Dissociating motor-speech from lexico-semantic systems in the left frontal lobe: insight from a series of 17 awake intraoperative mappings in glioma patients.

Functional brain mapping during awake surgery procedures is the gold standard technique in the management of left frontal lobe tumors. Nevertheless, a unified picture of the language subsystems encountered during left frontal lobe mapping is still lacking. We retrospectively analyzed the 49 cortical and the 33 axonal sites of functional language mapping performed in 17 patients operated for a left frontal lobe glioma under awake conditions. Sites were tagged on the postoperative MRI, based on anatomical landmarks and intraoperative photography. All MRIs and tags were then registered in the MNI template. Speech disturbances related to motor functions (speech arrest-with or without superior limb arrest-, stuttering, and vocalization) were grouped together as "motor-speech" responses. Anomias, semantic paraphasia, perseverations, and PPTT errors were classified as "lexico-semantic" responses. MNI-registered axonal sites were used as seed for computing disconnectome maps from a tractogram atlas of ten healthy individuals, as implemented in the BCB toolkit. The cortical distribution of lexico-semantic responses appeared to be located anteriorly (pars triangularis of the inferior frontal gyrus and posterior end of the middle and superior frontal gyrus) compared to motor-speech responses (lower end of the precentral gyrus and pars opercularis). Within the white matter, motor-speech responses and lexico-semantic responses overlapped on the trajectory of the aslant and fronto-striatal tracts, but the lexico-semantic sites were located more anteriorly (mean Y coordinate on the MNI system was 21.2 mm for lexico-semantic sites and 14.3 mm for the motor-speech sites; Wilcoxon test: W = 60.5, p = 0.03). Moreover, disconnectome maps evidenced a clear distinction between the two subsystems: posterior fronto-striatal and frontal aslant tracts, corpus callosum and cortico-spinal tract were related to the motor-speech sites, whereas anterior frontal aslant tract, inferior-fronto-occipital fasciculus (IFOF) and anterior thalamic radiations were related to the lexico-semantic sites. Hence, we evidenced distinct anatomical substrates for the motor-speech and lexico-semantic systems. Regarding the aslant/fronto-striatal system, an anterior to posterior gradient was found, with a lexico-semantic role for the anterior part and a motor-speech involvement for the posterior part. For tumors abutting the precentral sulcus, posterior boundaries of the resection are made of motor-speech sites, meaning that the anteriorly located lexico-semantic system is no more functional, as a result of network reorganization by plasticity.