Dynamic network reorganization underlying neuroplasticity: the deficits-severity-related language network dynamics in patients with left hemispheric gliomas involving language network

Author:

Yuan Binke12ORCID,Xie Hui23,Gong Fangyuan4,Zhang Nan56ORCID,Xu Yangwen7,Zhang Hanqing12,Liu Jiaxuan12,Chen Lifeng12,Li Chaoqun12,Tan Shiyao12,Lin Zonghui12,Hu Xin12,Gu Tianyi12,Cheng Jingliang8,Lu Junfeng5910,Liu Dongqiang1112,Wu Jinsong5910ORCID,Yan Jing8

Affiliation:

1. South China Normal University, Ministry of Education Philosophy and Social Science Laboratory of Reading and Development in Children and Adolescents, , No. 55, West of Zhongshan Avenue, Tianhe District, Guangzhou 510631 , China

2. Institute for Brain Research and Rehabilitation, South China Normal University , No. 55, West of Zhongshan Avenue, Tianhe District, Guangzhou 5106318 , China

3. The University of Hong Kong, Pokfulam Department of Psychology, , Room 7.12, Jockey Club Tower, Hong Kong 999077 , China

4. Huashan Hospital Glioma Surgery Division, Department of Neurosurgery, , Fudan University, No. 12 Middle Wulumuqi Rd., Shanghai 200040 , China

5. Huashan Hospital, Fudan University Glioma Surgery Division, Department of Neurosurgery, , No. 12 Middle Wulumuqi Rd., Shanghai 200040 , China

6. The First Affiliated Hospital of USTC, University of Science and Technology of China Division of Life Sciences and Medicine, Department of Neurosurgery, , No. 17 Lujiang Road, Luyang District, Hefei City, Anhui 230001 , China

7. University of Trento Center for Mind/Brain Sciences (CIMeC), , Via Calepina, 14, Trento, 38122 , Italy

8. The First Affiliated Hospital of Zhengzhou University Department of MRI, , Zhengzhou , China

9. Neurosurgical Institute of Fudan University Brain Function Laboratory, , Shanghai , China

10. Shanghai Key Laboratory of Brain Function Restoration and Neural Regeneration , No. 12 Middle Wulumuqi Rd., Shanghai 20004010 , China

11. Liaoning Normal University Research Center of Brain and Cognitive Neuroscience, , Room 317, Dalian, Liaoning province 116029 , China

12. Key Laboratory of Brain and Cognitive Neuroscience , Room 317, Dalian, Liaoning province 116029 , China

Abstract

Abstract Brain network dynamics not only endow the brain with flexible coordination for various cognitive processes but also with a huge potential of neuroplasticity for development, skill learning, and after cerebral injury. Diffusive and progressive glioma infiltration triggers the neuroplasticity for functional compensation, which is an outstanding pathophysiological model for the investigation of network reorganization underlying neuroplasticity. In this study, we employed dynamic conditional correlation to construct framewise language networks and investigated dynamic reorganizations in 83 patients with left hemispheric gliomas involving language networks (40 patients without aphasia and 43 patients with aphasia). We found that, in healthy controls (HCs) and patients, the language network dynamics in resting state clustered into 4 temporal-reoccurring states. Language deficits-severity-dependent topological abnormalities of dFCs were observed. Compared with HCs, suboptimal language network dynamics were observed for those patients without aphasia, while more severe network disruptions were observed for those patients with aphasia. Machine learning-based dFC-linguistics prediction analyses showed that dFCs of the 4 states significantly predicted individual patients’ language scores. These findings shed light on our understanding of metaplasticity in glioma. Glioma-induced language network reorganizations were investigated under a dynamic “meta-networking” (network of networks) framework. In healthy controls and patients with glioma, the framewise language network dynamics in resting-state robustly clustered into 4 temporal-reoccurring states. The spatial but not temporal language deficits-severity-dependent abnormalities of dFCs were observed in patients with left hemispheric gliomas involving language network. Language network dynamics significantly predicted individual patients’ language scores.

Funder

Shanghai Shenkang Hospital Development Center

Shanghai Municipal Science and Technology Major Project

Fundamental Research Funds for the Central Universities

Natural Science Foundation of Anhui Province

Key Program of Medical Science and Technique Foundation of Henan Province

Excellent Youth Talent Cultivation Program of Innovation in Health Science and Technology of Henan Province

National Natural Science Foundation of China

Key-Area Research and Development Program of Guangdong Province

National Social Science Foundation of China

Publisher

Oxford University Press (OUP)

Subject

Cellular and Molecular Neuroscience,Cognitive Neuroscience

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