Abstract
BackgroundPrior investigations of language functions have focused on the response profiles of particular brain regions. However, the specialized and static view of language processing does not explain numerous observations of functional recovery following brain surgery. To investigate the dynamic alterations of functional connectivity (FC) within language network (LN) in glioma patients, we explored a new flexible model based on the neuroscientific hypothesis of core-periphery organization in LN.MethodsGroup-level LN mapping was determined from 109 glioma patients and forty-two healthy controls (HCs) using independent component analysis (ICA). FC and mean network connectivity (mNC: l/rFCw, FCb, and FCg) were compared between patients and HCs. Correlations between mNC and tumor volume (TV) were calculated.ResultsWe identified ten separate LN modules from ICA. Compared to HCs, glioma patients showed a significant reduction in language network functional connectivity (LNFC), with a distinct pattern modulated by tumor position. Left hemisphere gliomas had a broader impact on FC than right hemisphere gliomas, with more reduced edges away from tumor sites (p=0.011). mNC analysis revealed a significant reduction in all indicators of FC except for lFCw in right hemisphere gliomas. These alterations were associated with TV in a double correlative relationship depending on the tumor position across hemispheres.ConclusionOur findings emphasize the importance of considering the modulatory effects of core-periphery mechanisms from a network perspective. Preoperative evaluation of changes in LN caused by gliomas could provide the surgeon a reference to optimize resection while maintaining functional balance.
Highlights
The posterior part of the left superior temporal gyrus (Wernicke’s area) and the rostral part of the left inferior frontal cortices (Broca’s area) have been associated with language comprehension and production and are classically designated as “eloquent” areas [1, 2]
Corresponding to the glioma locations in the four subsystems of language-related areas, we categorized the patients into four subgroups, the left frontal glioma subgroup (LFG), left temporal glioma subgroup (LTG), right frontal glioma subgroup (RFG), and right temporal glioma subgroup (RTG), to study the effect of lesion topography on language network functional connectivity (LNFC)
Language scores derived from Mini Mental State Examination (MMSE) sections demonstrated a significant difference among patient groups and HCs [F [4, 146] = 2.75; p =0.03], no remarkable difference was found among the four patient groups [F [3, 105] = 1.77; p = 0.09]
Summary
The posterior part of the left superior temporal gyrus (Wernicke’s area) and the rostral part of the left inferior frontal cortices (Broca’s area) have been associated with language comprehension and production and are classically designated as “eloquent” areas [1, 2]. Recent studies have revealed that bilateral temporal, parietal, prefrontal, and putamen regions [3] and even the cerebellum [4] are involved in language processing, reflecting a large-scale network engaging in language comprehension and production distributed at both the cortical and subcortical levels. Within this distributed language processing system, the left hemisphere frontotemporal subnetwork is widely assumed to underpin language comprehension in the key combinatorial language domains of grammatical computations and semantic operations [5], while the right hemisphere subnetwork contributes to linguistic working memory capacity [6, 7]. To investigate the dynamic alterations of functional connectivity (FC) within language network (LN) in glioma patients, we explored a new flexible model based on the neuroscientific hypothesis of core-periphery organization in LN
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