The Use of Motor Mapping to Aid Resection of Eloquent Gliomas

Neurosurgery Clinics of North America

Volumn 23, Issue 2, 2012, Pages 215-225

  Choi, Bryan D ^a   Mehta, Ankit I ^a   Batich, Kristen A ^a   Friedman, Allan H ^a   Sampson, John H ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Brain mapping; Glioma; Motor cortex; Neurosurgery

Indexed keywords

BOLD SIGNAL; BRAIN CORTEX STIMULATION; BRAIN MAPPING; CENTRAL SULCUS; DIFFUSION WEIGHTED IMAGING; ELECTROMYOGRAM; ELECTROSTIMULATION; EVOKED SOMATOSENSORY RESPONSE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GLIOMA; HUMAN; MAGNETOENCEPHALOGRAPHY; MOTOR CORTEX; MOTOR SYSTEM; NEUROIMAGING; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; REVIEW; SENSORIMOTOR CORTEX; SURGICAL TECHNIQUE; TRANSCRANIAL MAGNETIC STIMULATION;

BRAIN MAPPING; BRAIN NEOPLASMS; GLIOMA; HUMANS; MONITORING, INTRAOPERATIVE; MOTOR CORTEX; NEUROSURGICAL PROCEDURES;

EID: 84858608734     PISSN: 10423680     EISSN: 15581349     Source Type: Journal    
DOI: 10.1016/j.nec.2012.01.013     Document Type: Review

References (120)

1. Shapiro W.R. Treatment of neuroectodermal brain tumors. Ann Neurol 1982, 12:231-237.
2. Sanai N., Berger M.S. Glioma extent of resection and its impact on patient outcome. Neurosurgery 2008, 62:753-764. [discussion: 264-6].
3. Ammirati M., Vick N., Liao Y.L., et al. Effect of the extent of surgical resection on survival and quality of life in patients with supratentorial glioblastomas and anaplastic astrocytomas. Neurosurgery 1987, 21:201-206.
4. Ciric I., Ammirati M., Vick N., et al. Supratentorial gliomas: surgical considerations and immediate postoperative results. Gross total resection versus partial resection. Neurosurgery 1987, 21:21-26.
5. Hirakawa K., Suzuki K., Ueda S., et al. Multivariate analysis of factors affecting postoperative survival in malignant astrocytoma. Importance of DNA quantification. J Neurooncol 1984, 2:331-340.
6. Yordanova Y.N., Moritz-Gasser S., Duffau H. Awake surgery for WHO Grade II gliomas within " noneloquent" areas in the left dominant hemisphere: toward a " supratotal" resection. Clinical article. J Neurosurg 2011, 115:232-239.
7. Ballance C. A glimpse into the history of the surgery of the brain. Lancet 1922, 1:111-116.
8. Foerster O. The motor cortex in man in the light of Hughlings Jackson's doctrines. Brain 1936, 59:135-159.
9. Fritsch G., Hitzig E. Electric excitability of the cerebrum (Uber die elektrische erregbarkeit des grosshirns). Epilepsy Behav 2009, 15:123-130.
10. 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, 70:92-115.
11. Horsley V. Remarks on ten consecutive cases of operations upon the brain and cranial cavity to illustrate the details and safety of the method employed. Br Med J 1887, 1:863-865.
12. Thomas H.M., Cushing H. Removal of a subcortical cystic tumor at a second-stage operation without anesthesia. JAMA 1908, 50:847-856.
13. Cushing H. A note upon the faradic stimulation of the postcentral gyrus in conscious patients. Brain 1909, 32:44-53.
14. Cushing H. Partial hypophysectomy for acromegaly: with remarks on the function of the hypophysis. Ann Surg 1909, 50:1002-1017.
15. Penfield W., Boldrey E. Somatic motor and sensory representation in the cerebral cortex of man as studied by electrical stimulation. Brain 1937, 60:389-443.
16. Penfield W., Perot P. The brain's record of auditory and visual experience. A final summary and discussion. Brain 1963, 86:595-696.
