Abstract

Background: The simplistic approaches to language circuits are continuously challenged by new findings in brain structure and connectivity. The posterior middle frontal gyrus and area 55b (pFMG/area55b), in particular, has gained a renewed interest in the overall language network.Methods: This is a retrospective single-center cohort study of patients who have undergone awake craniotomy for tumor resection. Navigated transcranial magnetic simulation (nTMS), tractography, and intraoperative findings were correlated with language outcomes.Results: Sixty-five awake craniotomies were performed between 2012 and 2020, and 24 patients were included. nTMS elicited 42 positive responses, 76.2% in the inferior frontal gyrus (IFG), and hesitation was the most common error (71.4%). In the pMFG/area55b, there were seven positive errors (five hesitations and two phonemic errors). This area had the highest positive predictive value (43.0%), negative predictive value (98.3%), sensitivity (50.0%), and specificity (99.0%) among all the frontal gyri. Intraoperatively, there were 33 cortical positive responses—two (6.0%) in the superior frontal gyrus (SFG), 15 (45.5%) in the MFG, and 16 (48.5%) in the IFG. A total of 29 subcortical positive responses were elicited−21 in the deep IFG–MFG gyri and eight in the deep SFG–MFG gyri. The most common errors identified were speech arrest at the cortical level (20 responses−13 in the IFG and seven in the MFG) and anomia at the subcortical level (nine patients—eight in the deep IFG–MFG and one in the deep MFG–SFG). Moreover, 83.3% of patients had a transitory deterioration of language after surgery, mainly in the expressive component (p = 0.03). An increased number of gyri with intraoperative positive responses were related with better preoperative (p = 0.037) and worse postoperative (p = 0.029) outcomes. The involvement of the SFG–MFG subcortical area was related with worse language outcomes (p = 0.037). Positive nTMS mapping in the IFG was associated with a better preoperative language outcome (p = 0.017), relating to a better performance in the expressive component, while positive mapping in the MFG was related to a worse preoperative receptive component of language (p = 0.031).Conclusion: This case series suggests that the posterior middle frontal gyrus, including area 55b, is an important integration cortical hub for both dorsal and ventral streams of language.

Highlights

  • Previous models of parcellation of the cerebral cortex have been proposed based on cytoarchitectonic [1, 2], myeloarchitectonic [3, 4], or functional characteristics of the different cerebral cortical areas [5, 6].More recently, a new mapping of the human cortex has been described, using a multi-modal gradient-based parcellation approach [7]

  • High-grade gliomas were prevalent in this series [71% World Health Organization (WHO) grade III and IV]

  • Previous studies have implicated the role of posterior middle frontal gyrus (MFG) and area 55b in language [7, 9, 10]

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Summary

Introduction

Previous models of parcellation of the cerebral cortex have been proposed based on cytoarchitectonic [1, 2], myeloarchitectonic [3, 4], or functional characteristics of the different cerebral cortical areas [5, 6].More recently, a new mapping of the human cortex has been described, using a multi-modal gradient-based parcellation approach [7]. Previous models of parcellation of the cerebral cortex have been proposed based on cytoarchitectonic [1, 2], myeloarchitectonic [3, 4], or functional characteristics of the different cerebral cortical areas [5, 6]. It has been described to be involved in various language production tasks and fluency of speech [7, 9, 10]. These findings are responsible for the renewed interest in the contribution of the posterior MFG to the overall language network. The posterior middle frontal gyrus and area 55b (pFMG/area55b), in particular, has gained a renewed interest in the overall language network

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