Tract-specific white matter hyperintensities disrupt neural network function in Alzheimer’s disease

Alexander N. W. Taylor; Lana Kambeitz-Ilankovic; Benno Gesierich; Lee Simon-Vermot; Nicolai Franzmeier; Miguel A.  Araque Caballero; Sophia   Meuller; Liu Hesheng; Birgit  Ertl-Wagner; Katharina Beurger; Michael Weiner; Martin Dichgans; Marco Duering; Michael Ewers

doi:10.1016/j.jalz.2016.06.2358

Tract-specific white matter hyperintensities disrupt neural network function in Alzheimer’s disease

Alexander N. W. Taylor, Lana Kambeitz-Ilankovic, Benno Gesierich, Lee Simon-Vermot, Nicolai Franzmeier, Miguel A. Araque Caballero, Sophia Meuller, Liu Hesheng, Birgit Ertl-Wagner, Katharina Beurger, Michael Weiner, Martin Dichgans, Marco Duering, Michael Ewers

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Abstract

Introduction
White matter hyperintensities (WMHs) increase the risk of Alzheimer's disease (AD). Whether WMHs are associated with the decline of functional neural networks in AD is debated.

Method
Resting-state functional magnetic resonance imaging and WMH were assessed in 78 subjects with increased amyloid levels on AV-45 positron emission tomography (PET) in different clinical stages of AD. We tested the association between WMH volume in major atlas-based fiber tract regions of interest (ROIs) and changes in functional connectivity (FC) between the tracts' projection areas within the default mode network (DMN).

Results
WMH volume within the inferior fronto-occipital fasciculus (IFOF) was the highest among all tract ROIs and associated with reduced FC in IFOF-connected DMN areas, independently of global AV-45 PET. Higher AV-45 PET contributed to reduced FC in IFOF-connected, temporal, and parietal DMN areas.

Conclusions
High fiber tract WMH burden is associated with reduced FC in connected areas, thus adding to the effects of amyloid pathology on neuronal network function.

Original language	English
Pages (from-to)	225-235
Number of pages	11
Journal	Alzheimer's & Dementia
Volume	13
Issue number	3
Early online date	15 Jul 2016
DOIs	https://doi.org/10.1016/j.jalz.2016.06.2358
Publication status	Published - 01 Mar 2017
Externally published	Yes

Keywords

Alzheimer's disease
Functional connectivity
Fibre tract
resting-state fMRI
White matter hyperintensities
vascular
amyloid-beta
Resting-state fMRI
Fiber tract
Vascular
Amyloid-beta
Humans
Male
Nerve Net/diagnostic imaging
Positron-Emission Tomography
White Matter/diagnostic imaging
Neuropsychological Tests
Magnetic Resonance Imaging
Image Processing, Computer-Assisted
Aged, 80 and over
Brain Mapping
Female
Aged
Alzheimer Disease/diagnostic imaging

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Tract-specific white matter hyperintensities disrupt neural network function in Alzheimer's diseaseFinal published version, 1.95 MBLicence: CC BY-NC-ND

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Taylor, A. N. W., Kambeitz-Ilankovic, L., Gesierich, B., Simon-Vermot, L., Franzmeier, N., Araque Caballero, M. A., Meuller, S., Hesheng, L., Ertl-Wagner, B., Beurger, K., Weiner, M., Dichgans, M., Duering, M., & Ewers, M. (2017). Tract-specific white matter hyperintensities disrupt neural network function in Alzheimer’s disease. Alzheimer's & Dementia, 13(3), 225-235. https://doi.org/10.1016/j.jalz.2016.06.2358

@article{06333c2182b34c11b081016bfb5cec01,

title = "Tract-specific white matter hyperintensities disrupt neural network function in Alzheimer{\textquoteright}s disease",

abstract = "Introduction White matter hyperintensities (WMHs) increase the risk of Alzheimer's disease (AD). Whether WMHs are associated with the decline of functional neural networks in AD is debated. Method Resting-state functional magnetic resonance imaging and WMH were assessed in 78 subjects with increased amyloid levels on AV-45 positron emission tomography (PET) in different clinical stages of AD. We tested the association between WMH volume in major atlas-based fiber tract regions of interest (ROIs) and changes in functional connectivity (FC) between the tracts' projection areas within the default mode network (DMN). Results WMH volume within the inferior fronto-occipital fasciculus (IFOF) was the highest among all tract ROIs and associated with reduced FC in IFOF-connected DMN areas, independently of global AV-45 PET. Higher AV-45 PET contributed to reduced FC in IFOF-connected, temporal, and parietal DMN areas. Conclusions High fiber tract WMH burden is associated with reduced FC in connected areas, thus adding to the effects of amyloid pathology on neuronal network function.",

keywords = "Alzheimer's disease, Functional connectivity, Fibre tract, resting-state fMRI, White matter hyperintensities, vascular, amyloid-beta, Resting-state fMRI, Fiber tract, Vascular, Amyloid-beta, Humans, Male, Nerve Net/diagnostic imaging, Positron-Emission Tomography, White Matter/diagnostic imaging, Neuropsychological Tests, Magnetic Resonance Imaging, Image Processing, Computer-Assisted, Aged, 80 and over, Brain Mapping, Female, Aged, Alzheimer Disease/diagnostic imaging",

