Structural and Functional Reorganization Within Cognitive Control Network Associated With Protection of Executive Function in Patients With Unilateral Frontal Gliomas.

Yong Liu,Kun Yang,Dongming Liu,Zonghong Li,Jiu Chen,Yun Yu,Guanjie Hu,Hongyi Liu,Xinhua Hu,Yuanjie Zou,Zijuan Jiang

doi:10.3389/fonc.2020.00794

Abstract

Background: The cognitive control network (CCN) is widely considered to be a frontoparietal circuit that is involved in executive function. This study aimed to investigate the structural and functional plasticity within the CCN in unilateral frontal gliomas, which are associated with the protection of executive functions.Methods: To detect structural and functional changes within the CCN, we measured gray matter (GM) volume, regional homogeneity, the amplitude of low-frequency fluctuation (ALFF), degree centrality, and functional connectivity within the CCN in 37 patients with gliomas invading the left frontal lobe (n = 16) or the right frontal lobe (n = 21) and 40 healthy controls (CNs). Partial correlation analysis was performed to assess the association between the altered structural and functional indices and executive function.Results: When the tumor invaded the left frontal lobe, the patients showed reduced ALFF in the dorsal medial prefrontal cortex (dmPFC) within the CCN and increased ALFF in the right superior parietal cortex (rSP) within the CCN compared to the CNs. When the tumor invaded the right frontal lobe, the patients showed significantly increased GM volume and ALFF in the left superior parietal cortex (lSP) within the CCN compared to the CNs. Furthermore, the patients showed significantly increased functional connectivities between the lSP and the dmPFC and between the lSP and the rSP within the CCN compared to the CNs. Increased ALFF in the lSP within the CCN was positively correlated with executive function.Conclusions: Tumors invading the frontal lobe induced contralesional structural and functional reorganization within the posterior CCN in patients with unilateral frontal gliomas. This further suggests that the contralesional superior parietal cortex acts as a functional compensation hub within the CCN, which may protect it against the detrimental effects of tumor invasion on executive functions.

Highlights

Gliomas are considered to be the most common primary brain tumors [1], with the highest proportion of frontal lobe invasion [2]
When tumors invaded the left frontal lobe, the patients showed no significant differences in gray matter (GM) volumes in any brain regions within the cognitive control network (CCN) compared to the CNs (Figure S1)
When the tumor invaded the left frontal lobe, the patients showed significantly decreased amplitude of low-frequency fluctuations (ALFF) in the dorsal medial prefrontal cortex (dmPFC) within the CCN and increased ALFF in the right superior parietal gyrus (rSP) within the CCN compared to the CNs (p < 0.05, TFCE-FWE corrected and cluster size > 30 voxels), as shown in Figure 2 and Table 2

Summary

Introduction

Gliomas are considered to be the most common primary brain tumors [1], with the highest proportion of frontal lobe invasion [2]. Local frontal lesions, which are located in the cognitive control network (CCN) involved in executive function, can affect the executive function of the brain [3,4,5,6,7]. Clinical observations show that patients with frontal gliomas retain intact executive function. Little is known about whether tumor invasion induces functional or morphological remodeling in patients with frontal gliomas, contributing to the clinical compensation phenomenon of intact executive function. The cognitive control network (CCN) is widely considered to be a frontoparietal circuit that is involved in executive function. This study aimed to investigate the structural and functional plasticity within the CCN in unilateral frontal gliomas, which are associated with the protection of executive functions

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Conclusion