Mapping the Functional Boundaries of the Speech Articulation Network Using Positive and Negative Direct Electrical Stimulation With Resting-State Functional MRI

Abstract

Background and objectives: Resting-state functional MRI (rs-fMRI) is a noninvasive tool for studying brain function, with growing applications in clinical oncology, such as preoperative planning and brain reorganization mapping. Direct electrical stimulation (DES) during awake surgery remains the gold standard for causally identifying functional brain regions. Although previous studies have mapped the speech articulation network (SAN) from rs-fMRI using DES-positive points, the inclusion of DES-negative points remains unexplored. This study integrates both positive and negative DES data to create a more comprehensive SAN atlas and refine its functional borders using presurgical functional connectivity from glioma patients.

Methods: We analyzed 25 glioma patients (16 high-grade, 9 low-grade) who underwent awake surgery with DES mapping for speech articulation. Seventy-four DES points (32 positive, 42 negative) were identified in gray matter. Presurgical rs-fMRI data were used for seed-based connectivity analysis, with DES-positive and DES-negative points analyzed separately. Group SAN-positive and SAN-negative networks were assessed for overlap across each other and with regions from an anatomical atlas. DES-negative and DES-positive points were used to estimate the sensitivity and specificity of the group SAN-positive network at different thresholds for group frequency.

Results: The DES-positive SAN was bilaterally located in the rolandic operculum, inferior frontal gyrus, and superior temporal gyrus, consistent with previous studies. DES-negative points revealed distinct connectivity patterns, with only partial overlap, helping to delineate the SAN's functional borders, particularly in the central sulcus (posterior and anterior) and inferior frontal gyrus (pars triangularis and opercularis). Anticorrelated networks from DES-positive points further differentiated the roles of positive and negative sites within the SAN. A 41% threshold in the SAN-positive gives approximately 80% specificity and sensitivity.

Conclusion: DES-positive points define the SAN robustly. DES-negative points served to establish a threshold for the group SAN atlas and a more detailed definition of the functional SAN borders.

Keywords: Brain mapping; Brain surgery; Direct electrical stimulation; Functional magnetic resonance imaging; Glioma; Presurgical planning; Resting state.