Neuropsychological evidence for the crucial role of the right arcuate fasciculus in the face-based mentalizing network: A disconnection analysis

Recent evidence from axonal stimulation mapping studies suggests that at least two white matter connectivities in the right hemisphere may be involved in face-based mentalizing, i.e. the ability to infer complex cognitive and affective states from human faces: the inferior fronto-occipital (IFOF) and the superior longitudinal/arcuate (SLF/AF) fasciculi. However, to date, only a handful of neuropsychological studies have focused on the white matter tracts subserving mentalizing in general, and face-based mentalizing in particular. Therefore, the main goal of this study was to confirm the abovementioned results by applying voxelwise and tractwise lesion-symptom analyses to a set of behavioral data obtained from a large and homogeneous group of neurological participants. More precisely, 122 patients operated on for diffuse low-grade glioma were assessed postoperatively with the well-validated “Reading the Mind in the Eyes” (RME) test. For each patient, the resection cavity and the residual tumor infiltration were mapped separately on the respective postoperative structural MRI. Behavioral data, previously controlled for sociodemographic factors, were then submitted to a standard voxel-based and to a less conservative, region-of-interest (ROI)-based, lesion-deficit analyses. Results were invariably the same: no anatomo-functional relationships were pinpointed by these investigations, making thus impossible the cortical topological localization of mentalizing deficits. In a second time, two kinds of tractwise lesion-symptom analyses based on the damaged volume and the disconnection probabilities of the white matter tracts, were performed. All results were corrected with the Bonferroni correction. Converging and strong evidence was found that resection-related disconnection of the right AF is especially deleterious for face-based mentalizing. More anecdotally, we identified the involvement of certain ventral tracts, especially the IFOF and the uncinate fasciculus (UF). Taken as a whole, the reported findings confirm the critical role of the right AF in mentalizing abilities. From a more clinical standpoint, they highlight the necessity to perform an intraoperative map of this connectivity during awake surgery in order to avoid long-lasting social cognition disorders.