17. Agnew W.F., McCreery D.B. Considerations for safety in the use of extracranial stimulation for motor evoked potentials. Neurosurgery 1987, 20:143-147.
18. Jayakar P. Physiological principles of electrical stimulation. Adv Neurol 1993, 63:17-27.
19. Yingling C.D., Ojemann S., Dodson B., et al. Identification of motor pathways during tumor surgery facilitated by multichannel electromyographic recording. J Neurosurg 1999, 91:922-927.
20. Sartorius C.J., Berger M.S. Rapid termination of intraoperative stimulation-evoked seizures with application of cold Ringer's lactate to the cortex. Technical note. J Neurosurg 1998, 88:349-351.
21. Gordon B., Lesser R.P., Rance N.E., et al. Parameters for direct cortical electrical stimulation in the human: histopathologic confirmation. Electroencephalogr Clin Neurophysiol 1990, 75:371-377.
22. Jayakar P., Alvarez L.A., Duchowny M.S., et al. A safe and effective paradigm to functionally map the cortex in childhood. J Clin Neurophysiol 1992, 9:288-293.
23. Cedzich C., Taniguchi M., Schafer S., et al. Somatosensory evoked potential phase reversal and direct motor cortex stimulation during surgery in and around the central region. Neurosurgery 1996, 38:962-970.
24. Taniguchi M., Cedzich C., Schramm J. Modification of cortical stimulation for motor evoked potentials under general anesthesia: technical description. Neurosurgery 1993, 32:219-226.
25. Haglund M.M., Ojemann G.A., Hochman D.W. Optical imaging of epileptiform and functional activity in human cerebral cortex. Nature 1992, 358:668-671.
26. Haglund M.M., Ojemann G.A., Blasdel G.G. Optical imaging of bipolar cortical stimulation. J Neurosurg 1993, 78:785-793.
27. Nathan S.S., Sinha S.R., Gordon B., et al. Determination of current density distributions generated by electrical stimulation of the human cerebral cortex. Electroencephalogr Clin Neurophysiol 1993, 86:183-192.
28. Phillips C.G., Porter R. Unifocal and bifocal stimulation of the motor cortex. J Physiol 1962, 162:532-538.
29. Wongsarnpigoon A., Grill W.M. Computer-based model of epidural motor cortex stimulation: effects of electrode position and geometry on activation of cortical neurons. Clin Neurophysiol 2012, 123(1):160-172.
30. Kombos T., Suess O., Kern B.C., et al. Comparison between monopolar and bipolar electrical stimulation of the motor cortex. Acta Neurochir (Wien) 1999, 141:1295-1301.
31. Suess O., Suess S., Brock M., et al. Intraoperative electrocortical stimulation of Brodman area 4: a 10-year analysis of 255 cases. Head Face Med 2006, 2:20.
32. Ng W.H., Ochi A., Rutka J.T., et al. Stimulation threshold potentials of intraoperative cortical motor mapping using monopolar trains of five in pediatric epilepsy surgery. Childs Nerv Syst 2010, 26:675-679.
33. Ranck J.B. Which elements are excited in electrical stimulation of mammalian central nervous system: a review. Brain Res 1975, 98:417-440.
34. Tehovnik E.J. Electrical stimulation of neural tissue to evoke behavioral responses. J Neurosci Methods 1996, 65:1-17.
35. Tehovnik E.J., Tolias A.S., Sultan F., et al. Direct and indirect activation of cortical neurons by electrical microstimulation. J Neurophysiol 2006, 96:512-521.
36. Nowak L.G., Bullier J. 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 1998, 118:489-500.
37. Berger M.S., Kincaid J., Ojemann G.A., et al. Brain mapping techniques to maximize resection, safety, and seizure control in children with brain tumors. Neurosurgery 1989, 25:786-792.
38. Ebeling U., Schmid U.D., Reulen H.J. Tumour-surgery within the central motor strip: surgical results with the aid of electrical motor cortex stimulation. Acta Neurochir (Wien) 1989, 101:100-107.
