Abstract
Objectives: To describe cortical reorganisation and the effects of glioma infiltration on local brain function in three patients who underwent two operations 12–24 months apart.
Methods: Three patients who had no neurological deficit underwent two operations for low grade glioma, located in functionally important brain regions. During each operation, local brain function was characterised by electrical mapping and awake craniotomy.
Results: Language or sensorimotor areas had been invaded by the tumour at the time of the first operation, leading to incomplete glioma removal in all cases. Because of a tumour recurrence, the patients were reoperated on between 12 and 24 months later. Functional reorganisation of the language, sensory, and motor maps was detected by electrical stimulation of the brain, and this allowed total glioma removal without neurological sequelae.
Conclusions: These findings show that surgical resection of a glioma can lead to functional reorganisation in the peritumorous and infiltrated brain. It may be that this reorganisation is directly or indirectly caused by the surgical procedure. If this hypothesis is confirmed by other studies, the use of such brain plasticity potential could be used when planning surgical options in some patients with low grade glioma. Such a strategy could extend the limits of tumour resection in gliomas involving eloquent brain areas without causing permanent morbidity.
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Selected References
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- Binkofski F., Seitz R. J., Arnold S., Classen J., Benecke R., Freund H. J. Thalamic metbolism and corticospinal tract integrity determine motor recovery in stroke. Ann Neurol. 1996 Apr;39(4):460–470. doi: 10.1002/ana.410390408. [DOI] [PubMed] [Google Scholar]
- Brasil-Neto J. P., Cohen L. G., Pascual-Leone A., Jabir F. K., Wall R. T., Hallett M. Rapid reversible modulation of human motor outputs after transient deafferentation of the forearm: a study with transcranial magnetic stimulation. Neurology. 1992 Jul;42(7):1302–1306. doi: 10.1212/wnl.42.7.1302. [DOI] [PubMed] [Google Scholar]
- Byrne J. A., Calford M. B. Short-term expansion of receptive fields in rat primary somatosensory cortex after hindpaw digit denervation. Brain Res. 1991 Nov 29;565(2):218–224. doi: 10.1016/0006-8993(91)91652-h. [DOI] [PubMed] [Google Scholar]
- Chollet F., DiPiero V., Wise R. J., Brooks D. J., Dolan R. J., Frackowiak R. S. The functional anatomy of motor recovery after stroke in humans: a study with positron emission tomography. Ann Neurol. 1991 Jan;29(1):63–71. doi: 10.1002/ana.410290112. [DOI] [PubMed] [Google Scholar]
- Daumas-Duport C., Scheithauer B. W., Kelly P. J. A histologic and cytologic method for the spatial definition of gliomas. Mayo Clin Proc. 1987 Jun;62(6):435–449. doi: 10.1016/s0025-6196(12)65469-x. [DOI] [PubMed] [Google Scholar]
- Dinse H. R., Godde B., Hilger T., Haupt S. S., Spengler F., Zepka R. Short-term functional plasticity of cortical and thalamic sensory representations and its implication for information processing. Adv Neurol. 1997;73:159–178. [PubMed] [Google Scholar]
- Duffau H. Acute functional reorganisation of the human motor cortex during resection of central lesions: a study using intraoperative brain mapping. J Neurol Neurosurg Psychiatry. 2001 Apr;70(4):506–513. doi: 10.1136/jnnp.70.4.506. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Duffau H., Bauchet L., Lehéricy S., Capelle L. Functional compensation of the left dominant insula for language. Neuroreport. 2001 Jul 20;12(10):2159–2163. doi: 10.1097/00001756-200107200-00023. [DOI] [PubMed] [Google Scholar]
