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

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Abstract

Background

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.

Method

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

Results

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.

Conclusion

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.

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References

  1. Agarwal VS, Thakor NV, Lesser RP, Gordon B, Nathan SS (1994) Modelling electrical stimulation of the human cerebral cortex. Annu Int Conf IEEE 1:185–186

    Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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 98:764–778

    Article  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  22. Geddes LA (2004) Accuracy limitations of chronaxie values. IEEE Trans Biomed Eng 51:176–181. doi:10.1109/TBME.2003.820340

    Article  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  28. Haglund MM, Ojemann GA, Blasdel GG (1993) Optical imaging of bipolar cortical stimulation. J Neurosurg 78:785–793

    Article  CAS  PubMed  Google Scholar 

  29. Hamberger MJ, Goodman RR, Perrine K, Tamny T (2001) Anatomic dissociation of auditory and visual naming in the lateral temporal cortex. Neurology 56:56–61

    CAS  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  31. Hamberger MJ, Seidel WT, Goodman RR, Perrine K, McKhann GM (2003) Temporal lobe stimulation reveals anatomic distinction between auditory naming processes. Neurology 60:1478–1483

    CAS  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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 11:2997–3000

    Article  CAS  PubMed  Google Scholar 

  35. Jayakar P (1993) Electrical and magnetic stimulation of the brain and spinal cord. Raven Press, New York

    Google Scholar 

  36. Jayakar P (1993) Physiological principles of electrical stimulation. Adv Neurol 63:17–27

    CAS  PubMed  Google Scholar 

  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

    CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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 100:369–375

    Article  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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 62:1323–1332

    CAS  PubMed  Google Scholar 

  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 92:589–598

    Article  CAS  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  50. McClelland JL, Rogers TT (2003) The parallel distributed processing approach to semantic cognition. Nat Rev Neurosci 4:310–322. doi:10.1038/nrn1076

    Article  CAS  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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 11:385–421

    Google Scholar 

  53. Montgomery EB Jr, Baker KB (2000) Mechanisms of deep brain stimulation and future technical developments. Neurol Res 22:259–266

    PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  56. Nathan SS, Lesser RP, Gordon B, Nv T (1993) Electrical stimulation of the human cerebral cortex. Theoritical approach. Raven Press, New York

    Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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 71:316–326

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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 Neurol

  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 101:458–466

    Article  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  66. Ranck JB (1981) Extracellular stimulation. Academic Press, New York

    Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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 1345–1337

    Article  PubMed  Google Scholar 

  71. Sanai N, Berger MS (2008) Glioma extent of resection and its impact on patient outcome. Neurosurgery 62:753–764. doi:10.1227/01.neu.0000318159.21731.cf discussion 264–756

    Article  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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 88:349–351

    Article  CAS  PubMed  Google Scholar 

  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

    Article  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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 90:35–41

    Article  CAS  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  80. Testerman RL (2005) Comments on "accuracy limitations of chronaxie values". IEEE Trans Biomed Eng 52:750. doi:10.1109/TBME.2004.836506

    Article  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  83. Yeomans JS (1990) Principles of brain stimulation. Oxford University Press, New York

    Google Scholar 

  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 91:922–927

    Article  CAS  PubMed  Google Scholar 

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The authors thank Dr. Mélanie Pelegrini-Issac and Mrs. Judy Benson for helpful comments on the manuscript and English revision.

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Mandonnet, E., Winkler, P.A. & Duffau, H. Direct electrical stimulation as an input gate into brain functional networks: principles, advantages and limitations. Acta Neurochir 152, 185–193 (2010). https://doi.org/10.1007/s00701-009-0469-0

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