39. Ebeling U., Schmid U.D., Ying H., et al. Safe surgery of lesions near the motor cortex using intra-operative mapping techniques: a report on 50 patients. Acta Neurochir (Wien) 1992, 119:23-28.
40. Kombos T., Suess O., Ciklatekerlio O., et al. Monitoring of intraoperative motor evoked potentials to increase the safety of surgery in and around the motor cortex. J Neurosurg 2001, 95:608-614.
41. Kombos T., Suess O., Funk T., et al. Intra-operative mapping of the motor cortex during surgery in and around the motor cortex. Acta Neurochir (Wien) 2000, 142:263-268.
42. Berger M.S., Ojemann G.A., Lettich E. Neurophysiological monitoring during astrocytoma surgery. Neurosurg Clin N Am 1990, 1:65-80.
43. Luders H.O., Dinner D.S., Morris H.H., et al. Cortical electrical stimulation in humans. The negative motor areas. Adv Neurol 1995, 67:115-129.
44. Sutherling W.W., Crandall P.H., Darcey T.M., et al. The magnetic and electric fields agree with intracranial localizations of somatosensory cortex. Neurology 1988, 38:1705-1714.
45. Szelenyi A., Langer D., Beck J., et al. Transcranial and direct cortical stimulation for motor evoked potential monitoring in intracerebral aneurysm surgery. Neurophysiol Clin 2007, 37:391-398.
46. Lang F.F., Olansen N.E., DeMonte F., et al. Surgical resection of intrinsic insular tumors: complication avoidance. J Neurosurg 2001, 95:638-650.
47. Peraud A., Meschede M., Eisner W., et al. Surgical resection of grade II astrocytomas in the superior frontal gyrus. Neurosurgery 2002, 50:966-975. [discussion: 75-7].
48. Coenen V.A., Krings T., Mayfrank L., et al. Three-dimensional visualization of the pyramidal tract in a neuronavigation system during brain tumor surgery: first experiences and technical note. Neurosurgery 2001, 49:86-92. [discussion: 92-3].
49. Carrabba G., Fava E., Giussani C., et al. Cortical and subcortical motor mapping in rolandic and perirolandic glioma surgery: impact on postoperative morbidity and extent of resection. J Neurosurg Sci 2007, 51:45-51.
50. Duffau H., Capelle L., Denvil D., et al. 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 2003, 98:764-778.
51. Keles G.E., Lundin D.A., Lamborn K.R., et al. 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 2004, 100:369-375.
52. Goldring S. A method for surgical management of focal epilepsy, especially as it relates to children. J Neurosurg 1978, 49:344-356.
53. Goldring S., Gregorie E.M. Surgical management of epilepsy using epidural recordings to localize the seizure focus. Review of 100 cases. J Neurosurg 1984, 60:457-466.
54. Aiba T., Seki Y. Intraoperative identification of the central sulcus: a practical method. Acta Neurochir Suppl (Wien) 1988, 42:22-26.
55. Allen A., Starr A., Nudleman K. Assessment of sensory function in the operating room utilizing cerebral evoked potentials: a study of fifty-six surgically anesthetized patients. Clin Neurosurg 1981, 28:457-481.
56. Allison T. Scalp and cortical recordings of initial somatosensory cortex activity to median nerve stimulation in man. Ann N Y Acad Sci 1982, 388:671-678.
57. Allison T. Localization of sensorimotor cortex in neurosurgery by recording of somatosensory evoked potentials. Yale J Biol Med 1987, 60:143-150.
58. Allison T., McCarthy G., Wood C.C., et al. Human cortical potentials evoked by stimulation of the median nerve. I. Cytoarchitectonic areas generating short-latency activity. J Neurophysiol 1989, 62:694-710.
59. Desmedt J.E., Cheron G. Somatosensory evoked potentials in man: subcortical and cortical components and their neural basis. Ann N Y Acad Sci 1982, 388:388-411.
60. Firsching R., Klug N., Borner U., et al. Lesions of the sensorimotor region: somatosensory evoked potentials and ultrasound guided surgery. Acta Neurochir (Wien) 1992, 118:87-90.