- Duffau H., Capelle L., Lopes M., Faillot T., Sichez J. P., Fohanno D. The insular lobe: physiopathological and surgical considerations. Neurosurgery. 2000 Oct;47(4):801–811. doi: 10.1097/00006123-200010000-00001. [DOI] [PubMed] [Google Scholar]
- Duffau H., Capelle L., Sichez J., Faillot T., Abdennour L., Law Koune J. D., Dadoun S., Bitar A., Arthuis F., Van Effenterre R. Intra-operative direct electrical stimulations of the central nervous system: the Salpêtrière experience with 60 patients. Acta Neurochir (Wien) 1999;141(11):1157–1167. doi: 10.1007/s007010050413. [DOI] [PubMed] [Google Scholar]
- Duffau H., Sichez J. P., Lehéricy S. Intraoperative unmasking of brain redundant motor sites during resection of a precentral angioma: evidence using direct cortical stimulation. Ann Neurol. 2000 Jan;47(1):132–135. [PubMed] [Google Scholar]
- Ebeling U., Schmid U. D., Ying H., Reulen H. J. Safe surgery of lesions near the motor cortex using intra-operative mapping techniques: a report on 50 patients. Acta Neurochir (Wien) 1992;119(1-4):23–28. doi: 10.1007/BF01541777. [DOI] [PubMed] [Google Scholar]
- Eysel U. T. Perilesional cortical dysfunction and reorganization. Adv Neurol. 1997;73:195–206. [PubMed] [Google Scholar]
- Fandino J., Kollias S. S., Wieser H. G., Valavanis A., Yonekawa Y. Intraoperative validation of functional magnetic resonance imaging and cortical reorganization patterns in patients with brain tumors involving the primary motor cortex. J Neurosurg. 1999 Aug;91(2):238–250. doi: 10.3171/jns.1999.91.2.0238. [DOI] [PubMed] [Google Scholar]
- Garraghty P. E., Kaas J. H. Large-scale functional reorganization in adult monkey cortex after peripheral nerve injury. Proc Natl Acad Sci U S A. 1991 Aug 15;88(16):6976–6980. doi: 10.1073/pnas.88.16.6976. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Grady M. S., Jane J. A., Steward O. Synaptic reorganization within the human central nervous system following injury. J Neurosurg. 1989 Oct;71(4):534–537. doi: 10.3171/jns.1989.71.4.0534. [DOI] [PubMed] [Google Scholar]
- Hagemann G., Redecker C., Neumann-Haefelin T., Freund H. J., Witte O. W. Increased long-term potentiation in the surround of experimentally induced focal cortical infarction. Ann Neurol. 1998 Aug;44(2):255–258. doi: 10.1002/ana.410440217. [DOI] [PubMed] [Google Scholar]
- Haglund M. M., Berger M. S., Shamseldin M., Lettich E., Ojemann G. A. Cortical localization of temporal lobe language sites in patients with gliomas. Neurosurgery. 1994 Apr;34(4):567–576. doi: 10.1227/00006123-199404000-00001. [DOI] [PubMed] [Google Scholar]
- Jacobs K. M., Donoghue J. P. Reshaping the cortical motor map by unmasking latent intracortical connections. Science. 1991 Feb 22;251(4996):944–947. doi: 10.1126/science.2000496. [DOI] [PubMed] [Google Scholar]
- Karbe H., Herholz K., Kessler J., Wienhard K., Pietrzyk U. E., Heiss W. D. Recovery of language after brain damage. Adv Neurol. 1997;73:347–358. [PubMed] [Google Scholar]
- Lewine J. D., Astur R. S., Davis L. E., Knight J. E., Maclin E. L., Orrison W. W., Jr Cortical organization in adulthood is modified by neonatal infarct: a case study. Radiology. 1994 Jan;190(1):93–96. doi: 10.1148/radiology.190.1.8259435. [DOI] [PubMed] [Google Scholar]
- Lüders H. O., Comair Y. G., Bleasel A. F., Holthausen H. Recovery of function following lesions of eloquent brain areas. Adv Neurol. 1997;73:335–346. [PubMed] [Google Scholar]
- Maldjian J., Atlas S. W., Howard R. S., 2nd, Greenstein E., Alsop D., Detre J. A., Listerud J., D'Esposito M., Flamm E. S. Functional magnetic resonance imaging of regional brain activity in patients with intracerebral arteriovenous malformations before surgical or endovascular therapy. J Neurosurg. 1996 Mar;84(3):477–483. doi: 10.3171/jns.1996.84.3.0477. [DOI] [PubMed] [Google Scholar]
