Connectivity related to major brain functions in Alzheimer disease progression: microstructural properties of the cingulum bundle and its subdivision using diffusion-weighted MRI

Abstract Background The cingulum bundle is a brain white matter fasciculus associated with the cingulate gyrus. It connects areas from the temporal to the frontal lobe. It is composed of fibers with different terminations, lengths, and structural properties, related to specific brain functions. We a...

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Main Authors: Mattia Ricchi, Guido Campani, Anastasiia Nagmutdinova, Villiam Bortolotti, Danilo Greco, Carlo Golini, James Grist, Leonardo Brizi, Claudia Testa
Format: Article
Language:English
Published: SpringerOpen 2025-03-01
Series:European Radiology Experimental
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Online Access:https://doi.org/10.1186/s41747-025-00570-5
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author Mattia Ricchi
Guido Campani
Anastasiia Nagmutdinova
Villiam Bortolotti
Danilo Greco
Carlo Golini
James Grist
Leonardo Brizi
Claudia Testa
author_facet Mattia Ricchi
Guido Campani
Anastasiia Nagmutdinova
Villiam Bortolotti
Danilo Greco
Carlo Golini
James Grist
Leonardo Brizi
Claudia Testa
author_sort Mattia Ricchi
collection DOAJ
description Abstract Background The cingulum bundle is a brain white matter fasciculus associated with the cingulate gyrus. It connects areas from the temporal to the frontal lobe. It is composed of fibers with different terminations, lengths, and structural properties, related to specific brain functions. We aimed to automatically reconstruct this fasciculus in patients with Alzheimer disease (AD) and mild cognitive impairment (MCI) and to assess whether trajectories have different microstructural properties in relation to dementia progression. Methods Multi-shell high angular resolution diffusion imaging−HARDI image datasets from the "Alzheimer's Disease Neuroimaging Initiative"−ADNI repository of 10 AD, 18 MCI, and 21 cognitive normal (CN) subjects were used to reconstruct three subdivisions of the cingulum bundle, using a probabilistic approach, combined with measurements of diffusion tensor and neurite orientation dispersion and density imaging metrics in each subdivision. Results The subdivisions exhibit different pathways, terminations, and structural characteristics. We found differences in almost all the diffusivity metrics among the subdivisions (p < 0.001 for all the metrics) and between AD versus CN and MCI versus CN subjects for mean diffusivity (p = 0.007–0.038), radial diffusivity (p = 0.008–0.049) and neurite dispersion index (p = 0.005–0.049). Conclusion Results from tractography analysis of the subdivisions of the cingulum bundle showed an association in the role of groups of fibers with their functions and the variance of their properties in relation to dementia progression. Relevance statement The cingulum bundle is a complex tract with several pathways and terminations related to many cognitive functions. A probabilistic automatic approach is proposed to reconstruct its subdivisions, showing different microstructural properties and variations. A larger sample of patients is needed to confirm results and elucidate the role of diffusion parameters in characterizing alterations in brain function and progression to dementia. Key Points The microstructure of the cingulum bundle is related to brain cognitive functions. A probabilistic automatic approach is proposed to reconstruct the subdivisions of the cingulum bundle by diffusion-weighted images. The subdivisions showed different microstructural properties and variations in relation to the progression of dementia. Graphical Abstract
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spelling doaj-art-ea36e0b3ea6d445396866a3ccb29d1742025-08-20T03:41:39ZengSpringerOpenEuropean Radiology Experimental2509-92802025-03-019111310.1186/s41747-025-00570-5Connectivity related to major brain functions in Alzheimer disease progression: microstructural properties of the cingulum bundle and its subdivision using diffusion-weighted MRIMattia Ricchi0Guido Campani1Anastasiia Nagmutdinova2Villiam Bortolotti3Danilo Greco4Carlo Golini5James Grist6Leonardo Brizi7Claudia Testa8Department of Computer Science, University of PisaEuropean Institue of Oncology (IEO)Department of Civil, Chemical, Environmental, and Materials Engineering, University of BolognaDepartment of Civil, Chemical, Environmental, and Materials Engineering, University of BolognaDepartment of Management, Economics and Industrial