Advertisement

Neurosurgical Review

, Volume 39, Issue 2, pp 241–249 | Cite as

Difference of language cortex reorganization between cerebral arteriovenous malformations, cavernous malformations, and gliomas: a functional MRI study

  • Xiaofeng Deng
  • Long Xu
  • Yan Zhang
  • Bo Wang
  • Shuo Wang
  • Yuanli Zhao
  • Yong Cao
  • Dong Zhang
  • Rong Wang
  • Xun Ye
  • Jun Wu
  • Jizong ZhaoEmail author
Original Article

Abstract

The authors attempted to demonstrate the difference in language cortex reorganization between cerebral malformations (AVMs), cavernous malformations (CMs), and gliomas by blood oxygen level-dependent (BOLD) functional magnetic resonance imaging. Clinical and imaging data of 27 AVM patients (AVM-L group), 29 CM patients (CM-L group), and 20 glioma patients (Glioma-L group) were retrospectively reviewed, with lesions overlying the left inferior frontal gyrus (Broca area). As a control, patients with lesions involving the right inferior frontal gyrus were also enrolled, including 14 AVM patients (AVM-R group), 20 CM patients (CM-R group), and 14 glioma patients (Glioma-R group). All patients were right-handed. Lateralization indices (LI) of BOLD signal activations were calculated separately for Broca and Wernicke areas. In AVM-L group, right-sided lateralization of BOLD signals was observed in 10 patients (37.0 %), including 6 in the Broca area alone, 1 in the Wernicke area alone, and 3 in both areas. Three patients (10.3 %) of CM-L group showed right-sided lateralization in both Broca and Wernicke areas, and 1 patient (5.0 %) of Glioma-L group had right-sided lateralization in the Wernicke area alone. A significant difference of right-sided lateralization was observed between the AVM-L group and CM-L group (P = 0.018) and also between the AVM-L group and Glioma-L group (P = 0.027). No patient in AVM-R, CM-R, or Glioma-R groups showed right-sided lateralization. Language cortex reorganization may occur in AVM, CM, and glioma patients when the traditional language cortex was involved by lesions, but the potential of reorganization for CM and glioma patients seems to be insufficient compared with AVM patients.

Keywords

Language cortex reorganization Arteriovenous malformation Cavernous malformation Glioma Functional MRI Aphasia 

Notes

Acknowledgments

This study is granted by the Ministry of Science and Technology of China grant (2012CB825505 and 2011BAI08B08), National Key Technology Research and Development Program of the Ministry of Science and Technology of China (2013BAI09B03), and Center of Stroke, Beijing Institute for Brain Disorders (BIBD-PXM2013_014226_07_000084).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