61. Grundy B.L. Intraoperative monitoring of sensory-evoked potentials. Anesthesiology 1983, 58:72-87.
62. Wood C.C., Spencer D.D., Allison T., et al. Localization of human sensorimotor cortex during surgery by cortical surface recording of somatosensory evoked potentials. J Neurosurg 1988, 68:99-111.
63. Woolsey C.N., Erickson T.C., Gilson W.E. Localization in somatic sensory and motor areas of human cerebral cortex as determined by direct recording of evoked potentials and electrical stimulation. J Neurosurg 1979, 51:476-506.
64. Romstock J., Fahlbusch R., Ganslandt O., et al. Localisation of the sensorimotor cortex during surgery for brain tumours: feasibility and waveform patterns of somatosensory evoked potentials. J Neurol Neurosurg Psychiatry 2002, 72:221-229.
65. King R.B., Schell G.R. Cortical localization and monitoring during cerebral operations. J Neurosurg 1987, 67:210-219.
66. Miller K.J., denNijs M., Shenoy P., et al. Real-time functional brain mapping using electrocorticography. Neuroimage 2007, 37:504-507.
67. Darvas F., Scherer R., Ojemann J.G., et al. High gamma mapping using EEG. Neuroimage 2010, 49:930-938.
68. Duffau H., Lopes M., Arthuis F., et al. 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 2005, 76:845-851.
69. Ojemann G., Ojemann J., Lettich E., et al. Cortical language localization in left, dominant hemisphere. An electrical stimulation mapping investigation in 117 patients. J Neurosurg 1989, 71:316-326.
70. Merton P.A., Morton H.B. Stimulation of the cerebral cortex in the intact human subject. Nature 1980, 285:227.
71. Barker A.T., Jalinous R., Freeston I.L. Non-invasive magnetic stimulation of human motor cortex. Lancet 1985, 1:1106-1107.
72. 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, 69:581-588. [discussion: 8].
73. Forster M.T., Hattingen E., Senft C., et al. Navigated transcranial magnetic stimulation and functional magnetic resonance imaging: advanced adjuncts in preoperative planning for central region tumors. Neurosurgery 2011, 68:1317-1324. [discussion: 24-5].
74. Krings T., Buchbinder B.R., Butler W.E., et al. Stereotactic transcranial magnetic stimulation: correlation with direct electrical cortical stimulation. Neurosurgery 1997, 41:1319-1325. [discussion: 25-6].
75. Sack A.T., Linden D.E. Combining transcranial magnetic stimulation and functional imaging in cognitive brain research: possibilities and limitations. Brain Res Brain Res Rev 2003, 43:41-56.
76. Ogawa S., Lee T.M., Kay A.R., et al. Brain magnetic resonance imaging with contrast dependent on blood oxygenation. Proc Natl Acad Sci U S A 1990, 87:9868-9872.
77. Fox P.T., Raichle M.E. Focal physiological uncoupling of cerebral blood flow and oxidative metabolism during somatosensory stimulation in human subjects. Proc Natl Acad Sci U S A 1986, 83:1140-1144.
78. Heeger D.J., Huk A.C., Geisler W.S., et al. Spikes versus BOLD: what does neuroimaging tell us about neuronal activity?. Nat Neurosci 2000, 3:631-633.
79. Logothetis N.K., Pauls J., Augath M., et al. Neurophysiological investigation of the basis of the fMRI signal. Nature 2001, 412:150-157.
80. Yoo S.S., Talos I.F., Golby A.J., et al. Evaluating requirements for spatial resolution of fMRI for neurosurgical planning. Hum Brain Mapp 2004, 21:34-43.
81. Gati J.S., Menon R.S., Ugurbil K., et al. Experimental determination of the BOLD field strength dependence in vessels and tissue. Magn Reson Med 1997, 38:296-302.
82. Roux F.E., Boulanouar K., Ranjeva J.P., et al. Usefulness of motor functional MRI correlated to cortical mapping in rolandic low-grade astrocytomas. Acta Neurochir (Wien) 1999, 141:71-79.
