways in a consecutive series of 115 patients with grade II glioma in the left dominant hemisphere. J Neurosurg 109:461–471. doi:10.3171/JNS/2008/109/9/0461 CrossRefPubMedGoogle Scholar
  20. 20.
    Fried I, Mateer C, Ojemann G, Wohns R, Fedio P (1982) Organization of visuospatial functions in human cortex. Evidence from electrical stimulation. Brain 105:349–371. doi:10.1093/brain/105.2.349 CrossRefPubMedGoogle Scholar
  21. 21.
    Fuentes R, Petersson P, Siesser WB, Caron MG, Nicolelis MA (2009) Spinal cord stimulation restores locomotion in animal models of Parkinson's disease. Science 323:1578–1582. doi:10.1126/science.1164901 CrossRefPubMedGoogle Scholar
  22. 22.
    Geddes LA (2004) Accuracy limitations of chronaxie values. IEEE Trans Biomed Eng 51:176–181. doi:10.1109/TBME.2003.820340 CrossRefPubMedGoogle Scholar
  23. 23.
    Geddes LA, Baker LE (1967) The specific resistance of biological material—a compendium of data for the biomedical engineer and physiologist. Med Biol Eng 5:271–293. doi:10.1007/BF02474537 CrossRefPubMedGoogle Scholar
  24. 24.
    Giese A, Bjerkvig R, Berens ME, Westphal M (2003) Cost of migration: invasion of malignant gliomas and implications for treatment. J Clin Oncol 21:1624–1636. doi:10.1200/JCO.2003.05.063 CrossRefPubMedGoogle Scholar
  25. 25.
    Gil Robles S, Gatignol P, Capelle L, Mitchell MC, Duffau H (2005) The role of dominant striatum in language: a study using intraoperative electrical stimulations. J Neurol Neurosurg Psychiatry 76:940–946. doi:10.1136/jnnp. 2004.045948 CrossRefPubMedGoogle Scholar
  26. 26.
    Gordon B, Lesser RP, Rance NE, Hart J Jr, Webber R, Uematsu S, Fisher RS (1990) Parameters for direct cortical electrical stimulation in the human: histopathologic confirmation. Electroencephalogr Clin Neurophysiol 75:371–377. doi:10.1016/0013-4694(90)90082-U CrossRefPubMedGoogle Scholar
  27. 27.
    Haglund MM, Berger MS, Shamseldin MB, Lettich E, Ojemann G (1994) Cortical localization of temporal lobe language sites in patients with gliomas. Neurosurgery 34:567–576. doi:10.1097/00006123-199404000-00001 CrossRefPubMedGoogle Scholar
  28. 28.
    Haglund MM, Ojemann GA, Blasdel GG (1993) Optical imaging of bipolar cortical stimulation. J Neurosurg 78:785–793CrossRefPubMedGoogle Scholar
  29. 29.
    Hamberger MJ, Goodman RR, Perrine K, Tamny T (2001) Anatomic dissociation of auditory and visual naming in the lateral temporal cortex. Neurology 56:56–61PubMedGoogle Scholar
  30. 30.
    Hamberger MJ, McClelland S 3rd, McKhann GM 2nd, Williams AC, Goodman RR (2007) Distribution of auditory and visual naming sites in nonlesional temporal lobe epilepsy patients and patients with space-occupying temporal lobe lesions. Epilepsia 48:531–538. doi:10.1111/j.1528-1167.2006.00955.x CrossRefPubMedGoogle Scholar
  31. 31.
    Hamberger MJ, Seidel WT, Goodman RR, Perrine K, McKhann GM (2003) Temporal lobe stimulation reveals anatomic distinction between auditory naming processes. Neurology 60:1478–1483PubMedGoogle Scholar
  32. 32.
    Hamberger MJ, Seidel WT, McKhann GM 2nd, Perrine K, Goodman RR (2005) Brain stimulation reveals critical auditory naming cortex. Brain 128:2742–2749. doi:10.1093/brain/awh621 CrossRefPubMedGoogle Scholar
  33. 33.
