Alterations in brain morphology and functional connectivity mediate cognitive decline in carotid atherosclerotic stenosis

Subinuer Maimaitiaili; Chen Tang; Cheng Liu; Xiaochen Lv; Zhipeng Chen; Mengqiang Zhang; Jing Cai; Zishun Liang; Biao Zhao; Wen Zhang; Tong Qiao

doi:10.3389/fnagi.2024.1395911

Alterations in brain morphology and functional connectivity mediate cognitive decline in carotid atherosclerotic stenosis

Front Aging Neurosci. 2024 Jun 20:16:1395911. doi: 10.3389/fnagi.2024.1395911. eCollection 2024.

Authors

Affiliations

¹ Department of Vascular Surgery, Nanjing Drum Tower Hospital, Affiliated Hospital of Medical School, Nanjing University, Nanjing, China.
² Department of Radiology, Nanjing Drum Tower Hospital, Affiliated Hospital of Medical School, Nanjing University, Nanjing, China.

^# Contributed equally.

Abstract

Background: Patients with carotid atherosclerotic stenosis (CAS) often have varying degrees of cognitive decline. However, there is little evidence regarding how brain morphological and functional abnormalities impact the cognitive decline in CAS patients. This study aimed to determine how the brain morphological and functional changes affected the cognitive decline in patients with CAS.

Methods: The brain morphological differences were analyzed using surface and voxel-based morphometry, and the seed-based whole-brain functional connectivity (FC) abnormalities were analyzed using resting-state functional magnetic resonance imaging. Further, mediation analyses were performed to determine whether and how morphological and FC changes affect cognition in CAS patients.

Results: The CAS-MCI (CAS patients with mild cognitive impairment) group performed worse in working memory, verbal fluency, and executive time. Cortical thickness (CT) of the left postcentral and superiorparietal were significantly reduced in CAS-MCI patients. The gray matter volume (GMV) of the right olfactory, left temporal pole (superior temporal gyrus) (TPOsup.L), left middle temporal gyrus (MTG.L), and left insula (INS.L) were decreased in the CAS-MCI group. Besides, decreased seed-based FC between TPOsup.L and left precuneus, between MTG.L and TPOsup.L, and between INS.L and MTG.L, left middle frontal gyrus, as well as Superior frontal gyrus, were found in CAS-MCI patients. Mediation analyses demonstrated that morphological and functional abnormalities fully mediated the association between the maximum degree of carotid stenosis and cognitive function.

Conclusion: Multiple brain regions have decreased GMV and CT in CAS-MCI patients, along with disrupted seed-based FC. These morphological and functional changes play a crucial role in the cognitive impairment in CAS patients.

Keywords: cognitive impairment; cortical thickness; functional connectivity; gray matter volume; maximum degree of carotid stenosis.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This work was supported by the funding for Clinical Trials from the Affiliated Drum Tower Hospital, Medical School of Nanjing University (2021-LCYJ-MS-18), Jiangsu Provincial Health Commission Research Project (ZD2021056), and Nanjing Medical Science and Technology Development Foundation (ZKX22012).