Neural pathways subserving face-based mentalizing

Abstract

Over the past few years, considerable progress has been done in clarifying the neural networks underlying mentalizing. However, although the cortical architecture of this function is relatively well understood, the white matter pathways that may be involved in conveying neural signals within the mentalizing network remain to be elucidated. To gain insight into this matter, a detailed stimulation mapping of face-based mentalizing was performed in 27 patients undergoing awake surgery for a right-sided diffuse low-grade glioma (DLGG). Direct electrical stimulation (DES) was applied to both the cortical and subcortical levels. In perfect agreement with previous literature using face-based mentalizing tasks, cortical sites were identified in the posterior inferior frontal gyrus (IFG), the dorsolateral prefrontal cortex (dlPFC), and the posterior superior temporal gyrus (pSTG). Most importantly, critical sites were found along the inferior fronto-occipital fasciculus (IFOF), and within the white matter fibres supplying the dlPFC. Disconnectome analyses confirmed the very high probability of IFOF disconnection during temporal subcortical stimulation, and revealed an additional implication of the superior longitudinal fasciculus/arcuate fasciculus (SLF/AF) during prefrontal subcortical stimulations. Altogether, these findings suggest that functional integrity of both the IFOF and the SLF is required for accurately inferring complex mental states from human faces.

White Matter and Social Cognition

“…We found that more than half of the studies, particularly of the mirroring and mentalizing network, are based on clinical populations. They include major psychiatric and neurological disorders characterized by prominent social impairments, such as autism spectrum disorder (ASD) (Fishman, Datko, Cabrera, Carper, & Müller, 2015;Kana, Libero, Hu, Deshpande, & Colburn, 2014;Mueller et al, 2013), behavioral-variant frontotemporal dementia (Downey et al, 2015), and prosopagnosia (Gomez et al, 2015;Grossi et al, 2014;Song et al, 2015;Thomas et al, 2008Thomas et al, , 2009Valdés-Sosa et al, 2011), as well as those with secondary impairments in social cognition, such as schizophrenia (Fujino et al, 2014;Saito et al, 2017), amyotrophic lateral sclerosis (ALS) (Crespi et al, 2014(Crespi et al, , 2016, mild cognitive impairment (MCI) (Fujie et al, 2008), traumatic brain injury (Genova et al, 2015;Levin et al, 2011;Scheibel et al, 2011), Parkinson's disease (PD) (Baggio et al, 2012), brain lesion/stroke (Oishi et al, 2015;Philippi et al, 2009), velocardiofacial syndrome (Jalbrzikowski et al, 2014;Olszewski et al, 2017;Radoeva et al, 2012), multiple sclerosis (MS) (Mike et al, 2013) and diffuse low-grade glioma (Herbet et al, 2014;Herbet, Lafargue, Moritz-Gasser, Menjot de Champfleur, et al, 2015;Yordanova, Duffau, & Herbet, 2017). In terms of social cognitive measurements, the literature has employed several behavioral paradigms to probe each social function (see Table 1-3).…”

“…Benton tests, Philadelphia battery) (Gomez et al, 2015;Grossi et al, 2014;Thomas et al, 2008;Unger et al, 2016), and face memory tasks (e.g. Cambridge tests) (Gomez et al, 2015;Song et al, 2015;Unger et al, 2016); empathy was assessed by the "empathy quotient" (Chou et al, 2011;Herbet, Lafargue, Moritz-Gasser, Menjot de Champfleur, et al, 2015;Nakagawa et al, 2015;Takeuchi et al, 2013), the "interpersonal reactivity index" (Fujino et al, 2014;Parkinson & Wheatley, 2014), and the "trait emotional intelligence questionnaire" (empathy subsets) (Olszewski et al, 2017); mentalizing abilities were evaluated by "false belief" stories (Grosse Wiesmann et al, 2017), cartoon animations Scheibel et al, 2011), comic strip vignettes (Herbet et al, 2014;Kana et al, 2014), and the "reading the mind in the eyes" task (Anderson et al, 2015;Cabinio et al, 2015;Herbet et al, 2014;Mike et al, 2013;Yordanova et al, 2017). Such a wide variety of seemingly disparate disorders as well as diverse behavioral paradigms provide excellent opportunities for exploring the relationship between WM tracts and social functions.…”

“…Perhaps the most compelling evidence comes from two studies using direct electrical stimulation (DES) of WM tracts during neurosurgery-the only technique that allows for direct information on the functional role of WM tracts in cognition. Both studies found that virtual disconnection of the right AF or cingulum severely impairs the accuracy of mental state attribution Yordanova et al, 2017). This suggests that proper functioning of these tracts is essential for normal mentalizing abilities.…”

“…It is part of the limbic system and is broadly involved in attention, memory, and emotional processing (Catani & Thiebaut de Schotten, 2008). Given that the cingulum provides strong structural connections between the MPFC and PCC, it has been argued as the main structural skeleton of the default mode network (van den Heuvel, Mandl, Luigjes, & Hulshoff Pol, 2008) and the mentalizing network (Yordanova et al, 2017). The arcuate fasciculus (AF) has long been implicated in language processing, as it connects Wernicke's area to Broca's area in the left hemisphere; however, the function of the right AF remains unclear.…”

Limitations of functional neuroimaging for patient selection and surgical planning in glioma surgery

“…It is in the elucidation of these higher-order functions that functional neuroimaging is most likely to advance the neurosurgical management of glioma patients. Recent work suggests that rs-fMRI 61 and DTI, 62 in conjunction with DES, may be able to map the networks and tracts involved in mentalizing tasks. Mandonnet et al similarly used rs-fMRI and DTI pre-and postoperatively to illustrate that resection of a right temporoparietal glioma disrupted a large-scale network involved in cognitive flexibility.…”