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03-02-2025 | Cerebral Small Vessel Disease | Advanced Neuroimaging

Cortical structural degeneration and functional network connectivity changes in patients with subcortical vascular cognitive impairment

Authors: Haixia Mao, Yachen Shi, Qianqian Gao, Min Xu, Xiaoyun Hu, Feng Wang, Xiangming Fang

Published in: Neuroradiology

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Abstract

Purpose

To explore the structural basis of functional network connectivity (FNC) changes and early cortical degenerative patterns in subcortical vascular cognitive impairment (SVCI).

Methods

We prospectively included SVCI cases and healthy controls (HCs). FNC alterations were evaluated using group-independent component analysis of resting-state functional MRI data. Cortical microstructural and macrostructural alterations were assessed using gray matter-based spatial statistics analysis with neurite orientation dispersion and density imaging and cortical thickness analysis with FreeSurfer software on T1-weighted images, respectively. Spearman correlation analyses were performed to assess relationships between FNC alterations and cortical microstructural/macrostructural alterations and between FNC, cortical thickness, or neurite density index (NDI)/orientation dispersion index (ODI) alterations and cognitive performance.

Results

Forty-six SVCI patients and 73 HCs were recruited. FNC analysis showed lower network connectivity between the visual network (VN) and sensorimotor network (SMN) in SVCI, positively correlated with information processing speed (p=0.008) and negatively with summary SVD score (p = 0.037). Cortical microstructural analyses exhibited a lower NDI, mainly in the VN and default mode network (DMN) areas (PFWE < 0.05, cluster > 100 voxels), and lower ODI, mainly in the SMN and DMN areas (PFWE < 0.05, cluster > 100 voxels) in SVCI, both of which were related to cognitive function (p < 0.05). However, cortical thickness did not differ between groups. Lower NDI in the lateral occipital cortex was linked to lower VN-SMN connectivity in SVCI (p = 0.002).

Conclusion

Cortical microstructural alterations may serve as the basis for FNC changes in SVCI