    Havel P, Braun B, Rau S, Tonn JC, Fesl G, Bruckmann H, Ilmberger J (2006) Reproducibility of activation in four motor paradigms: An fMRI study. J Neurol 253:471–476. doi:10.1007/s00415-005-0028-4 CrossRefPubMedGoogle Scholar
  34. 34.
    Ishitobi M, Nakasato N, Suzuki K, Nagamatsu K, Shamoto H, Yoshimoto T (2000) Remote discharges in the posterior language area during basal temporal stimulation. NeuroReport 11:2997–3000PubMedCrossRefGoogle Scholar
  35. 35.
    Jayakar P (1993) Electrical and magnetic stimulation of the brain and spinal cord. Raven Press, New YorkGoogle Scholar
  36. 36.
    Jayakar P (1993) Physiological principles of electrical stimulation. Adv Neurol 63:17–27PubMedGoogle Scholar
  37. 37.
    Jayakar P, Alvarez LA, Duchowny MS, Resnick TJ (1992) A safe and effective paradigm to functionally map the cortex in childhood. J Clin Neurophysiol 9:288–293. doi:10.1097/00004691-199204010-00009 PubMedGoogle Scholar
  38. 38.
    Johnson MD, Ojemann GA (2000) The role of the human thalamus in language and memory: evidence from electrophysiological studies. Brain Cogn 42:218–230. doi:10.1006/brcg.1999.1101 CrossRefPubMedGoogle Scholar
  39. 39.
    Keles GE, Lundin DA, Lamborn KR, Chang EF, Ojemann G, Berger MS (2004) Intraoperative subcortical stimulation mapping for hemispherical perirolandic gliomas located within or adjacent to the descending motor pathways: evaluation of morbidity and assessment of functional outcome in 294 patients. J Neurosurg 100:369–375CrossRefPubMedGoogle Scholar
  40. 40.
    Kinoshita M, Yamada K, Hashimoto N, Kato A, Izumoto S, Baba T, Maruno M, Nishimura T, Yoshimine T (2005) Fiber-tracking does not accurately estimate size of fiber bundle in pathological condition: initial neurosurgical experience using neuronavigation and subcortical white matter stimulation. Neuroimage 25:424–429. doi:10.1016/j.neuroimage.2004.07.076 CrossRefPubMedGoogle Scholar
  41. 41.
    Korvenoja A, Kirveskari E, Aronen HJ, Avikainen S, Brander A, Huttunen J, Ilmoniemi RJ, Jaaskelainen JE, Kovala T, Makela JP, Salli E, Seppa M (2006) Sensorimotor cortex localization: comparison of magnetoencephalography, functional MR imaging, and intraoperative cortical mapping. Radiology 241:213–222. doi:10.1148/radiol.2411050796 CrossRefPubMedGoogle Scholar
  42. 42.
    Krainik A, Duffau H, Capelle L, Cornu P, Boch AL, Mangin JF, Le Bihan D, Marsault C, Chiras J, Lehericy S (2004) Role of the healthy hemisphere in recovery after resection of the supplementary motor area. Neurology 62:1323–1332PubMedGoogle Scholar
  43. 43.
    Lehericy S, Duffau H, Cornu P, Capelle L, Pidoux B, Carpentier A, Auliac S, Clemenceau S, Sichez JP, Bitar A, Valery CA, Van Effenterre R, Faillot T, Srour A, Fohanno D, Philippon J, Le Bihan D, Marsault C (2000) Correspondence between functional magnetic resonance imaging somatotopy and individual brain anatomy of the central region: comparison with intraoperative stimulation in patients with brain tumors. J Neurosurg 92:589–598CrossRefPubMedGoogle Scholar
  44. 44.
    Luders H, Lesser RP, Hahn J, Dinner DS, Morris HH, Wyllie E, Godoy J (1991) Basal temporal language area. Brain 114(Pt 2):743–754. doi:10.1093/brain/114.2.743 CrossRefPubMedGoogle Scholar
  45. 45.
