Neural Networks Mediating High-Level Mentalizing in Patients With Right Cerebral Hemispheric Gliomas

Abstract

Mentalizing is the ability to understand others’ mental state through external cues. It consists of two networks, namely low-level and high-level metalizing. Although it is an essential function in our daily social life, surgical resection of right cerebral hemisphere disturbs mentalizing processing with high possibility. In the past, little was known about the white matter related to high-level mentalizing, and the conservation of high-level mentalizing during surgery has not been a focus of attention. Therefore, the main purpose of this study was to examine the neural networks underlying high-level mentalizing and then, secondarily, investigate the usefulness of awake surgery in preserving the mentalizing network. A total of 20 patients with glioma localized in the right hemisphere who underwent awake surgery participated in this study. All patients were assigned to two groups: with or without intraoperative assessment of high-level mentalizing. Their high-level mentalizing abilities were assessed before surgery and 1 week and 3 months after surgery. At 3 months after surgery, only patients who received the intraoperative high-level mentalizing test showed the same score as normal healthy volunteers. The tract-based lesion symptom analysis was performed to confirm the severity of damage of associated fibers and high-level mentalizing accuracy. This analysis revealed the superior longitudinal fascicles (SLF) III and fronto-striatal tract (FST) to be associated with high-level mentalizing processing. Moreover, the voxel-based lesion symptom analysis demonstrated that resection of orbito-frontal cortex (OFC) causes persistent mentalizing dysfunction. Our study indicates that damage of the OFC and structural connectivity of the SLF and FST causes the disorder of mentalizing after surgery, and assessing high-level mentalizing during surgery may be useful to preserve these pathways.

Alterations of white matter integrity associated with cognitive deficits in patients with glioma

“…Nakajima et al. demonstrated that high‐level mentalizing processing was associated with structural connectivity networks, which were influenced by the effect of right cerebral hemispheric glioma and its resection (Nakajima et al., 2018). Zhou et al.…”

Theory of mind and decision science: Towards a typology of tasks and computational models

“…This emphasizes that the functional ToM network is built on structural connectivity and can be disrupted by severing significant white matter connections. These results for high-level mentalizing were later confirmed in additional glioma patients, which also highlighted the superior longitudinal fasciculus and the fronto-striatal tract, whereas lower-level and face-based mentalizing was also associated with the OFC and the uncinate fasciculus (Nakajima et al, 2018a(Nakajima et al, , 2018b. Furthermore, a recent functional connectivity study (Fishman et al, 2014) found that in contrast to commonly held beliefs, persons with AS compared to NT controls exhibit increased and not decreased connectivity between the mentalizing and the simulation networks, giving rise to the intriguing hypothesis that persons with AS may suffer from overconnectivity and -as a result -a diminished functional segregation between these two networks.…”

Preserving Right Pre-motor and Posterior Prefrontal Cortices Contribute to Maintaining Overall Basic Emotion

“…First, as mentioned in the preceding section, we cannot validate the usefulness of intraoperative monitoring of basic emotion compared to the control group. Although several previous reports have revealed the utility of intraoperative monitoring for right cerebral hemispheric function including emotional function, assessment of right frontal lobe function is still a challenge (Thiebaut de Schotten et al, 2005 ; Herbet et al, 2015 , 2016 ; Kinoshita et al, 2016 ; Nakajima et al, 2018 ). The usefulness of intraoperative monitoring of neuropsychological function should be considered from various aspects, such as the extent of resection, progression-free survival, overall survival, functional outcome, and postoperative social lives of patients.…”

“…Our patient’s group includes both low-grade and high-grade gliomas, although they are not biologically the same. However, several recent studies that investigated functional localization via awake brain mapping include both tumor types and obtain meaningful results (Gras-Combe et al, 2012 ; Saito et al, 2016 ; Nakajima et al, 2018 ; Puglisi et al, 2018 ; Rolland et al, 2018 ; Nakada et al, 2020 ). Additionally, we could not study the white matter tract, since we found only a few positive mapping sites at the subcortical level in our patient group.…”