References

  1. 1.
    Choi JH, Mohr JP (2005) Brain arteriovenous malformations in adults. Lancet Neurol 4:299–308CrossRefPubMedGoogle Scholar
  2. 2.
    Mohr JP (2005) Brain arteriovenous malformations: children and adults. Stroke 36:2060–2061CrossRefPubMedGoogle Scholar
  3. 3.
    Jeon JS, Kim JE, Chung YS, Oh S, Ahn JH, Cho WS, Son YJ, Bang JS, Kang HS, Sohn CH, Oh CW (2014) A risk factor analysis of prospective symptomatic haemorrhage in adult patients with cerebral cavernous malformation. J Neurol Neurosurg Psychiatry 85:1366–1370CrossRefPubMedGoogle Scholar
  4. 4.
    Moultrie F, Horne MA, Josephson CB, Hall JM, Counsell CE, Bhattacharya JJ, Papanastassiou V, Sellar RJ, Warlow CP, Murray GD, Al-Shahi SR (2014) Outcome after surgical or conservative management of cerebral cavernous malformations. Neurology 83:582–589CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Alkadhi H, Kollias SS, Crelier GR, Golay X, Hepp-Reymond MC, Valavanis A (2000) Plasticity of the human motor cortex in patients with arteriovenous malformations: a functional MR imaging study. AJNR Am J Neuroradiol 21:1423–1433PubMedGoogle Scholar
  6. 6.
    Maestu F, Saldana C, Amo C, Gonzalez-Hidalgo M, Fernandez A, Fernandez S, Mata P, Papanicolaou A, Ortiz T (2004) Can small lesions induce language reorganization as large lesions do? Brain Lang 89:433–438CrossRefPubMedGoogle Scholar
  7. 7.
    Dronkers NF, Wilkins DP, Van Valin RD Jr, Redfern BB, Jaeger JJ (2004) Lesion analysis of the brain areas involved in language comprehension. Cognition 92:145–177CrossRefPubMedGoogle Scholar
  8. 8.
    Duffau H (2013) The huge plastic potential of adult brain and the role of connectomics: new insights provided by serial mappings in glioma surgery. Cortex 58:325–337CrossRefPubMedGoogle Scholar
  9. 9.
    Rosler J, Niraula B, Strack V, Zdunczyk A, Schilt S, Savolainen P, Lioumis P, Makela J, Vajkoczy P, Frey D, Picht T (2013) Language mapping in healthy volunteers and brain tumor patients with a novel navigated TMS system: evidence of tumor-induced plasticity. Clin Neurophysiol 125:526–536CrossRefPubMedGoogle Scholar
  10. 10.
    Fuller GN, Scheithauer BW (2007) The 2007 revised world health organization (WHO) classification of tumours of the central nervous system: newly codified entities. Brain Pathol 17:304–307CrossRefPubMedGoogle Scholar
  11. 11.
    Tan LH, Feng CM, Fox PT, Gao JH (2001) An fMRI study with written Chinese. Neuroreport 12:83–88CrossRefPubMedGoogle Scholar
  12. 12.
    Tan LH, Liu HL, Perfetti CA, Spinks JA, Fox PT, Gao JH (2001) The neural system underlying Chinese logograph reading. Neuroimage 13:836–846CrossRefPubMedGoogle Scholar
  13. 13.
    Rutten GJ, Ramsey NF, van Rijen PC, Alpherts WC, van Veelen CW (2002) FMRI-determined language lateralization in patients with unilateral or mixed language dominance according to the Wada test. Neuroimage 17:447–460CrossRefPubMedGoogle Scholar
  14. 14.
    Lee DJ, Pouratian N, Bookheimer SY, Martin NA (2010) Factors predicting language lateralization in patients with perisylvian vascular malformations. Clin Article J Neurosurg 113:723–730CrossRefGoogle Scholar
  15. 15.
    La Piana R, Klein D, Cortes M, Tampieri D (2009) Speech reorganization after an AVM bleed cured by embolization. A case report and review of the literature. Interv Neuroradiol 15:456–461PubMedPubMedCentralGoogle Scholar
  16. 16.
    Lehericy S, Biondi A, Sourour N, Vlaicu M, Du MST, Cohen L, Vivas E, Capelle L, Faillot T, Casasco A, Le BD, Marsault C (2002) Arteriovenous brain malformations: is functional MR imaging reliable for studying language reorganization in patients? Initial observations. Radiology 223:672–682CrossRefPubMedGoogle Scholar
  17. 17.
    Vikingstad EM, Cao Y, Thomas AJ, Johnson AF, Malik GM, Welch KM (2000) Language hemispheric dominance in patients with congenital lesions of eloquent brain. Neurosurgery 47:562–570PubMedGoogle Scholar
  18. 18.
    Winhuisen L, Thiel A, Schumacher B, Kessler J, Rudolf J, Haupt WF, Heiss WD (2005) Role of the contralateral inferior frontal gyrus in recovery of language function in poststroke aphasia: a combined repetitive transcranial magnetic stimulation and positron emission tomography study. Stroke 36:1759–1763CrossRefPubMedGoogle Scholar
  19. 19.
    Janszky J, Mertens M, Janszky I, Ebner A, Woermann FG (2006) Left-sided interictal epileptic activity induces shift of language lateralization in temporal lobe epilepsy: an fMRI study. Epilepsia 47:921–927CrossRefPubMedGoogle Scholar
  20. 20.
    Sanai N, Mirzadeh Z, Berger MS (2008) Functional outcome after language mapping for glioma resection. N Engl J Med 358:18–27CrossRefPubMedGoogle Scholar
  21. 21.
    Wang L, Chen D, Yang X, Olson JJ, Gopinath K, Fan T, Mao H (2013) Group independent component analysis and functional MRI examination of changes in language areas associated with brain tumors at different locations. PLoS One 8, e59657CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Ojemann G, Ojemann J, Lettich E, Berger M (2008) Cortical language localization in left, dominant hemisphere. An electrical stimulation mapping investigation in 117 patients. J Neurosurg 108:411–421CrossRefPubMedGoogle Scholar
  23. 23.
    Lee L, Sitoh YY, Ng I, Ng WH (2013) Cortical reorganization of motor functional areas in cerebral arteriovenous malformations. J Clin Neurosci 20:649–653CrossRefPubMedGoogle Scholar
  24. 24.
    Ulmer JL, Hacein-Bey L, Mathews VP, 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 55:569–579CrossRefPubMedGoogle Scholar
  25. 25.
    Cannestra AF, Pouratian N, Forage J, Bookheimer SY, Martin NA, Toga AW (2004) Functional magnetic resonance imaging and optical imaging for dominant-hemisphere perisylvian arteriovenous malformations. Neurosurgery 55:804–812CrossRefPubMedGoogle Scholar
  26. 26.
    Pouratian N, Bookheimer SY, Rex DE, Martin NA, Toga AW (2002) Utility of preoperative functional magnetic resonance imaging for identifying language cortices in patients with vascular malformations. J Neurosurg 97:21–32CrossRefPubMedGoogle Scholar
  27. 27.
    Gross BA, Du R (2013) Natural history of cerebral arteriovenous malformations: a meta-analysis. J Neurosurg 118:437–443CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Xiaofeng Deng
    • 1
    • 2
    • 3
    • 4
  • Long Xu
    • 1
    • 2
    • 3
    • 4
  • Yan Zhang
    • 1
    • 2
    • 3
    • 4
  • Bo Wang
    • 5
  • Shuo Wang
    • 1
    • 2
    • 3
    • 4
  • Yuanli Zhao
    • 1
    • 2
    • 3
    • 4
  • Yong Cao
    • 1
    • 2
    • 3
    • 4
  • Dong Zhang
    • 1
    • 2
    • 3
    • 4
  • Rong Wang
    • 1
    • 2
    • 3
    • 4
  • Xun Ye
    • 1
    • 2
    • 3
    • 4
  • Jun Wu
    • 1
    • 2
    • 3
    • 4
  • Jizong Zhao
    • 1
    • 2
    • 3
    • 4
    Email author
  1. 1.Department of Neurosurgery, Beijing Tiantan HospitalCapital Medical UniversityBeijingChina
  2. 2.China National Clinical Research Center for Neurological Diseases (NCRC-ND)BeijingChina
  3. 3.Center of StrokeBeijing Institute for Brain DisordersBeijingChina
  4. 4.Beijing Key Laboratory of Translational Medicine for Cerebrovascular DiseaseBeijingChina
  5. 5.State Key Laboratory of Brain and Cognitive Science, Beijing MRI Center for Brain Research, Institute of BiophysicsChinese Academy of SciencesBeijingChina

Personalised recommendations