Multimodal MRI analysis of basal forebrain structure and function across the Alzheimer's disease spectrum.

Alzheimer’s Disease Cholinergic Basal Forebrain Functional Connectivity Mean Diffusivity Resting-state fMRI Subjective Cognitive Decline

Journal

NeuroImage. Clinical
ISSN: 2213-1582
Titre abrégé: Neuroimage Clin
Pays: Netherlands
ID NLM: 101597070

Informations de publication

Date de publication:
2020
Historique:
received: 03 08 2020
revised: 19 10 2020
accepted: 02 11 2020
entrez: 5 1 2021
pubmed: 6 1 2021
medline: 29 6 2021
Statut: ppublish

Résumé

Dysfunction of the cholinergic basal forebrain (cBF) is associated with cognitive decline in Alzheimer's disease (AD). Multimodal MRI allows for the investigation of cBF changes in-vivo. In this study we assessed alterations in cBF functional connectivity (FC), mean diffusivity (MD), and volume across the spectrum of AD. We further assessed effects of amyloid pathology on these changes. Participants included healthy controls, and subjects with subjective cognitive decline (SCD), mild cognitive impairment (MCI), or AD dementia (ADD) from the multicenter DELCODE study. Resting-state functional MRI (rs-fMRI) and structural MRI data was available for 477 subjects, and a subset of 243 subjects also had DTI data available. Differences between diagnostic groups were investigated using seed-based FC, volumetric, and MD analyses of functionally defined anterior (a-cBF) and posterior (p-cBF) subdivisions of a cytoarchitectonic cBF region-of-interest. In complementary analyses groups were stratified according to amyloid status based on CSF Aβ42/40 biomarker data, which was available in a subset of participants. a-cBF and p-cBF subdivisions showed regional FC profiles that were highly consistent with previously reported patterns, but there were only minimal differences between diagnostic groups. Compared to controls, cBF volumes and MD were significantly different in MCI and ADD but not in SCD. The Aβ42/40 stratified analyses largely matched these results. We reproduced subregion-specific FC profiles of the cBF in a clinical sample spanning the AD spectrum. At least in this multicentric cohort study, cBF-FC did not show marked changes along the AD spectrum, and multimodal MRI did not provide more sensitive measures of AD-related cBF changes compared to volumetry.

Sections du résumé

BACKGROUND
Dysfunction of the cholinergic basal forebrain (cBF) is associated with cognitive decline in Alzheimer's disease (AD). Multimodal MRI allows for the investigation of cBF changes in-vivo. In this study we assessed alterations in cBF functional connectivity (FC), mean diffusivity (MD), and volume across the spectrum of AD. We further assessed effects of amyloid pathology on these changes.
METHODS
Participants included healthy controls, and subjects with subjective cognitive decline (SCD), mild cognitive impairment (MCI), or AD dementia (ADD) from the multicenter DELCODE study. Resting-state functional MRI (rs-fMRI) and structural MRI data was available for 477 subjects, and a subset of 243 subjects also had DTI data available. Differences between diagnostic groups were investigated using seed-based FC, volumetric, and MD analyses of functionally defined anterior (a-cBF) and posterior (p-cBF) subdivisions of a cytoarchitectonic cBF region-of-interest. In complementary analyses groups were stratified according to amyloid status based on CSF Aβ42/40 biomarker data, which was available in a subset of participants.
RESULTS
a-cBF and p-cBF subdivisions showed regional FC profiles that were highly consistent with previously reported patterns, but there were only minimal differences between diagnostic groups. Compared to controls, cBF volumes and MD were significantly different in MCI and ADD but not in SCD. The Aβ42/40 stratified analyses largely matched these results.
CONCLUSIONS
We reproduced subregion-specific FC profiles of the cBF in a clinical sample spanning the AD spectrum. At least in this multicentric cohort study, cBF-FC did not show marked changes along the AD spectrum, and multimodal MRI did not provide more sensitive measures of AD-related cBF changes compared to volumetry.

Identifiants

pubmed: 33395986
pii: S2213-1582(20)30332-6
doi: 10.1016/j.nicl.2020.102495
pmc: PMC7689403
pii:
doi:

Types de publication

Journal Article Multicenter Study Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

102495

Informations de copyright

Copyright © 2020 The Authors. Published by Elsevier Inc. All rights reserved.

