Broader functionality of language areas at the left middle frontal gyrus in patients with Broca's area tumors

The frontal language area (FLA; left posterior inferior frontal gyrus [pIFG] or Broca's area), critical for language processing can reorganize in response to lesion progression. While reorganization in the contralateral hemisphere is well known, how reorganization occurs within the ipsilateral hemisphere, especially in the perilesional region, remains unclear. Direct electrical stimulation (DES) during awake surgery enables identification of causal relationships between brain regions and language functions with high spatial resolution. In this study, we investigated cortical reorganization within the ipsilateral hemisphere of the FLA. Seventy-two patients with left hemisphere gliomas were studied. Patients were divided into FLA and non-FLA groups based on whether lesions included the pIFG (n = 10 and n = 62, respectively). All patients underwent DES during a picture-naming task, as recommended by awake surgery guidelines. A subset also underwent resting-state functional MRI (rsfMRI) before surgery to calculate betweenness centrality, an index of network importance of brain areas. DES revealed that the pIFG exhibited positive (impaired) responses to the picture-naming task in both groups. Notably, the frequency of positive responses in the middle frontal gyrus (MFG) was significantly higher in the FLA group than in the non-FLA group. RsfMRI-based network analyses revealed that two areas in the MFG, one in the anterior part and the other in the posterior part, showed higher centrality than surrounding frontal areas in both groups, especially the posterior one. These results suggest that language areas can be observed in the perilesional MFG regions following tumor progression, and raise the possibility that network hubs contribute to maintaining cognitive functions after brain lesions.