83. Majos A., Tybor K., Stefanczyk L., et al. Cortical mapping by functional magnetic resonance imaging in patients with brain tumors. Eur Radiol 2005, 15:1148-1158.
84. Roux F.E., Boulanouar K., Ibarrola D., et al. Functional MRI and intraoperative brain mapping to evaluate brain plasticity in patients with brain tumours and hemiparesis. J Neurol Neurosurg Psychiatry 2000, 69:453-463.
85. Yousry T.A., Schmid U.D., Jassoy A.G., et al. Topography of the cortical motor hand area: prospective study with functional MR imaging and direct motor mapping at surgery. Radiology 1995, 195:23-29.
86. Roessler K., Donat M., Lanzenberger R., et al. Evaluation of preoperative high magnetic field motor functional MRI (3 Tesla) in glioma patients by navigated electrocortical stimulation and postoperative outcome. J Neurol Neurosurg Psychiatry 2005, 76:1152-1157.
87. Lee C.C., Ward H.A., Sharbrough F.W., et al. Assessment of functional MR imaging in neurosurgical planning. AJNR Am J Neuroradiol 1999, 20:1511-1519.
88. Petrella J.R., Shah L.M., Harris K.M., et al. Preoperative functional MR imaging localization of language and motor areas: effect on therapeutic decision making in patients with potentially resectable brain tumors. Radiology 2006, 240:793-802.
89. Schreckenberger M., Spetzger U., Sabri O., et al. Localisation of motor areas in brain tumour patients: a comparison of preoperative [18F]FDG-PET and intraoperative cortical electrostimulation. Eur J Nucl Med 2001, 28:1394-1403.
90. Vinas F.C., Zamorano L., Mueller R.A., et al. [15O]-water PET and intraoperative brain mapping: a comparison in the localization of eloquent cortex. Neurol Res 1997, 19:601-608.
91. Fried I., Nenov V.I., Ojemann S.G., et al. Functional MR and PET imaging of rolandic and visual cortices for neurosurgical planning. J Neurosurg 1995, 83:854-861.
92. Tai Y.F., Piccini P. Applications of positron emission tomography (PET) in neurology. J Neurol Neurosurg Psychiatry 2004, 75:669-676.
93. Alavi J.B., Alavi A., Chawluk J., et al. Positron emission tomography in patients with glioma. A predictor of prognosis. Cancer 1988, 62:1074-1078.
94. Pirotte B., Acerbi F., Lubansu A., et al. PET imaging in the surgical management of pediatric brain tumors. Childs Nerv Syst 2007, 23:739-751.
95. Gallen C.C., Schwartz B.J., Bucholz R.D., et al. Presurgical localization of functional cortex using magnetic source imaging. J Neurosurg 1995, 82:988-994.
96. Kamada K., Takeuchi F., Kuriki S., et al. Functional neurosurgical simulation with brain surface magnetic resonance images and magnetoencephalography. Neurosurgery 1993, 33:269-272. [discussion: 72-3].
97. Rezai A.R., Hund M., Kronberg E., et al. Introduction of magnetoencephalography to stereotactic techniques. Stereotact Funct Neurosurg 1995, 65:37-41.
98. Castillo E.M., Simos P.G., Wheless J.W., et al. Integrating sensory and motor mapping in a comprehensive MEG protocol: clinical validity and replicability. Neuroimage 2004, 21:973-983.
99. Rezai A.R., Hund M., Kronberg E., et al. The interactive use of magnetoencephalography in stereotactic image-guided neurosurgery. Neurosurgery 1996, 39:92-102.
100. McDonald J.D., Chong B.W., Lewine J.D., et al. Integration of preoperative and intraoperative functional brain mapping in a frameless stereotactic environment for lesions near eloquent cortex. Technical note. J Neurosurg 1999, 90:591-598.
101. Ganslandt O., Fahlbusch R., Nimsky C., et al. Functional neuronavigation with magnetoencephalography: outcome in 50 patients with lesions around the motor cortex. J Neurosurg 1999, 91:73-79.
102. Schulder M., Maldjian J.A., Liu W.C., et al. Functional image-guided surgery of intracranial tumors located in or near the sensorimotor cortex. J Neurosurg 1998, 89:412-418.