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Auteurs

Meret Herdick (M)

German Center for Neurodegenerative Diseases (DZNE), Rostock, Germany; Department of Psychosomatic Medicine, Rostock University Medical Center, Rostock, Germany.

Martin Dyrba (M)

German Center for Neurodegenerative Diseases (DZNE), Rostock, Germany.

Hans-Christian J Fritz (HJ)

German Center for Neurodegenerative Diseases (DZNE), Rostock, Germany; Department of Psychosomatic Medicine, Rostock University Medical Center, Rostock, Germany.

Slawek Altenstein (S)

German Center for Neurodegenerative Diseases (DZNE), Berlin, Germany; Department of Psychiatry and Psychotherapy, Charité, Charitéplatz 1, 10117 Berlin, Germany.

Tommaso Ballarini (T)

German Center for Neurodegenerative Diseases (DZNE), Bonn, Venusberg-Campus 1, 53127 Bonn, Germany.

Frederic Brosseron (F)

German Center for Neurodegenerative Diseases (DZNE), Bonn, Venusberg-Campus 1, 53127 Bonn, Germany; Department for Neurodegenerative Diseases and Geriatric Psychiatry, University Hospital Bonn, Venusberg-Campus 1, 53127 Bonn, Germany.

Katharina Buerger (K)

German Center for Neurodegenerative Diseases (DZNE, Munich), Feodor-Lynen-Strasse 17, 81377 Munich, Germany; Institute for Stroke and Dementia Research (ISD), University Hospital, LMU Munich, Feodor-Lynen-Strasse 17, 81377 Munich, Germany.

Arda Can Cetindag (A)

Charité - Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Institute of Psychiatry and Psychotherapy, Hindenburgdamm 30, 12203 Berlin, Germany.

Peter Dechent (P)

MR-Research in Neurology and Psychiatry, Georg-August-University Göttingen, Germany.

Laura Dobisch (L)

German Center for Neurodegenerative Diseases (DZNE), Magdeburg, Germany.

Emrah Duezel (E)

German Center for Neurodegenerative Diseases (DZNE), Magdeburg, Germany; Institute of Cognitive Neurology and Dementia Research (IKND), Otto-von-Guericke University, Magdeburg, Germany.

Birgit Ertl-Wagner (B)

Institute for Clinical Radiology, Ludwig-Maximilians-University, Marchioninistr. 15, 81377 Munich, Germany.

Klaus Fliessbach (K)

German Center for Neurodegenerative Diseases (DZNE), Bonn, Venusberg-Campus 1, 53127 Bonn, Germany; Department for Neurodegenerative Diseases and Geriatric Psychiatry, University Hospital Bonn, Venusberg-Campus 1, 53127 Bonn, Germany.

Silka Dawn Freiesleben (S)

Charité - Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Institute of Psychiatry and Psychotherapy, Hindenburgdamm 30, 12203 Berlin, Germany.

Ingo Frommann (I)

German Center for Neurodegenerative Diseases (DZNE), Bonn, Venusberg-Campus 1, 53127 Bonn, Germany.

Wenzel Glanz (W)

German Center for Neurodegenerative Diseases (DZNE), Magdeburg, Germany.

John Dylan Haynes (J)

Bernstein Center for Computational Neuroscience, Charité - Universitätsmedizin, Berlin, Germany.

Michael T Heneka (MT)

German Center for Neurodegenerative Diseases (DZNE), Bonn, Venusberg-Campus 1, 53127 Bonn, Germany; Department for Neurodegenerative Diseases and Geriatric Psychiatry, University Hospital Bonn, Venusberg-Campus 1, 53127 Bonn, Germany.

Daniel Janowitz (D)

Institute for Stroke and Dementia Research (ISD), University Hospital, LMU Munich, Feodor-Lynen-Strasse 17, 81377 Munich, Germany.

Ingo Kilimann (I)

German Center for Neurodegenerative Diseases (DZNE), Rostock, Germany; Department of Psychosomatic Medicine, Rostock University Medical Center, Rostock, Germany.

Christoph Laske (C)

German Center for Neurodegenerative Diseases (DZNE), Tübingen, Germany; Section for Dementia Research, Hertie Institute for Clinical Brain Research and Department of Psychiatry and Psychotherapy, University of Tübingen, Tübingen, Germany.

