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

Alexander N.W. Taylor; Lana M. Kambeitz-Ilankovic; Benno Gesierich; Lee Simon-Vermot; Nicolai Franzmeier; Miguel Á. Araque Caballero; Sophia Müller; Liu Hesheng; Birgit Ertl-Wagner; Katharina Bürger; Michael W. Weiner; Martin Dichgans; Marco Duering; Michael Ewers; Alzheimer's Disease Neuroimaging Initiative

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 M. Kambeitz-Ilankovic
, Benno Gesierich
, Lee Simon-Vermot
, Nicolai Franzmeier
, Miguel Á. Araque Caballero
, Sophia Müller
, Liu Hesheng
, Birgit Ertl-Wagner
, Katharina Bürger
, Michael W. Weiner
, Martin Dichgans
, Marco Duering
, Michael Ewers
, Alzheimer's Disease Neuroimaging Initiative

School of Psychology

Research output: Contribution to journal › Article › peer-review

56 Citations (Scopus)

15 Downloads (Pure)

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 and Dementia
Volume	13
Issue number	3
Early online date	16 Jul 2016
DOIs	https://doi.org/10.1016/j.jalz.2016.06.2358
Publication status	Published - 1 Mar 2017

Keywords

Alzheimer's disease
Functional connectivity
Fiber tract
Resting-state fMRI
White matter hyperintensities
Vascular
Amyloid-beta

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10.1016/j.jalz.2016.06.2358Licence: CC BY-NC-ND

Published manuscript
This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Final published version, 1.95 MBLicence: CC BY-NC-ND

http://linkinghub.elsevier.com/retrieve/pii/S1552526016326607Licence: CC BY-NC-ND

Cite this

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

@article{ecba58b9238a4222a898297db3d11e32,

title = "Tract-specific white matter hyperintensities disrupt neural network function in Alzheimer'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, Fiber tract, Resting-state fMRI, White matter hyperintensities, Vascular, Amyloid-beta",

author = "Taylor, \{Alexander N.W.\} and Kambeitz-Ilankovic, \{Lana M.\} and Benno Gesierich and Lee Simon-Vermot and Nicolai Franzmeier and \{Araque Caballero\}, \{Miguel {\'A}.\} and Sophia M{\"u}ller and Liu Hesheng and Birgit Ertl-Wagner and Katharina B{\"u}rger and Weiner, \{Michael W.\} and Martin Dichgans and Marco Duering and Michael Ewers and \{Alzheimer's Disease Neuroimaging Initiative\}",

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day = "1",

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

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Taylor, ANW, Kambeitz-Ilankovic, LM, Gesierich, B, Simon-Vermot, L, Franzmeier, N, Araque Caballero, MÁ, Müller, S, Hesheng, L, Ertl-Wagner, B, Bürger, K, Weiner, MW, Dichgans, M, Duering, M, Ewers, M & Alzheimer's Disease Neuroimaging Initiative 2017, 'Tract-specific white matter hyperintensities disrupt neural network function in Alzheimer's disease', Alzheimer's and 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 M.

AU - Gesierich, Benno

AU - Simon-Vermot, Lee

AU - Franzmeier, Nicolai

AU - Araque Caballero, Miguel Á.

AU - Müller, Sophia

AU - Hesheng, Liu

AU - Ertl-Wagner, Birgit

AU - Bürger, Katharina

AU - Weiner, Michael W.

AU - Dichgans, Martin

AU - Duering, Marco

AU - Ewers, Michael

AU - Alzheimer's Disease Neuroimaging Initiative

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 - Fiber tract

KW - Resting-state fMRI

KW - White matter hyperintensities

KW - Vascular

KW - Amyloid-beta

U2 - 10.1016/j.jalz.2016.06.2358

DO - 10.1016/j.jalz.2016.06.2358

M3 - Article

SN - 1552-5260

VL - 13

SP - 225

EP - 235

JO - Alzheimer's and Dementia

JF - Alzheimer's and Dementia

IS - 3

ER -