    Mandonnet E, Capelle L, Duffau H (2006) Extension of paralimbic low grade gliomas: toward an anatomical classification based on white matter invasion patterns. J Neurooncol 78:179–185. doi:10.1007/s11060-005-9084-y CrossRefPubMedGoogle Scholar
  46. 46.
    Manola L, Holsheimer J, Veltink P, Buitenweg JR (2007) Anodal vs cathodal stimulation of motor cortex: a modeling study. Clin Neurophysiol 118:464–474. doi:10.1016/j.clinph.2006.09.012 CrossRefPubMedGoogle Scholar
  47. 47.
    Marrelec G, Krainik A, Duffau H, Pelegrini-Issac M, Lehericy S, Doyon J, Benali H (2006) Partial correlation for functional brain interactivity investigation in functional MRI. Neuroimage 32:228–237. doi:10.1016/j.neuroimage.2005.12.057 CrossRefPubMedGoogle Scholar
  48. 48.
    Matsumoto R, Nair DR, LaPresto E, Bingaman W, Shibasaki H, Luders HO (2007) Functional connectivity in human cortical motor system: a cortico-cortical evoked potential study. Brain 130:181–197. doi:10.1093/brain/awl257 CrossRefPubMedGoogle Scholar
  49. 49.
    Matsumoto R, Nair DR, LaPresto E, Najm I, Bingaman W, Shibasaki H, Luders HO (2004) Functional connectivity in the human language system: a cortico-cortical evoked potential study. Brain 127:2316–2330. doi:10.1093/brain/awh246 CrossRefPubMedGoogle Scholar
  50. 50.
    McClelland JL, Rogers TT (2003) The parallel distributed processing approach to semantic cognition. Nat Rev Neurosci 4:310–322. doi:10.1038/nrn1076 CrossRefPubMedGoogle Scholar
  51. 51.
    McIntyre CC, Savasta M, Walter BL, Vitek JL (2004) How does deep brain stimulation work? Present understanding and future questions. J Clin Neurophysiol 21:40–50. doi:10.1097/00004691-200401000-00006 CrossRefPubMedGoogle Scholar
  52. 52.
    Montgomery EB Jr (2004) Dynamically coupled, high-frequency reentrant, non-linear oscillators embedded in scale-free ganglia-thalamic-cortical networks mediating function and deep brain stimulation effects. Nonlinear Stud 11:385–421Google Scholar
  53. 53.
    Montgomery EB Jr, Baker KB (2000) Mechanisms of deep brain stimulation and future technical developments. Neurol Res 22:259–266PubMedGoogle Scholar
  54. 54.
    Montgomery EB Jr, Gale JT (2008) Mechanisms of action of deep brain stimulation (DBS). Neurosci Biobehav Rev 32:388–407. doi:10.1016/j.neubiorev.2007.06.003 CrossRefPubMedGoogle Scholar
  55. 55.
    Naeser MA, Palumbo CL, Helm-Estabrooks N, Stiassny-Eder D, Albert ML (1989) Severe nonfluency in aphasia. Role of the medial subcallosal fasciculus and other white matter pathways in recovery of spontaneous speech. Brain 112(Pt 1):1–38. doi:10.1093/brain/112.1.1 CrossRefPubMedGoogle Scholar
  56. 56.
    Nathan SS, Lesser RP, Gordon B, Nv T (1993) Electrical stimulation of the human cerebral cortex. Theoritical approach. Raven Press, New YorkGoogle Scholar
  57. 57.
    Nowak LG, Bullier J (1998) Axons, but not cell bodies, are activated by electrical stimulation in cortical gray matter. I. Evidence from chronaxie measurements. Exp Brain Res 118:477–488. doi:10.1007/s002210050304 CrossRefPubMedGoogle Scholar
  58. 58.
    Nowak LG, Bullier J (1998) Axons, but not cell bodies, are activated by electrical stimulation in cortical gray matter. II. Evidence from selective inactivation of cell bodies and axon initial segments. Exp Brain Res 118:489–500. doi:10.1007/s002210050305 CrossRefPubMedGoogle Scholar
  59. 59.
