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

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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.

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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).

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    Authors and Affiliations

    1. Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing, 100050, China

      Xiaofeng Deng, Long Xu, Yan Zhang, Shuo Wang, Yuanli Zhao, Yong Cao, Dong Zhang, Rong Wang, Xun Ye, Jun Wu & Jizong Zhao

    2. China National Clinical Research Center for Neurological Diseases (NCRC-ND), Beijing, China

      Xiaofeng Deng, Long Xu, Yan Zhang, Shuo Wang, Yuanli Zhao, Yong Cao, Dong Zhang, Rong Wang, Xun Ye, Jun Wu & Jizong Zhao

    3. Center of Stroke, Beijing Institute for Brain Disorders, Beijing, China

      Xiaofeng Deng, Long Xu, Yan Zhang, Shuo Wang, Yuanli Zhao, Yong Cao, Dong Zhang, Rong Wang, Xun Ye, Jun Wu & Jizong Zhao

    4. Beijing Key Laboratory of Translational Medicine for Cerebrovascular Disease, Beijing, China

      Xiaofeng Deng, Long Xu, Yan Zhang, Shuo Wang, Yuanli Zhao, Yong Cao, Dong Zhang, Rong Wang, Xun Ye, Jun Wu & Jizong Zhao

    5. State Key Laboratory of Brain and Cognitive Science, Beijing MRI Center for Brain Research, Institute of Biophysics, Chinese Academy of Sciences, Beijing, China

      Bo Wang

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    1. Xiaofeng Deng
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    2. Long Xu
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    Peter Willems, Leiden, The Netherlands

    The authors describe an interesting retrospective fMRI analysis of surgical cases harboring an arteriovenous malformation (AVM), a cavernous malformation (CM), or a glioma in or near the Broca area (assumed to reside in the left hemisphere) or its homology in the contralateral hemisphere. They conclude that AVMs more frequently cause language area reorganization than CMs or gliomas, while they produce aphasia less frequently. One would expect functional cerebral reorganization to occur when two conditions are met: the brain tissue responsible for a specific function should be sufficiently disturbed and sufficient neuroplasticity should be present to allow that function to relocate. The first condition is likely influenced by lesion size and should definitely be regarded as fulfilled if functional impairment occurs (in this case aphasia). The second condition is likely influenced by patient age at the time of lesion growth and by the lesion growth rate. Thus, if a lesion develops early and slowly, no aphasia should occur due to relocation of function. This is in close agreement with the findings for AVMs. On the other hand, if a lesion develops late and fast, aphasia may occur but will not lead to relocation of function, as the results show for gliomas. The CM results are more difficult to categorize. There were some cases with aphasia, but also some cases with relocation of language function. Perhaps some of these lesions may lead to reorganization because they do disturb the language area at a sufficiently young age, while others just remain too small or take too long to reach the size that will induce aphasia.

    Xiaofeng Deng and Long Xu contributed equally to this work.

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    Deng, X., Xu, L., Zhang, Y. et al. Difference of language cortex reorganization between cerebral arteriovenous malformations, cavernous malformations, and gliomas: a functional MRI study. Neurosurg Rev 39, 241–249 (2016). https://doi.org/10.1007/s10143-015-0682-7

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