Coraline D Metzger (CD)

German Center for Neurodegenerative Diseases (DZNE), Magdeburg, Germany; Institute of Cognitive Neurology and Dementia Research (IKND), Otto-von-Guericke University, Magdeburg, Germany; Department of Psychiatry and Psychotherapy, Otto-von-Guericke University, Magdeburg, Germany.

Matthias H Munk (MH)

German Center for Neurodegenerative Diseases (DZNE), Tübingen, Germany; Section for Dementia Research, Hertie Institute for Clinical Brain Research and Department of Psychiatry and Psychotherapy, University of Tübingen, Tübingen, Germany.

Oliver Peters (O)

German Center for Neurodegenerative Diseases (DZNE), Berlin, Germany; Charité - Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Institute of Psychiatry and Psychotherapy, Hindenburgdamm 30, 12203 Berlin, Germany.

Josef Priller (J)

German Center for Neurodegenerative Diseases (DZNE), Berlin, Germany; Department of Psychiatry and Psychotherapy, Charité, Charitéplatz 1, 10117 Berlin, Germany.

Nina Roy (N)

German Center for Neurodegenerative Diseases (DZNE), Bonn, Venusberg-Campus 1, 53127 Bonn, Germany.

Klaus Scheffler (K)

Department for Biomedical Magnetic Resonance, University of Tübingen, 72076 Tübingen, Germany.

Anja Schneider (A)

German Center for Neurodegenerative Diseases (DZNE), Bonn, Venusberg-Campus 1, 53127 Bonn, Germany; Department for Neurodegenerative Diseases and Geriatric Psychiatry, University Hospital Bonn, Venusberg-Campus 1, 53127 Bonn, Germany.

Annika Spottke (A)

German Center for Neurodegenerative Diseases (DZNE), Bonn, Venusberg-Campus 1, 53127 Bonn, Germany; Department of Neurology, University of Bonn, Venusberg-Campus 1, 53127 Bonn, Germany.

Eike Jakob Spruth (E)

German Center for Neurodegenerative Diseases (DZNE), Berlin, Germany; Department of Psychiatry and Psychotherapy, Charité, Charitéplatz 1, 10117 Berlin, Germany.

Maike Tscheuschler (M)

Department of Psychiatry, University of Cologne, Medical Faculty, Kerpener Strasse 62, 50924 Cologne, Germany.

Ruth Vukovich (R)

Department of Psychiatry and Psychotherapy, University Medical Center Goettingen, University of Goettingen, Von-Siebold-Str. 5, 37075 Goettingen, Germany.

Jens Wiltfang (J)

Department of Psychiatry and Psychotherapy, University Medical Center Goettingen, University of Goettingen, Von-Siebold-Str. 5, 37075 Goettingen, Germany; German Center for Neurodegenerative Diseases (DZNE), Goettingen, Germany; Neurosciences and Signaling Group, Institute of Biomedicine (iBiMED), Department of Medical Sciences, University of Aveiro, Aveiro, Portugal.

Frank Jessen (F)

German Center for Neurodegenerative Diseases (DZNE), Bonn, Venusberg-Campus 1, 53127 Bonn, Germany; Department of Psychiatry, University of Cologne, Medical Faculty, Kerpener Strasse 62, 50924 Cologne, Germany; Excellence Cluster on Cellular Stress Responses in Aging-Associated Diseases (CECAD), University of Cologne, Joseph-Stelzmann-Strasse 26, 50931Köln, Germany.

Stefan Teipel (S)

German Center for Neurodegenerative Diseases (DZNE), Rostock, Germany; Department of Psychosomatic Medicine, Rostock University Medical Center, Rostock, Germany. Electronic address: stefan.teipel@med.uni-rostock.de.

Michel J Grothe (MJ)

German Center for Neurodegenerative Diseases (DZNE), Rostock, Germany; Unidad de Trastornos del Movimiento, Servicio de Neurología y Neurofisiología Clínica, Instituto de Biomedicina de Sevilla, Hospital Universitario Virgen del Rocío/CSIC/Universidad de Sevilla, Seville, Spain. Electronic address: michel.grothe@dzne.de.

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