    Ojemann G, Ojemann J, Lettich E, Berger M (1989) Cortical language localization in left, dominant hemisphere. An electrical stimulation mapping investigation in 117 patients. J Neurosurg 71:316–326CrossRefPubMedGoogle Scholar
  60. 60.
    Pagni CA, Altibrandi MG, Bentivoglio A, Caruso G, Cioni B, Fiorella C, Insola A, Lavano A, Maina R, Mazzone P, Signorelli CD, Sturiale C, Valzania F, Zeme S, Zenga F (2005) Extradural motor cortex stimulation (EMCS) for Parkinson's disease. History and first results by the study group of the Italian neurosurgical society. Acta Neurochir Suppl (Wien) 93:113–119. doi:10.1007/3-211-27577-0_19 CrossRefGoogle Scholar
  61. 61.
    Pallud J, Devaux B, Daumas-Duport C, Oppenheim C, Roux FX (2005) Glioma dissemination along the corticospinal tract. J Neurooncol 73:239–240. doi:10.1007/s11060-005-0378-x CrossRefPubMedGoogle Scholar
  62. 62.
    Ponten SC, Douw L, Bartolomei F, Reijneveld JC, Stam CJ (2009) Indications for network regularization during absence seizures: Weighted and unweighted graph theoretical analyses. Exp NeurolGoogle Scholar
  63. 63.
    Pouratian N, Cannestra AF, Bookheimer SY, Martin NA, Toga AW (2004) Variability of intraoperative electrocortical stimulation mapping parameters across and within individuals. J Neurosurg 101:458–466CrossRefPubMedGoogle Scholar
  64. 64.
    Quigg M, Fountain NB (1999) Conduction aphasia elicited by stimulation of the left posterior superior temporal gyrus. J Neurol Neurosurg Psychiatry 66:393–396. doi:10.1136/jnnp. 66.3.393 CrossRefPubMedGoogle Scholar
  65. 65.
    Quigg M, Geldmacher DS, Elias WJ (2006) Conduction aphasia as a function of the dominant posterior perisylvian cortex. Report of two cases. J Neurosurg 104:845–848. doi:10.3171/jns.2006.104.5.845 CrossRefPubMedGoogle Scholar
  66. 66.
    Ranck JB (1981) Extracellular stimulation. Academic Press, New YorkGoogle Scholar
  67. 67.
    Ranck JB Jr (1975) Which elements are excited in electrical stimulation of mammalian central nervous system: a review. Brain Res 98:417–440. doi:10.1016/0006-8993(75)90364-9 CrossRefPubMedGoogle Scholar
  68. 68.
    Rattay F (1999) The basic mechanism for the electrical stimulation of the nervous system. Neuroscience 89:335–346. doi:10.1016/S0306-4522(98)00330-3 CrossRefPubMedGoogle Scholar
  69. 69.
    Rau S, Fesl G, Bruhns P, Havel P, Braun B, Tonn JC, Ilmberger J (2007) Reproducibility of activations in Broca area with two language tasks: a functional MR imaging study. AJNR Am J Neuroradiol 28:1346–1353. doi:10.3174/ajnr.A0581 CrossRefPubMedGoogle Scholar
  70. 70.
    Roux FE, Boulanouar K, Lotterie JA, Mejdoubi M, LeSage JP, Berry I (2003) Language functional magnetic resonance imaging in preoperative assessment of language areas: correlation with direct cortical stimulation. Neurosurgery 52:1335–1345. doi:10.1227/01.NEU.0000064803.05077.40 discussion 1345–1337CrossRefPubMedGoogle Scholar
  71. 71.
    Sanai N, Berger MS (2008) Glioma extent of resection and its impact on patient outcome. Neurosurgery 62:753–764. doi:10.1227/ discussion 264–756CrossRefPubMedGoogle Scholar
  72. 72.
    Sanai N, Mirzadeh Z, Berger MS (2008) Functional outcome after language mapping for glioma resection. N Engl J Med 358:18–27. doi:10.1056/NEJMoa067819 CrossRefPubMedGoogle Scholar
  73. 73.