Graphical abstract

Appendix
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Literature
3.
13.
go back to reference Skrobot OA, Black SE, Chen C, DeCarli C, Erkinjuntti T, Ford GA, Kalaria RN, O’Brien J, Pantoni L, Pasquier F, Roman GC, Wallin A, Sachdev P, Skoog I, Ben-Shlomo Y, Passmore AP, Love S, Kehoe PG (2018) Progress toward standardized diagnosis of vascular cognitive impairment: guidelines from the vascular impairment of cognition classification consensus study. Alzheimers Dement 14:280–292. https://doi.org/10.1016/j.jalz.2017.09.007CrossRefPubMed Skrobot OA, Black SE, Chen C, DeCarli C, Erkinjuntti T, Ford GA, Kalaria RN, O’Brien J, Pantoni L, Pasquier F, Roman GC, Wallin A, Sachdev P, Skoog I, Ben-Shlomo Y, Passmore AP, Love S, Kehoe PG (2018) Progress toward standardized diagnosis of vascular cognitive impairment: guidelines from the vascular impairment of cognition classification consensus study. Alzheimers Dement 14:280–292. https://​doi.​org/​10.​1016/​j.​jalz.​2017.​09.​007CrossRefPubMed
15.
go back to reference Duering M, Biessels GJ, Brodtmann A, Chen C, Cordonnier C, de Leeuw F-E, Debette S, Frayne R, Jouvent E, Rost NS, Ter Telgte A, Al-Shahi Salman R, Backes WH, Bae H-J, Brown R, Chabriat H, De Luca A, deCarli C, Dewenter A, Doubal FN, Ewers M, Field TS, Ganesh A, Greenberg S, Helmer KG, Hilal S, Jochems ACC, Jokinen H, Kuijf H, Lam BYK, Lebenberg J, MacIntosh BJ, Maillard P, Mok VCT, Pantoni L, Rudilosso S, Satizabal CL, Schirmer MD, Schmidt R, Smith C, Staals J, Thrippleton MJ, van Veluw SJ, Vemuri P, Wang Y, Werring D, Zedde M, Akinyemi RO, Del Brutto OH, Markus HS, Zhu Y-C, Smith EE, Dichgans M, Wardlaw JM (2023) Neuroimaging standards for research into small vessel disease-advances since 2013. Lancet Neurol 22:602–618. https://doi.org/10.1016/S1474-4422(23)00131-XCrossRefPubMed Duering M, Biessels GJ, Brodtmann A, Chen C, Cordonnier C, de Leeuw F-E, Debette S, Frayne R, Jouvent E, Rost NS, Ter Telgte A, Al-Shahi Salman R, Backes WH, Bae H-J, Brown R, Chabriat H, De Luca A, deCarli C, Dewenter A, Doubal FN, Ewers M, Field TS, Ganesh A, Greenberg S, Helmer KG, Hilal S, Jochems ACC, Jokinen H, Kuijf H, Lam BYK, Lebenberg J, MacIntosh BJ, Maillard P, Mok VCT, Pantoni L, Rudilosso S, Satizabal CL, Schirmer MD, Schmidt R, Smith C, Staals J, Thrippleton MJ, van Veluw SJ, Vemuri P, Wang Y, Werring D, Zedde M, Akinyemi RO, Del Brutto OH, Markus HS, Zhu Y-C, Smith EE, Dichgans M, Wardlaw JM (2023) Neuroimaging standards for research into small vessel disease-advances since 2013. Lancet Neurol 22:602–618. https://​doi.​org/​10.​1016/​S1474-4422(23)00131-XCrossRefPubMed
23.
go back to reference Guo T, Wu J, Zhou C, Guan X, Gao T, Bai X, Song Z, Xuan M, Gu Q, Huang P, Zhang B, Pu J, Xu X, Xu D, Zhang M (2020) Aberrant Fiber coherence of Amygdala-Accumbens-Pallidum pathway is associated with disorganized Nigrostriatal-Nigropallidal pathway in Parkinson’s Disease. J Magn Reson Imaging 52:1799–1808. https://doi.org/10.1002/jmri.27273CrossRefPubMed Guo T, Wu J, Zhou C, Guan X, Gao T, Bai X, Song Z, Xuan M, Gu Q, Huang P, Zhang B, Pu J, Xu X, Xu D, Zhang M (2020) Aberrant Fiber coherence of Amygdala-Accumbens-Pallidum pathway is associated with disorganized Nigrostriatal-Nigropallidal pathway in Parkinson’s Disease. J Magn Reson Imaging 52:1799–1808. https://​doi.​org/​10.​1002/​jmri.​27273CrossRefPubMed
39.
go back to reference Huang SY, Witzel T, Keil B, Scholz A, Davids M, Dietz P, Rummert E, Ramb R, Kirsch JE, Yendiki A, Fan Q, Tian Q, Ramos-Llordén G, Lee H-H, Nummenmaa A, Bilgic B, Setsompop K, Wang F, Avram AV, Komlosh M, Benjamini D, Magdoom KN, Pathak S, Schneider W, Novikov DS, Fieremans E, Tounekti S, Mekkaoui C, Augustinack J, Berger D, Shapson-Coe A, Lichtman J, Basser PJ, Wald LL, Rosen BR (2021) Connectome 2.0: Developing the next-generation ultra-high gradient strength human MRI scanner for bridging studies of the micro-, meso- and macro-connectome. Neuroimage 243:118530. https://doi.org/10.1016/j.neuroimage.2021.118530 Huang SY, Witzel T, Keil B, Scholz A, Davids M, Dietz P, Rummert E, Ramb R, Kirsch JE, Yendiki A, Fan Q, Tian Q, Ramos-Llordén G, Lee H-H, Nummenmaa A, Bilgic B, Setsompop K, Wang F, Avram AV, Komlosh M, Benjamini D, Magdoom KN, Pathak S, Schneider W, Novikov DS, Fieremans E, Tounekti S, Mekkaoui C, Augustinack J, Berger D, Shapson-Coe A, Lichtman J, Basser PJ, Wald LL, Rosen BR (2021) Connectome 2.0: Developing the next-generation ultra-high gradient strength human MRI scanner for bridging studies of the micro-, meso- and macro-connectome. Neuroimage 243:118530. https://​doi.​org/​10.​1016/​j.​neuroimage.​2021.​118530
44.
go back to reference Mattioli P, Pardini M, Famà F, Girtler N, Brugnolo A, Orso B, Meli R, Filippi L, Grisanti S, Massa F, Bauckneht M, Miceli A, Terzaghi M, Morbelli S, Nobili F, Arnaldi D (2021) Cuneus/precuneus as a central hub for brain functional connectivity of mild cognitive impairment in idiopathic REM sleep behavior patients. Eur J Nucl Med Mol Imaging 48:2834–2845. https://doi.org/10.1007/s00259-021-05205-6CrossRefPubMed Mattioli P, Pardini M, Famà F, Girtler N, Brugnolo A, Orso B, Meli R, Filippi L, Grisanti S, Massa F, Bauckneht M, Miceli A, Terzaghi M, Morbelli S, Nobili F, Arnaldi D (2021) Cuneus/precuneus as a central hub for brain functional connectivity of mild cognitive impairment in idiopathic REM sleep behavior patients. Eur J Nucl Med Mol Imaging 48:2834–2845. https://​doi.​org/​10.​1007/​s00259-021-05205-6CrossRefPubMed
48.
49.
go back to reference Banerjee G, Jang H, Kim HJ, Kim ST, Kim JS, Lee JH, Im K, Kwon H, Lee JM, Na DL, Seo SW, Werring DJ (2018) Total MRI small vessel disease burden correlates with cognitive performance, cortical atrophy, and network measures in a memory clinic population. J Alzheimers Dis 63:1485–1497. https://doi.org/10.3233/JAD-170943CrossRefPubMed Banerjee G, Jang H, Kim HJ, Kim ST, Kim JS, Lee JH, Im K, Kwon H, Lee JM, Na DL, Seo SW, Werring DJ (2018) Total MRI small vessel disease burden correlates with cognitive performance, cortical atrophy, and network measures in a memory clinic population. J Alzheimers Dis 63:1485–1497. https://​doi.​org/​10.​3233/​JAD-170943CrossRefPubMed
Metadata
Title
Cortical structural degeneration and functional network connectivity changes in patients with subcortical vascular cognitive impairment
Authors
Haixia Mao
Yachen Shi
Qianqian Gao
Min Xu
Xiaoyun Hu
Feng Wang
Xiangming Fang
Publication date
03-02-2025
Publisher
Springer Berlin Heidelberg
Published in
Neuroradiology
Print ISSN: 0028-3940
Electronic ISSN: 1432-1920
DOI
https://doi.org/10.1007/s00234-025-03550-z

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