Resting-state functional connectivity predicts individual language impairment of patients with left hemispheric gliomas involving language network

Language deficits following brain tumors should consider the dynamic interactions between different tumor growth kinetics and functional network reorganization. We measured the resting-state functional connectivity of 126 patients with left cerebral gliomas involving language network areas, includin...

Full description

Bibliographic Details
Main Authors: Binke Yuan, Nan Zhang, Jing Yan, Jingliang Cheng, Junfeng Lu, Jinsong Wu
Format: Article
Language:English
Published: Elsevier 2019-01-01
Series:NeuroImage: Clinical
Online Access:http://www.sciencedirect.com/science/article/pii/S2213158219303730
id doaj-8158336b711a4a6391a1b18352ae4aeb
record_format Article
spelling doaj-8158336b711a4a6391a1b18352ae4aeb2020-11-25T02:44:09ZengElsevierNeuroImage: Clinical2213-15822019-01-0124Resting-state functional connectivity predicts individual language impairment of patients with left hemispheric gliomas involving language networkBinke Yuan0Nan Zhang1Jing Yan2Jingliang Cheng3Junfeng Lu4Jinsong Wu5Center for Language and Brain, Shenzhen Institute of Neuroscience, Shenzhen, ChinaDepartment of Neurosurgery, The First Affiliated Hospital of USTC, Division of Life Sciences and Medicine, University of Science and Technology of China, Hefei, Anhui, China; Glioma Surgery Division, Department of Neurosurgery, Huashan Hospital, Fudan University, Shanghai, ChinaDepartment of MRI, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, ChinaDepartment of MRI, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, ChinaGlioma Surgery Division, Department of Neurosurgery, Huashan Hospital, Fudan University, Shanghai, ChinaGlioma Surgery Division, Department of Neurosurgery, Huashan Hospital, Fudan University, Shanghai, China; Shanghai Key Laboratory of Medical Image Computing and Computer Assisted Intervention, Shanghai, China; Corresponding author at: Glioma Surgery Division, Neurosurgery Department of Huashan Hospital, Shanghai Medical College, Fudan University, Shanghai 200040, China.Language deficits following brain tumors should consider the dynamic interactions between different tumor growth kinetics and functional network reorganization. We measured the resting-state functional connectivity of 126 patients with left cerebral gliomas involving language network areas, including 77 patients with low-grade gliomas (LGG) and 49 patients with high-grade gliomas (HGG). Functional network mapping for language was performed by construction of a multivariate machine learning-based prediction model of individual aphasia quotient (AQ), a summary score that indicates overall severity of language impairment. We found that the AQ scores for HGG patients were significantly lower than those of LGG patients. The prediction accuracy of HGG patients (R2 = 0.27, permutation P = 0.007) was much higher than that of LGG patients (R2 = 0.09, permutation P = 0.032). The rsFC regions predictive of LGG's AQ involved the bilateral frontal, temporal, and parietal lobes, subcortical regions, and bilateral cerebro-cerebellar connections, mainly in regions belonging to the canonical language network. The functional network of language processing for HGG patients showed strong dependence on connections of the left cerebro-cerebellar connections, limbic system, and the temporal, occipital, and prefrontal lobes. Together, our findings suggested that individual language processing of glioma patients links large-scale, bilateral, cortico-subcortical, and cerebro-cerebellar functional networks with different network reorganizational mechanisms underlying the different levels of language impairments in LGG and HGG patients. Keywords: Low-grade glioma, High-grade glioma, Resting-state fMRI, Language, Machine learninghttp://www.sciencedirect.com/science/article/pii/S2213158219303730
collection DOAJ
language English
format Article
sources DOAJ
author Binke Yuan
Nan Zhang
Jing Yan
Jingliang Cheng
Junfeng Lu
Jinsong Wu
spellingShingle Binke Yuan
Nan Zhang
Jing Yan
Jingliang Cheng
Junfeng Lu
Jinsong Wu
Resting-state functional connectivity predicts individual language impairment of patients with left hemispheric gliomas involving language network
NeuroImage: Clinical
author_facet Binke Yuan
Nan Zhang
Jing Yan
Jingliang Cheng
Junfeng Lu
Jinsong Wu
author_sort Binke Yuan
title Resting-state functional connectivity predicts individual language impairment of patients with left hemispheric gliomas involving language network
title_short Resting-state functional connectivity predicts individual language impairment of patients with left hemispheric gliomas involving language network
title_full Resting-state functional connectivity predicts individual language impairment of patients with left hemispheric gliomas involving language network
title_fullStr Resting-state functional connectivity predicts individual language impairment of patients with left hemispheric gliomas involving language network
title_full_unstemmed Resting-state functional connectivity predicts individual language impairment of patients with left hemispheric gliomas involving language network
title_sort resting-state functional connectivity predicts individual language impairment of patients with left hemispheric gliomas involving language network
publisher Elsevier
series NeuroImage: Clinical
issn 2213-1582
publishDate 2019-01-01
description Language deficits following brain tumors should consider the dynamic interactions between different tumor growth kinetics and functional network reorganization. We measured the resting-state functional connectivity of 126 patients with left cerebral gliomas involving language network areas, including 77 patients with low-grade gliomas (LGG) and 49 patients with high-grade gliomas (HGG). Functional network mapping for language was performed by construction of a multivariate machine learning-based prediction model of individual aphasia quotient (AQ), a summary score that indicates overall severity of language impairment. We found that the AQ scores for HGG patients were significantly lower than those of LGG patients. The prediction accuracy of HGG patients (R2 = 0.27, permutation P = 0.007) was much higher than that of LGG patients (R2 = 0.09, permutation P = 0.032). The rsFC regions predictive of LGG's AQ involved the bilateral frontal, temporal, and parietal lobes, subcortical regions, and bilateral cerebro-cerebellar connections, mainly in regions belonging to the canonical language network. The functional network of language processing for HGG patients showed strong dependence on connections of the left cerebro-cerebellar connections, limbic system, and the temporal, occipital, and prefrontal lobes. Together, our findings suggested that individual language processing of glioma patients links large-scale, bilateral, cortico-subcortical, and cerebro-cerebellar functional networks with different network reorganizational mechanisms underlying the different levels of language impairments in LGG and HGG patients. Keywords: Low-grade glioma, High-grade glioma, Resting-state fMRI, Language, Machine learning
url http://www.sciencedirect.com/science/article/pii/S2213158219303730
work_keys_str_mv AT binkeyuan restingstatefunctionalconnectivitypredictsindividuallanguageimpairmentofpatientswithlefthemisphericgliomasinvolvinglanguagenetwork
AT nanzhang restingstatefunctionalconnectivitypredictsindividuallanguageimpairmentofpatientswithlefthemisphericgliomasinvolvinglanguagenetwork
AT jingyan restingstatefunctionalconnectivitypredictsindividuallanguageimpairmentofpatientswithlefthemisphericgliomasinvolvinglanguagenetwork
AT jingliangcheng restingstatefunctionalconnectivitypredictsindividuallanguageimpairmentofpatientswithlefthemisphericgliomasinvolvinglanguagenetwork
AT junfenglu restingstatefunctionalconnectivitypredictsindividuallanguageimpairmentofpatientswithlefthemisphericgliomasinvolvinglanguagenetwork
AT jinsongwu restingstatefunctionalconnectivitypredictsindividuallanguageimpairmentofpatientswithlefthemisphericgliomasinvolvinglanguagenetwork
_version_ 1724767175790559232