Engineering, Politecnico di MilanoDepartment of Physics and Astronomy, University of BolognaDepartment of Physiology, Anatomy and Genetics, University of OxfordDepartment of Physics and Astronomy, University of BolognaINFN, Division of BolognaAbstract Background The cingulum bundle is a brain white matter fasciculus associated with the cingulate gyrus. It connects areas from the temporal to the frontal lobe. It is composed of fibers with different terminations, lengths, and structural properties, related to specific brain functions. We aimed to automatically reconstruct this fasciculus in patients with Alzheimer disease (AD) and mild cognitive impairment (MCI) and to assess whether trajectories have different microstructural properties in relation to dementia progression. Methods Multi-shell high angular resolution diffusion imaging−HARDI image datasets from the "Alzheimer's Disease Neuroimaging Initiative"−ADNI repository of 10 AD, 18 MCI, and 21 cognitive normal (CN) subjects were used to reconstruct three subdivisions of the cingulum bundle, using a probabilistic approach, combined with measurements of diffusion tensor and neurite orientation dispersion and density imaging metrics in each subdivision. Results The subdivisions exhibit different pathways, terminations, and structural characteristics. We found differences in almost all the diffusivity metrics among the subdivisions (p < 0.001 for all the metrics) and between AD versus CN and MCI versus CN subjects for mean diffusivity (p = 0.007–0.038), radial diffusivity (p = 0.008–0.049) and neurite dispersion index (p = 0.005–0.049). Conclusion Results from tractography analysis of the subdivisions of the cingulum bundle showed an association in the role of groups of fibers with their functions and the variance of their properties in relation to dementia progression. Relevance statement The cingulum bundle is a complex tract with several pathways and terminations related to many cognitive functions. A probabilistic automatic approach is proposed to reconstruct its subdivisions, showing different microstructural properties and variations. A larger sample of patients is needed to confirm results and elucidate the role of diffusion parameters in characterizing alterations in brain function and progression to dementia. Key Points The microstructure of the cingulum bundle is related to brain cognitive functions. A probabilistic automatic approach is proposed to reconstruct the subdivisions of the cingulum bundle by diffusion-weighted images. The subdivisions showed different microstructural properties and variations in relation to the progression of dementia. Graphical Abstracthttps://doi.org/10.1186/s41747-025-00570-5Alzheimer diseaseBrainCognitive dysfunctionDiffusion magnetic resonance imagingWhite matter
spellingShingle Mattia Ricchi
Guido Campani
Anastasiia Nagmutdinova
Villiam Bortolotti
Danilo Greco
Carlo Golini
James Grist
Leonardo Brizi
Claudia Testa
Connectivity related to major brain functions in Alzheimer disease progression: microstructural properties of the cingulum bundle and its subdivision using diffusion-weighted MRI
European Radiology Experimental
Alzheimer disease
Brain
Cognitive dysfunction
Diffusion magnetic resonance imaging
White matter
title Connectivity related to major brain functions in Alzheimer disease progression: microstructural properties of the cingulum bundle and its subdivision using diffusion-weighted MRI
title_full Connectivity related to major brain functions in Alzheimer disease progression: microstructural properties of the cingulum bundle and its subdivision using diffusion-weighted MRI
title_fullStr Connectivity related to major brain functions in Alzheimer disease progression: microstructural properties of the cingulum bundle and its subdivision using diffusion-weighted MRI
title_full_unstemmed Connectivity related to major brain functions in Alzheimer disease progression: microstructural properties of the cingulum bundle and its subdivision using diffusion-weighted MRI
title_short Connectivity related to major brain functions in Alzheimer disease progression: microstructural properties of the cingulum bundle and its subdivision using diffusion-weighted MRI
title_sort connectivity related to major brain functions in alzheimer disease progression microstructural properties of the cingulum bundle and its subdivision using diffusion weighted mri
topic Alzheimer disease
Brain
Cognitive dysfunction
Diffusion magnetic resonance imaging
White matter
url https://doi.org/10.1186/s41747-025-00570-5
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