Electrical stimulation of the dorsolateral prefrontal cortex impairs semantic cognition

Abstract

To identify the prefrontal cortical structures causally involved in verbal and nonverbal semantic cognition in both cerebral hemispheres. We retrospectively screened the intraoperative brain mapping data of 584 patients who underwent neurosurgery for neoplastic tumor under local anesthesia with direct cortical electrostimulation. Patients were included if they were right-handed, recently diagnosed with a diffuse low-grade glioma, and had a positive language mapping for verbal (naming task) and nonverbal (visual semantic association task) semantic cognition in the prefrontal cortex (n = 49). Among these, 30 were tested intraoperatively with both the naming and the semantic association tasks, while 19 were tested with the naming task only. Subsequently, each semantic site (n = 85) was plotted individually onto a common stereotaxic space for detailed analyses. The cortical sites associated with verbal semantic disturbances (n = 45) were distributed in the pars opercularis (n = 14) and pars triangularis (n = 19) of the left inferior frontal gyrus, and left dorsolateral prefrontal cortex (dlPFC, n = 12); only 2 sites were observed in the right dlPFC. In contrast, all but one cortical site associated with nonverbal semantic disturbances were observed in the left dorsolateral cortex (n = 8). In the right hemisphere, the same disturbances were found in the dlPFC (n = 14) and pars opercularis (n = 2). The present study demonstrated the critical role of the dlPFC in the semantic network, and indicated its specific and bilateral involvement in nonverbal semantic cognition in right-handers.