The role of the default mode network in longitudinal functional brain reorganization of brain gliomas

Abstract

The study of patients after glioma resection offers a unique opportunity to investigate brain reorganization. It is currently unknown how the whole-brain connectomic profile evolves longitudinally after surgical resection of a glioma and how this may be associated with tumor characteristics and cognitive outcome. In this longitudinal study, we investigate the impact of tumor lateralization and grade on functional connectivity (FC) in highly connected networks, or hubs, and cognitive performance. Twenty-eight patients (17 high-grade, 11 low-grade gliomas) underwent longitudinal pre/post-surgery resting-state fMRI scans and neuropsychological assessments (73 total measures). FC matrices were constructed considering as functional hubs the default mode (DMN) and fronto-parietal networks. No-hubs included primary sensory functional networks and any other no-hubs nodes. Both tumor hemisphere and grade affected brain reorganization post-resection. In right-hemisphere tumor patients, regardless of grade and relative to left-hemisphere gliomas, FC increased longitudinally after the intervention, both in terms of FC within hubs (phubs = 0.0004) and FC between hubs and no-hubs (phubs-no-hubs = 0.005). Regardless of tumor side, only lower-grade gliomas showed longitudinal FC increases relative to high-grade tumors within a precise hub network, the DMN. The neurocognitive profile was longitudinally associated with spatial features of the connectome, mainly within the DMN. We provide evidence that clinical glioma features, such as lateralization and grade, affect post-surgical longitudinal functional reorganization and cognitive recovery. The data suggest a possible role of the DMN in supporting cognition, providing useful information for prognostic prediction and surgical planning.

Segregated circuits for phonemic and semantic fluency: A novel patient-tailored disconnection study

“…Our analysis of the relationship between cortical lesions and impairment in verbal fluency one week after surgery confirmed the involvement of the left superior frontal gyrus in phonemic fluency and of the left superior temporal gyrus in semantic fluency, in accordance with previous results that identified a cortical dissociation ( Baldo et al, 2006 , Billingsley et al, 2004 , Henry and Crawford, 2004 , Hirshorn and Thompson-Schill, 2006 , Schmidt et al, 2019 ). Interestingly, in the FU assessment no negative relationships were found between cortical lesions and fluencies: this result reinforces the idea of a functional reorganization, thanks to the cortical plasticity, that may occur after glioma resection, in particular for motor function and language ( Cirillo et al, 2019 , Conway et al, 2017 , Duffau, 2020 , Duffau, 2021 , Duffau, 2020 , Duffau, 2014 , Duffau et al, 2003 , Saviola et al, 2022 ). Indeed, cortical areas nearby the tumor may have plastically reorganized their functions, in order to compensate the brain lesion ( Duffau, 2020 , Duffau, 2021 , Duffau, 2014 , Duffau et al, 2003 ).…”

Segregated Circuits for Phonemic and Semantic Fluency: A Novel Patient-Tailored Disconnection Study

“…Our analysis of the relationship between cortical lesions and impairment in verbal fluency one week after surgery confirmed the involvement of the left superior frontal gyrus in phonemic fluency and of the left superior temporal gyrus in semantic fluency, in accordance with previous results that identified a cortical dissociation (Baldo et al, 2006;Billingsley et al, 2004;Henry and Crawford, 2004;Hirshorn and Thompson-Schill, 2006;Schmidt et al, 2019). Interestingly, in the FU assessment no negative relationships were found between cortical lesions and fluencies: this result reinforces the idea of a functional reorganization, thanks to the cortical plasticity, that may occur after glioma resection, in particular for motor function and language (Cirillo et al, 2019;Conway et al, 2017;Duffau, 2021;Duffau, 2020;Duffau, 2014;Duffau et al, 2003;Saviola et al, 2022). Indeed, cortical areas nearby the tumor may have plastically reorganized their functions, in order to compensate the brain lesion (Duffau, 2021;Duffau, 2014;Duffau et al, 2003).…”

Surgical techniques and function outcome for cingulate gyrus glioma, how we do it

“…Recently, PCC was regarded as the hub of the default mode network (DMN), participating in the initial deactivated function and in engaging in spontaneous cognition ( 25 ). A recent imaging study on brain glioma showed that neurological profiles, including verbal fluency, verbal memory, and visual memory, are longitudinally associated with spatial features of the connectome, which is mainly within the DMN ( 26 ). Another study found that the surgical tissue changes of brain glioma, such as resection cavities or edema, have strong negative impacts on DMN nodes that result in bad performance in language processing and verbal working memory ( 27 ).…”