Lesion-induced pseudo-dominance at functional magnetic resonance imaging: Implications for preoperative assessments

John L. Ulmer, Lotfi Hacein-Bey, Vincent Mathews, Wade M. Mueller, Edgar A. DeYoe, Robert W. Prost, Glenn A. Meyer, Hendrikus G. Krouwer, Kathleen M. Schmainda

Research output: Contribution to journalArticle

137 Citations (Scopus)

Abstract

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, post-operative and posttreatment deficits, and/or lesion-induced deficits. fMRI activation maps were generated with cross-correlation (P < 0.001) or f 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 contratateral 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.

Original languageEnglish
Pages (from-to)569-579
Number of pages11
JournalNeurosurgery
Volume55
Issue number3
DOIs
StatePublished - Sep 2004

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Magnetic Resonance Imaging
Arteriovenous Malformations
Prefrontal Cortex
Glioma
Brain
Encephalomalacia
Meningoencephalitis
Motor Cortex
Frontal Lobe
Encephalitis
Upper Extremity
Paralysis
Edema
Motor Activity
Language
Hemodynamics
Hemorrhage
Inflammation

Keywords

  • Blood oxygen level-dependent contrast
  • Cortical reorganization
  • Functional magnetic resonance imaging
  • Neurovascular coupling
  • Preoperative mapping

ASJC Scopus subject areas

  • Clinical Neurology
  • Surgery

Cite this

Lesion-induced pseudo-dominance at functional magnetic resonance imaging : Implications for preoperative assessments. / Ulmer, John L.; Hacein-Bey, Lotfi; Mathews, Vincent; Mueller, Wade M.; DeYoe, Edgar A.; Prost, Robert W.; Meyer, Glenn A.; Krouwer, Hendrikus G.; Schmainda, Kathleen M.

In: Neurosurgery, Vol. 55, No. 3, 09.2004, p. 569-579.

Research output: Contribution to journalArticle

Ulmer, JL, Hacein-Bey, L, Mathews, V, Mueller, WM, DeYoe, EA, Prost, RW, Meyer, GA, Krouwer, HG & Schmainda, KM 2004, 'Lesion-induced pseudo-dominance at functional magnetic resonance imaging: Implications for preoperative assessments', Neurosurgery, vol. 55, no. 3, pp. 569-579. https://doi.org/10.1227/01.NEU.0000134384.94749.B2
Ulmer, John L. ; Hacein-Bey, Lotfi ; Mathews, Vincent ; Mueller, Wade M. ; DeYoe, Edgar A. ; Prost, Robert W. ; Meyer, Glenn A. ; Krouwer, Hendrikus G. ; Schmainda, Kathleen M. / Lesion-induced pseudo-dominance at functional magnetic resonance imaging : Implications for preoperative assessments. In: Neurosurgery. 2004 ; Vol. 55, No. 3. pp. 569-579.
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T2 - Implications for preoperative assessments

AU - Ulmer, John L.

AU - Hacein-Bey, Lotfi

AU - Mathews, Vincent

AU - Mueller, Wade M.

AU - DeYoe, Edgar A.

AU - Prost, Robert W.

AU - Meyer, Glenn A.

AU - Krouwer, Hendrikus G.

AU - Schmainda, Kathleen M.

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N2 - 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, post-operative and posttreatment deficits, and/or lesion-induced deficits. fMRI activation maps were generated with cross-correlation (P < 0.001) or f 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 contratateral 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.

AB - 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, post-operative and posttreatment deficits, and/or lesion-induced deficits. fMRI activation maps were generated with cross-correlation (P < 0.001) or f 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 contratateral 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.

KW - Blood oxygen level-dependent contrast

KW - Cortical reorganization

KW - Functional magnetic resonance imaging

KW - Neurovascular coupling

KW - Preoperative mapping

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