    Sartorius CJ, Berger MS (1998) Rapid termination of intraoperative stimulation-evoked seizures with application of cold Ringer's lactate to the cortex. Technical note. J Neurosurg 88:349–351CrossRefPubMedGoogle Scholar
  74. 74.
    Scherer H (1940) The forms of growth in gliomas and their practical significance. Brain 63:1–35. doi:10.1093/brain/63.1.1 CrossRefGoogle Scholar
  75. 75.
    Seeck M, Pegna AJ, Ortigue S, Spinelli L, Dessibourg CA, Delavelle J, Blanke O, Michel CM, Landis T, Villemure JG (2006) Speech arrest with stimulation may not reliably predict language deficit after epilepsy surgery. Neurology 66:592–594. doi:10.1212/01.wnl.0000199254.67398.a7 CrossRefPubMedGoogle Scholar
  76. 76.
    Smith JS, Chang EF, Lamborn KR, Chang SM, Prados MD, Cha S, Tihan T, Vandenberg S, McDermott MW, Berger MS (2008) Role of extent of resection in the long-term outcome of low-grade hemispheric gliomas. J Clin Oncol 26:1338–1345. doi:10.1200/JCO.2007.13.9337 CrossRefPubMedGoogle Scholar
  77. 77.
    Spencer SS (2002) Neural networks in human epilepsy: evidence of and implications for treatment. Epilepsia 43:219–227. doi:10.1046/j.1528-1157.2002.26901.x CrossRefPubMedGoogle Scholar
  78. 78.
    Taylor MD, Bernstein M (1999) Awake craniotomy with brain mapping as the routine surgical approach to treating patients with supratentorial intraaxial tumors: a prospective trial of 200 cases. J Neurosurg 90:35–41CrossRefPubMedGoogle Scholar
  79. 79.
    Teixidor P, Gatignol P, Leroy M, Masuet-Aumatell C, Capelle L, Duffau H (2007) Assessment of verbal working memory before and after surgery for low-grade glioma. J Neurooncol 81:305–313. doi:10.1007/s11060-006-9233-y CrossRefPubMedGoogle Scholar
  80. 80.
    Testerman RL (2005) Comments on "accuracy limitations of chronaxie values". IEEE Trans Biomed Eng 52:750. doi:10.1109/TBME.2004.836506 CrossRefPubMedGoogle Scholar
  81. 81.
    Thiebaut de Schotten M, Urbanski M, Duffau H, Volle E, Levy R, Dubois B, Bartolomeo P (2005) Direct evidence for a parietal-frontal pathway subserving spatial awareness in humans. Science 309:2226–2228. doi:10.1126/science.1116251 CrossRefPubMedGoogle Scholar
  82. 82.
    Warman EN, Grill WM, Durand D (1992) Modeling the effects of electric fields on nerve fibers: determination of excitation thresholds. IEEE Trans Biomed Eng 39:1244–1254. doi:10.1109/10.184700 CrossRefPubMedGoogle Scholar
  83. 83.
    Yeomans JS (1990) Principles of brain stimulation. Oxford University Press, New YorkGoogle Scholar
  84. 84.
    Yingling CD, Ojemann S, Dodson B, Harrington MJ, Berger MS (1999) Identification of motor pathways during tumor surgery facilitated by multichannel electromyographic recording. J Neurosurg 91:922–927CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Emmanuel Mandonnet
    • 1
    • 4
  • Peter A. Winkler
    • 2
  • Hugues Duffau
    • 3
  1. 1.Unité 678, Inserm/UPMCParis Cedex 13France
  2. 2.Department of Neurosurgery, Klinikum GrosshadernMarchioninistrasse 15, Ludwig Maximilian University of MunichMunichGermany
  3. 3.Department of NeurosurgeryHôpital Gui de Chauliac, CHU de MontpellierMontpellier Cedex 5France
  4. 4.Department of NeurosurgeryHôpital Lariboisière—Service de NeurochirurgieParisFrance

Personalised recommendations