Lesion-induced Pseudo-dominance at Functional Magnetic Resonance Imaging: Implications for Preoperative Assessments

OBJECTIVE:To illustrate how lesion-induced neurovascular uncoupling at functional magnetic resonance imaging (fMRI) can mimic hemispheric dominance opposite the side of a lesion preoperatively. METHODS:We retrospectively reviewed preoperative fMRI mapping data from 50 patients with focal brain abnormalities to establish patterns of hemispheric dominance of language, speech, visual, or motor system functions. Abnormalities included gliomas (31 patients), arteriovenous malformations (AVMs) (11 patients), other congenital lesions (4 patients), encephalomalacia (3 patients), and tumefactive encephalitis (1 patient). A laterality ratio of fMRI hemispheric dominance was compared with actual hemispheric dominance as verified by electrocortical stimulation, Wada testing, postoperative and posttreatment deficits, and/or lesion-induced deficits. fMRI activation maps were generated with cross-correlation (P < 0.001) or t test (P < 0.001) analysis. RESULTS:In 50 patients, a total of 85 functional areas were within 5 mm of the edge of a potentially resectable lesion. In 23 of these areas (27%), reduced fMRI signal in perilesional eloquent cortex in conjunction with preserved or increased signal in homologous contralateral brain areas revealed functional dominance opposite the side of the lesion. This suggested possible lesion-induced transhemispheric cortical reorganization to homologous brain regions (homotopic reorganization). In seven patients, however, the fMRI data were inconsistent with other methods of functional localization. In two patients with left inferior frontal gyrus gliomas and in one patient with focal tumefactive meningoencephalitis, fMRI incorrectly suggested strong right hemispheric speech dominance. In two patients with lateral precentral gyrus region gliomas and one patient with a left central sulcus AVM, the fMRI pattern incorrectly suggested primary corticobulbar motor dominance contralateral to the side of the lesion. In a patient with a right superior frontal gyrus AVM, fMRI revealed pronounced left dominant supplementary motor area activity in response to a bilateral complex motor task, but right superior frontal gyrus perilesional hemorrhage and edema subsequently caused left upper-extremity plegia. Pathophysiological factors that might have caused neurovascular uncoupling and facilitated pseudo-dominance at fMRI in these patients included direct tumor infiltration, neovascularity, cerebrovascular inflammation, and AVM-induced hemodynamic effects. Sixteen patients had proven (1 patient), probable (2 patients), or possible (13 patients) but unproven lesion-induced homotopic cortical reorganization. CONCLUSION:Lesion-induced neurovascular uncoupling causing reduced fMRI signal in perilesional eloquent cortex, in conjunction with normal or increased activity in homologous brain regions, may simulate hemispheric dominance and lesion-induced homotopic cortical reorganization.

[1]  J. Assheuer,et al.  Experimental transplantation gliomas in the adult cat brain , 1989, Acta Neurochirurgica.

[2]  W. Young,et al.  Displacement in Hypotensive Cortical Territories Adjacent to Arteriovenous Malformations , 1998 .

[3]  Wade M Mueller,et al.  Pseudo-reorganization of language cortical function at fMR imaging: a consequence of tumor-induced neurovascular uncoupling. , 2003, AJNR. American journal of neuroradiology.

[4]  Yue Cao,et al.  Pilot study of functional MRI to assess cerebral activation of motor function after poststroke hemiparesis. , 1998, Stroke.

[5]  W. Young,et al.  Characterization of arteriovenous malformation feeding vessels by carbon dioxide reactivity. , 1994, AJNR. American journal of neuroradiology.

[6]  Roland R. Lee,et al.  Temporal sequence of the ipsilateral and contralateral motor activities during voluntary finger movement revealed by MEG , 2001, NeuroImage.

[7]  V. Haughton,et al.  Supplementary motor area activation in patients with frontal lobe tumors and arteriovenous malformations. , 2003, AJNR. American journal of neuroradiology.

[8]  D. Le Bihan,et al.  Role of the supplementary motor area in motor deficit following medial frontal lobe surgery , 2001, Neurology.

[9]  S S Kollias,et al.  Intraoperative validation of functional magnetic resonance imaging and cortical reorganization patterns in patients with brain tumors involving the primary motor cortex. , 1999, Journal of neurosurgery.

[10]  W. Young,et al.  The effect of arteriovenous malformations on the distribution of intracerebral arterial pressures. , 1996, AJNR. American journal of neuroradiology.

[11]  J. Donoghue,et al.  Rapid reorganization of adult rat motor cortex somatic representation patterns after motor nerve injury. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[12]  Characterization of the tumor invasion area in the rat intracerebral glioma , 1996, Journal of Neuro-Oncology.

[13]  Claudio Babiloni,et al.  Hemispherical Asymmetry in Human SMA During Voluntary Simple Unilateral Movements. An fMRI Study , 2003, Cortex.

[14]  R. Turner,et al.  Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[15]  H. Freund,et al.  Role of the premotor cortex in recovery from middle cerebral artery infarction. , 1998, Archives of neurology.

[16]  B. Rosen,et al.  Functional mapping of the human visual cortex by magnetic resonance imaging. , 1991, Science.

[17]  R. Khanna The use of acetazolamide-enhanced regional cerebral blood flow measurement to predict risk to arteriovenous malformation patients. , 1993, Neurosurgery.

[18]  J. Lurito,et al.  Temporal lobe activation demonstrates sex-based differences during passive listening. , 2001, Radiology.

[19]  W. Young,et al.  Pressure autoregulation is intact after arteriovenous malformation resection. , 1993, Neurosurgery.

[20]  Shevelev Ia Functional brain mapping , 1987 .

