More widespread functionality of posterior language area in patients with brain tumors

Author:

Nakajima Riho1,Osada Takahiro2ORCID,Kinoshita Masashi3,Ogawa Akitoshi2ORCID,Okita Hirokazu4,Konishi Seiki2,Nakada Mitsutoshi35ORCID

Affiliation:

1. Department of Occupational Therapy, Faculty of Health Science, Institute of Medical, Pharmaceutical and Health Sciences Kanazawa University Kanazawa Japan

2. Department of Neurophysiology Juntendo University School of Medicine Tokyo Japan

3. Department of Neurosurgery, Faculty of Medicine, Institute of Medical, Pharmaceutical and Health Sciences Kanazawa University Kanazawa Japan

4. Department of Physical Medicine and Rehabilitation Kanazawa University Hospital Kanazawa Japan

5. Sapiens Life Sciences Evolution and Medicine Research Center Kanazawa University Kanazawa Japan

Abstract

AbstractDamage to the posterior language area (PLA), or Wernicke's area causes cortical reorganization in the corresponding regions of the contralateral hemisphere. However, the details of reorganization within the ipsilateral hemisphere are not fully understood. In this context, direct electrical stimulation during awake surgery can provide valuable opportunities to investigate neuromodulation of the human brain in vivo, which is difficult through the non‐invasive approaches. Thus, in this study, we aimed to investigate the characteristics of the cortical reorganization of the PLA within the ipsilateral hemisphere. Sixty‐two patients with left hemispheric gliomas were divided into groups depending on whether the lesion extended to the PLA. All patients underwent direct cortical stimulation with a picture‐naming task. We further performed functional connectivity analyses using resting‐state functional magnetic resonance imaging (MRI) in a subset of patients and calculated betweenness centrality, an index of the network importance of brain areas. During direct cortical stimulation, the regions showing positive (impaired) responses in the non‐PLA group were localized mainly in the posterior superior temporal gyrus (pSTG), whereas those in the PLA group were widely distributed from the pSTG to the posterior supramarginal gyrus (pSMG). Notably, the percentage of positive responses in the pSMG was significantly higher in the PLA group (47%) than in the non‐PLA group (8%). In network analyses of functional connectivity, the pSMG was identified as a hub region with high betweenness centrality in both the groups. These findings suggest that the language area can spread beyond the PLA to the pSMG, a hub region, in patients with lesion progression to the pSTG. The change in the pattern of the language area may be a compensatory mechanism to maintain efficient brain networks.

Funder

Japan Society for the Promotion of Science

Publisher

Wiley

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