author = "Taylor, \{Alexander N. W.\} and Lana Kambeitz-Ilankovic and Benno Gesierich and Lee Simon-Vermot and Nicolai Franzmeier and \{Araque Caballero\}, \{Miguel A.\} and Sophia Meuller and Liu Hesheng and Birgit Ertl-Wagner and Katharina Beurger and Michael Weiner and Martin Dichgans and Marco Duering and Michael Ewers",

year = "2017",

month = mar,

day = "1",

doi = "10.1016/j.jalz.2016.06.2358",

language = "English",

volume = "13",

pages = "225--235",

journal = "Alzheimer's \& Dementia",

issn = "1552-5260",

publisher = "Wiley",

number = "3",

}

Taylor, ANW, Kambeitz-Ilankovic, L, Gesierich, B, Simon-Vermot, L, Franzmeier, N, Araque Caballero, MA, Meuller, S, Hesheng, L, Ertl-Wagner, B, Beurger, K, Weiner, M, Dichgans, M, Duering, M & Ewers, M 2017, 'Tract-specific white matter hyperintensities disrupt neural network function in Alzheimer’s disease', Alzheimer's & Dementia, vol. 13, no. 3, pp. 225-235. https://doi.org/10.1016/j.jalz.2016.06.2358

TY - JOUR

T1 - Tract-specific white matter hyperintensities disrupt neural network function in Alzheimer’s disease

AU - Taylor, Alexander N. W.

AU - Kambeitz-Ilankovic, Lana

AU - Gesierich, Benno

AU - Simon-Vermot, Lee

AU - Franzmeier, Nicolai

AU - Araque Caballero, Miguel A.

AU - Meuller, Sophia

AU - Hesheng, Liu

AU - Ertl-Wagner, Birgit

AU - Beurger, Katharina

AU - Weiner, Michael

AU - Dichgans, Martin

AU - Duering, Marco

AU - Ewers, Michael

PY - 2017/3/1

Y1 - 2017/3/1

N2 - Introduction White matter hyperintensities (WMHs) increase the risk of Alzheimer's disease (AD). Whether WMHs are associated with the decline of functional neural networks in AD is debated. Method Resting-state functional magnetic resonance imaging and WMH were assessed in 78 subjects with increased amyloid levels on AV-45 positron emission tomography (PET) in different clinical stages of AD. We tested the association between WMH volume in major atlas-based fiber tract regions of interest (ROIs) and changes in functional connectivity (FC) between the tracts' projection areas within the default mode network (DMN). Results WMH volume within the inferior fronto-occipital fasciculus (IFOF) was the highest among all tract ROIs and associated with reduced FC in IFOF-connected DMN areas, independently of global AV-45 PET. Higher AV-45 PET contributed to reduced FC in IFOF-connected, temporal, and parietal DMN areas. Conclusions High fiber tract WMH burden is associated with reduced FC in connected areas, thus adding to the effects of amyloid pathology on neuronal network function.

AB - Introduction White matter hyperintensities (WMHs) increase the risk of Alzheimer's disease (AD). Whether WMHs are associated with the decline of functional neural networks in AD is debated. Method Resting-state functional magnetic resonance imaging and WMH were assessed in 78 subjects with increased amyloid levels on AV-45 positron emission tomography (PET) in different clinical stages of AD. We tested the association between WMH volume in major atlas-based fiber tract regions of interest (ROIs) and changes in functional connectivity (FC) between the tracts' projection areas within the default mode network (DMN). Results WMH volume within the inferior fronto-occipital fasciculus (IFOF) was the highest among all tract ROIs and associated with reduced FC in IFOF-connected DMN areas, independently of global AV-45 PET. Higher AV-45 PET contributed to reduced FC in IFOF-connected, temporal, and parietal DMN areas. Conclusions High fiber tract WMH burden is associated with reduced FC in connected areas, thus adding to the effects of amyloid pathology on neuronal network function.

KW - Alzheimer's disease

KW - Functional connectivity

KW - Fibre tract

KW - resting-state fMRI

KW - White matter hyperintensities

KW - vascular

KW - amyloid-beta

KW - Resting-state fMRI

KW - Fiber tract

KW - Vascular

KW - Amyloid-beta

KW - Humans

KW - Male

KW - Nerve Net/diagnostic imaging

KW - Positron-Emission Tomography

KW - White Matter/diagnostic imaging

KW - Neuropsychological Tests

KW - Magnetic Resonance Imaging

KW - Image Processing, Computer-Assisted

KW - Aged, 80 and over

KW - Brain Mapping

KW - Female

KW - Aged

KW - Alzheimer Disease/diagnostic imaging

UR - https://www.scopus.com/pages/publications/85000480329

U2 - 10.1016/j.jalz.2016.06.2358

DO - 10.1016/j.jalz.2016.06.2358

M3 - Article

C2 - 27432800

SN - 1552-5260

VL - 13

SP - 225

EP - 235

JO - Alzheimer's & Dementia

JF - Alzheimer's & Dementia

IS - 3

ER -

Tract-specific white matter hyperintensities disrupt neural network function in Alzheimer’s disease

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Alexander Taylor

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Tract-specific white matter hyperintensities disrupt neural network function in Alzheimer’s disease

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