Reorganization of cerebro‐cerebellar circuit in patients with left hemispheric gliomas involving language network: A combined structural and resting‐state functional MRI study

Abstract

The role of cerebellum and cerebro-cerebellar system in neural plasticity induced by cerebral gliomas involving language network has long been ignored. Moreover, whether or not the process of reorganization is different in glioma patients with different growth kinetics remains largely unknown. To address this issue, we utilized preoperative structural and resting-state functional MRI data of 78 patients with left cerebral gliomas involving language network areas, including 46 patients with low-grade glioma (LGG, WHO grade II), 32 with high-grade glioma (HGG, WHO grade III/IV), and 44 healthy controls. Spontaneous brain activity, resting-state functional connectivity and gray matter volume alterations of the cerebellum were examined. We found that both LGG and HGG patients exhibited bidirectional alteration of brain activity in language-related cerebellar areas. Brain activity in areas with increased alteration was significantly correlated with the language and MMSE scores. Structurally, LGG patients exhibited greater gray matter volume in regions with increased brain activity, suggesting a structure-function coupled alteration in cerebellum. Furthermore, we observed that cerebellar regions with decreased brain activity exhibited increased functional connectivity with contralesional cerebro-cerebellar system in LGG patients. Together, our findings provide empirical evidence for a vital role of cerebellum and cerebro-cerebellar circuit in neural plasticity following lesional damage to cerebral language network. Moreover, we highlight the possible different reorganizational mechanisms of brain functional connectivity underlying different levels of behavioral impairments in LGG and HGG patients.

Functional Mapping before and after Low-Grade Glioma Surgery: A New Way to Decipher Various Spatiotemporal Patterns of Individual Neuroplastic Potential in Brain Tumor Patients

“…Thus, the structural effect of tumor invasion may extend beyond the affected region, in a network-based reorganization (here, within the control cognitive network) underlying neuroplastic mechanisms. Interestingly, patients with hemispheric LGG involving language circuits can also exhibit an increased gray matter volume in language-cerebellar regions: Therefore, the cerebellum could be implicated in the process of post-lesional neuroplasticity [ 34 ]. At the ultrastructural level, these macroscopic changes might be underpinned by an increase in cell size or spine density, and neural or glial cell genesis [ 35 , 36 ].…”

“…Functional reshaping of cerebro-cerebellar networks in left hemispheric glioma involving language areas was also evidenced by rsfMRI, with modifications of the activity in language-related cerebellar areas [ 34 ]. Interestingly, different patterns of neuroplasticity based upon various mechanisms of FC changes were correlated with different levels of cognitive disturbances: Cerebellar activity in regions with increased alteration was significantly associated with language (especially naming and comprehension scores) and MMSE Mini Mental State Examination scores [ 34 ].…”

“…Functional reshaping of cerebro-cerebellar networks in left hemispheric glioma involving language areas was also evidenced by rsfMRI, with modifications of the activity in language-related cerebellar areas [ 34 ]. Interestingly, different patterns of neuroplasticity based upon various mechanisms of FC changes were correlated with different levels of cognitive disturbances: Cerebellar activity in regions with increased alteration was significantly associated with language (especially naming and comprehension scores) and MMSE Mini Mental State Examination scores [ 34 ]. Therefore, Yuan et al [ 72 ] concluded that individual language processing investigated in patients with a left hemispheric tumor using rsfMRI relied on large-scale, bilateral, cortical-subcortical, and cerebro-cerebellar circuits with various network reallocation mechanisms underpinning the different levels of language worsening in LGG and HGG patients.…”

What do we know about pre- and postoperative plasticity in patients with glioma? A review of neuroimaging and intraoperative mapping studies

“…Patients with HGG versus LGG often showed relevant presurgical impairments ( Campanella et al, 2008 ; Zhang et al, 2018 ). This is generally attributed to the more rapid HGG growth limiting the development of compensatory processes.…”

“…In HGG vs . LGG, greater variability in the lateralization indices and more frequent bilateral activation Ulmer et al, 2003 1 L frontal LGG fMRI and IOM Language x Discrepancy between fMRI showing almost only RH activation and IOM confirming LH dominance Voets et al, 2019 44 Language-dominant hemisphere Both fMRI Language x x Zhang et al, 2018 78 L language network Both sMRI (+resting-state functional connectivity) Language x In LGG (but not HGG), higher gray-matter volume in medial bilateral cerebellar lobule VII (region with increased spontaneous brain activity in the left hemisphere) + increase in functional connectivity Zheng et al, 2013 10 L frontal LGG DTI Language Increased left-lateralization of some language fascicles (i.e., ILF and IFOF), involved in compensation Sensorimotor and language systems Almairac et al, 2018 84 L or R insula LGG sMRI None x Herbet et al, 2016 231 Either hemisphere LGG IOM Language, sensory, motor Definition of an atlas of cortical and subcortical plasticity, showing low WM plasticity Ius et al, 2011 58 Close/in eloquent areas in either hemisphere LGG IOM Language, sensory, motor N/A Defined a 'minimal common brain' of structures with low compensation potential (especially WM) Ojemann et al, 1996 14 Close to eloquent areas in either hemisphere Both ...…”