- Merzenich M. M., Kaas J. H., Wall J., Nelson R. J., Sur M., Felleman D. Topographic reorganization of somatosensory cortical areas 3b and 1 in adult monkeys following restricted deafferentation. Neuroscience. 1983 Jan;8(1):33–55. doi: 10.1016/0306-4522(83)90024-6. [DOI] [PubMed] [Google Scholar]
- Mogilner A., Grossman J. A., Ribary U., Joliot M., Volkmann J., Rapaport D., Beasley R. W., Llinás R. R. Somatosensory cortical plasticity in adult humans revealed by magnetoencephalography. Proc Natl Acad Sci U S A. 1993 Apr 15;90(8):3593–3597. doi: 10.1073/pnas.90.8.3593. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Musso M., Weiller C., Kiebel S., Müller S. P., Bülau P., Rijntjes M. Training-induced brain plasticity in aphasia. Brain. 1999 Sep;122(Pt 9):1781–1790. doi: 10.1093/brain/122.9.1781. [DOI] [PubMed] [Google Scholar]
- Nudo R. J., Milliken G. W. Reorganization of movement representations in primary motor cortex following focal ischemic infarcts in adult squirrel monkeys. J Neurophysiol. 1996 May;75(5):2144–2149. doi: 10.1152/jn.1996.75.5.2144. [DOI] [PubMed] [Google Scholar]
- Ojemann G., Ojemann J., Lettich E., Berger M. Cortical language localization in left, dominant hemisphere. An electrical stimulation mapping investigation in 117 patients. J Neurosurg. 1989 Sep;71(3):316–326. doi: 10.3171/jns.1989.71.3.0316. [DOI] [PubMed] [Google Scholar]
- Ojemann J. G., Miller J. W., Silbergeld D. L. Preserved function in brain invaded by tumor. Neurosurgery. 1996 Aug;39(2):253–259. doi: 10.1097/00006123-199608000-00003. [DOI] [PubMed] [Google Scholar]
- Ojemann J. G., Silbergeld D. L. Cortical stimulation mapping of phantom limb rolandic cortex. Case report. J Neurosurg. 1995 Apr;82(4):641–644. doi: 10.3171/jns.1995.82.4.0641. [DOI] [PubMed] [Google Scholar]
- Pascual-Leone A., Tarazona F., Keenan J., Tormos J. M., Hamilton R., Catala M. D. Transcranial magnetic stimulation and neuroplasticity. Neuropsychologia. 1999 Feb;37(2):207–217. doi: 10.1016/s0028-3932(98)00095-5. [DOI] [PubMed] [Google Scholar]
- Rauschecker J. P. Mechanisms of compensatory plasticity in the cerebral cortex. Adv Neurol. 1997;73:137–146. [PubMed] [Google Scholar]
- Seitz R. J., Freund H. J. Plasticity of the human motor cortex. Adv Neurol. 1997;73:321–333. [PubMed] [Google Scholar]
- Seitz R. J., Huang Y., Knorr U., Tellmann L., Herzog H., Freund H. J. Large-scale plasticity of the human motor cortex. Neuroreport. 1995 Mar 27;6(5):742–744. doi: 10.1097/00001756-199503270-00009. [DOI] [PubMed] [Google Scholar]
- Skirboll S. S., Ojemann G. A., Berger M. S., Lettich E., Winn H. R. Functional cortex and subcortical white matter located within gliomas. Neurosurgery. 1996 Apr;38(4):678–685. [PubMed] [Google Scholar]
- Weder B., Seitz R. J. Deficient cerebral activation pattern in stroke recovery. Neuroreport. 1994 Jan 12;5(4):457–460. doi: 10.1097/00001756-199401120-00022. [DOI] [PubMed] [Google Scholar]
- Weiller C., Chollet F., Friston K. J., Wise R. J., Frackowiak R. S. Functional reorganization of the brain in recovery from striatocapsular infarction in man. Ann Neurol. 1992 May;31(5):463–472. doi: 10.1002/ana.410310502. [DOI] [PubMed] [Google Scholar]
- Witte O. W., Stoll G. Delayed and remote effects of focal cortical infarctions: secondary damage and reactive plasticity. Adv Neurol. 1997;73:207–227. [PubMed] [Google Scholar]
- Wunderlich G., Knorr U., Herzog H., Kiwit J. C., Freund H. J., Seitz R. J. Precentral glioma location determines the displacement of cortical hand representation. Neurosurgery. 1998 Jan;42(1):18–27. doi: 10.1097/00006123-199801000-00005. [DOI] [PubMed] [Google Scholar]
- Xerri C., Merzenich M. M., Peterson B. E., Jenkins W. Plasticity of primary somatosensory cortex paralleling sensorimotor skill recovery from stroke in adult monkeys. J Neurophysiol. 1998 Apr;79(4):2119–2148. doi: 10.1152/jn.1998.79.4.2119. [DOI] [PubMed] [Google Scholar]