[21]  Stéphane Lehéricy,et al.  Arteriovenous brain malformations: is functional MR imaging reliable for studying language reorganization in patients? Initial observations. , 2002, Radiology.

[22]  A. Grinvald,et al.  Interactions Between Electrical Activity and Cortical Microcirculation Revealed by Imaging Spectroscopy: Implications for Functional Brain Mapping , 1996, Science.

[23]  Mark J. Lowe,et al.  Quantitative Comparison of Functional Contrast from BOLD-Weighted Spin-Echo and Gradient-Echo Echoplanar Imaging at 1.5 Tesla and H215O PET in the Whole Brain , 2000, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[24]  O B Paulson,et al.  Does the release of potassium from astrocyte endfeet regulate cerebral blood flow? , 1987, Science.

[25]  T Morioka,et al.  Increased activity of the ipsilateral motor cortex during a hand motor task in patients with brain tumor and paresis. , 1997, AJNR. American journal of neuroradiology.

[26]  M. S. Lee,et al.  The role of functional MR imaging in patients with ischemia in the visual cortex. , 2001, AJNR. American journal of neuroradiology.

[27]  J Listerud,et al.  Functional magnetic resonance imaging of regional brain activity in patients with intracerebral arteriovenous malformations before surgical or endovascular therapy. , 1996, Journal of neurosurgery.

[28]  M. Jüptner,et al.  Reorganization of sensory and motor systems in hemiplegic stroke patients. A positron emission tomography study. , 1999, Stroke.

[29]  M. Moskowitz,et al.  Chronic Trigeminal Ganglionectomy or Topical Capsaicin Application to Pial Vessels Attenuates Postocclusive Cortical Hyperemia but Does Not Influence Postischemic Hypoperfusion , 1991, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[30]  E. DeYoe,et al.  Mapping striate and extrastriate visual areas in human cerebral cortex. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[31]  J. Tew,et al.  The relationship between the capillary structure and hemorrhage in gliomas. , 1987, Journal of neurosurgery.

[32]  W. Young,et al.  Intra-arterial nitrovasodilators do not increase cerebral blood flow in angiographically normal territories of arteriovenous malformation patients. , 1997, Stroke.

[33]  R. V. Van Heertum,et al.  Adaptive changes of autoregulation in chronic cerebral hypotension with arteriovenous malformations: an acetazolamide-enhanced single-photon emission CT study. , 1995, AJNR. American journal of neuroradiology.

[34]  J A Maldjian,et al.  The effect of brain tumors on BOLD functional MR imaging activation in the adjacent motor cortex: implications for image-guided neurosurgery. , 2000, AJNR. American journal of neuroradiology.

[35]  J G Ojemann,et al.  Preserved function in brain invaded by tumor. , 1996, Neurosurgery.

[36]  J Hennig,et al.  The influence of gliomas and nonglial space-occupying lesions on blood-oxygen-level-dependent contrast enhancement. , 2000, AJNR. American journal of neuroradiology.

[37]  Yue Cao,et al.  Language Hemispheric Dominance in Patients with Congenital Lesions of Eloquent Brain , 2000, Neurosurgery.

[38]  A Villringer,et al.  Coupling of brain activity and cerebral blood flow: basis of functional neuroimaging. , 1995, Cerebrovascular and brain metabolism reviews.

[39]  K. Hossmann,et al.  Experimental transplantation gliomas in the adult cat brain , 2005, Acta Neurochirurgica.

[40]  I. Whittle,et al.  Nitric oxide synthase is expressed in experimental malignant glioma and influences tumour blood flow , 2005, Acta Neurochirurgica.

[41]  W. Young,et al.  Evidence for adaptive autoregulatory displacement in hypotensive cortical territories adjacent to arteriovenous malformations. Columbia University AVM Study Project. , 1994, Neurosurgery.

[42]  D. Weinberger,et al.  Organization of the human motor system as studied by functional magnetic resonance imaging. , 1999, European journal of radiology.

[43]  G A Ojemann,et al.  Functional cortex and subcortical white matter located within gliomas. , 1996, Neurosurgery.

[44]  Alan C. Evans,et al.  Metabolic and hemodynamic evaluation of gliomas using positron emission tomography. , 1987, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

[45]  D E Sakas,et al.  The role of neuroeffector mechanisms in cerebral hyperperfusion syndromes. , 1991, Journal of neurosurgery.

[46]  K. Hossmann,et al.  Bioluminescence and fluoroscopic imaging of tissue pH and metabolites in experimental brain tumors of cat , 1992, NMR in biomedicine.

[47]  Charles B. Wilson,et al.  Magnetic Source Imaging Demonstrates Altered Cortical Distribution of Function in Patients with Arteriovenous Malformations , 2002, Neurosurgery.

[48]  J Pile-Spellman,et al.  'Steal' is an unestablished mechanism for the clinical presentation of cerebral arteriovenous malformations. , 1995, Stroke.

[49]  M. Aoyagi,et al.  Invasion of experimental rat brain tumor: early morphological changes following microinjection of C6 glioma cells , 2004, Acta Neuropathologica.

[50]  E. DeYoe,et al.  Visual Object Agnosia and Pure Word Alexia: Correlation of Functional Magnetic Resonance Imaging and Lesion Localization , 2004, Journal of computer assisted tomography.

[51]  I. Berry,et al.  Methodological and Technical Issues for Integrating Functional Magnetic Resonance Imaging Data in a Neuronavigational System , 2001, Neurosurgery.

[52]  Wilhelm Eisner,et al.  Surgical Resection of Grade II Astrocytomas in the Superior Frontal Gyrus , 2002, Neurosurgery.

[53]  V. Haughton,et al.  Functional MR of frontal lobe activation: comparison with Wada language results. , 1998, AJNR. American journal of neuroradiology.