103. Moseley M.E., Cohen Y., Kucharczyk J., et al. Diffusion-weighted MR imaging of anisotropic water diffusion in cat central nervous system. Radiology 1990, 176:439-445.
104. Jellison B.J., Field A.S., Medow J., et al. Diffusion tensor imaging of cerebral white matter: a pictorial review of physics, fiber tract anatomy, and tumor imaging patterns. AJNR Am J Neuroradiol 2004, 25:356-369.
105. Berman J.I., Berger M.S., Mukherjee P., et al. Diffusion-tensor imaging-guided tracking of fibers of the pyramidal tract combined with intraoperative cortical stimulation mapping in patients with gliomas. J Neurosurg 2004, 101:66-72.
106. Kamada K., Houkin K., Takeuchi F., et al. Visualization of the eloquent motor system by integration of MEG, functional, and anisotropic diffusion-weighted MRI in functional neuronavigation. Surg Neurol 2003, 59:352-361. [discussion: 61-2].
107. Krings T., Topper R., Willmes K., et al. Activation in primary and secondary motor areas in patients with CNS neoplasms and weakness. Neurology 2002, 58:381-390.
108. Moller-Hartmann W., Krings T., Coenen V.A., et al. Preoperative assessment of motor cortex and pyramidal tracts in central cavernoma employing functional and diffusion-weighted magnetic resonance imaging. Surg Neurol 2002, 58:302-307. [discussion: 8].
109. Parmar H., Sitoh Y.Y., Yeo T.T. Combined magnetic resonance tractography and functional magnetic resonance imaging in evaluation of brain tumors involving the motor system. J Comput Assist Tomogr 2004, 28:551-556.
110. Witwer B.P., Moftakhar R., Hasan K.M., et al. Diffusion-tensor imaging of white matter tracts in patients with cerebral neoplasm. J Neurosurg 2002, 97:568-575.
111. Nimsky C., Ganslandt O., Fahlbusch R. Implementation of fiber tract navigation. Neurosurgery 2006, 58:ONS-292-ONS-303. [discussion: ONS-4].
112. Nimsky C., Ganslandt O., Merhof D., et al. Intraoperative visualization of the pyramidal tract by diffusion-tensor-imaging-based fiber tracking. Neuroimage 2006, 30:1219-1229.
113. Hunsche S., Moseley M.E., Stoeter P., et al. Diffusion-tensor MR imaging at 1.5 and 3.0 T: initial observations. Radiology 2001, 221:550-556.
114. Duffau H. Lessons from brain mapping in surgery for low-grade glioma: insights into associations between tumour and brain plasticity. Lancet Neurol 2005, 4:476-486.
115. Nabavi A., Black P.M., Gering D.T., et al. Serial intraoperative magnetic resonance imaging of brain shift. Neurosurgery 2001, 48:787-797. [discussion: 97-8].
116. Nimsky C., Ganslandt O., Cerny S., et al. Quantification of, visualization of, and compensation for brain shift using intraoperative magnetic resonance imaging. Neurosurgery 2000, 47:1070-1079. [discussion: 9-80].
117. Nimsky C., Ganslandt O., Hastreiter P., et al. Intraoperative compensation for brain shift. Surg Neurol 2001, 56:357-364. [discussion: 64-5].
118. Hata N., Nabavi A., Wells W.M., et al. Three-dimensional optical flow method for measurement of volumetric brain deformation from intraoperative MR images. J Comput Assist Tomogr 2000, 24:531-538.
119. Reinges M.H., Nguyen H.H., Krings T., et al. Course of brain shift during microsurgical resection of supratentorial cerebral lesions: limits of conventional neuronavigation. Acta Neurochir (Wien) 2004, 146:369-377. [discussion: 77].
120. Archip N., Clatz O., Whalen S., et al. Non-rigid alignment of pre-operative MRI, fMRI, and DT-MRI with intra-operative MRI for enhanced visualization and navigation in image-guided neurosurgery. Neuroimage 2007, 35:609-624.