Effective connectivity in the default mode network is distinctively disrupted in Alzheimer's disease—A simultaneous resting‐state FDG‐PET/fMRI study

A prominent finding of postmortem and molecular imaging studies on Alzheimer's disease (AD) is the accumulation of neuropathological proteins in brain regions of the default mode network (DMN). Molecular models suggest that the progression of disease proteins depends on the directionality of si...

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Published inHuman brain mapping Vol. 42; no. 13; pp. 4134 - 4143
Main Authors Scherr, Martin, Utz, Lukas, Tahmasian, Masoud, Pasquini, Lorenzo, Grothe, Michel J., Rauschecker, Josef P., Grimmer, Timo, Drzezga, Alexander, Sorg, Christian, Riedl, Valentin
Format Journal Article
LanguageEnglish
Published Hoboken, USA John Wiley & Sons, Inc 01.09.2021
Subjects
Advertising executives
Aged
Alzheimer Disease - diagnostic imaging
Alzheimer Disease - metabolism
Alzheimer Disease - physiopathology
Alzheimer's disease
Brain mapping
Cerebral Cortex - diagnostic imaging
Cerebral Cortex - metabolism
Cerebral Cortex - physiopathology
Cognitive ability
Connectome - methods
Cortex (parietal)
default mode network
Default Mode Network - diagnostic imaging
Default Mode Network - metabolism
Default Mode Network - physiopathology
Development and progression
Diagnostic imaging
directional signaling
effective connectivity
energy metabolism
Functional magnetic resonance imaging
Hippocampus
Humans
Magnetic resonance imaging
Magnetic Resonance Imaging - methods
Medical imaging
Molecular modelling
Multimodal Imaging - methods
Neural networks
Neurodegenerative diseases
Neuroimaging
Positron emission
Positron emission tomography
Positron-Emission Tomography - methods
Prefrontal cortex
Proteins
resting state
Signal transduction
Signaling
simultaneous PET/fMRI
Tomography
Word of mouth advertising
simultaneous PET/fMRI
resting state
directional signaling
default mode network
energy metabolism
effective connectivity
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Abstract A prominent finding of postmortem and molecular imaging studies on Alzheimer's disease (AD) is the accumulation of neuropathological proteins in brain regions of the default mode network (DMN). Molecular models suggest that the progression of disease proteins depends on the directionality of signaling pathways. At network level, effective connectivity (EC) reflects directionality of signaling pathways. We hypothesized a specific pattern of EC in the DMN of patients with AD, related to cognitive impairment. Metabolic connectivity mapping is a novel measure of EC identifying regions of signaling input based on neuroenergetics. We simultaneously acquired resting‐state functional MRI and FDG‐PET data from patients with early AD (n = 35) and healthy subjects (n = 18) on an integrated PET/MR scanner. We identified two distinct subnetworks of EC in the DMN of healthy subjects: an anterior part with bidirectional EC between hippocampus and medial prefrontal cortex and a posterior part with predominant input into medial parietal cortex. Patients had reduced input into the medial parietal system and absent input from hippocampus into medial prefrontal cortex (p < 0.05, corrected). In a multiple linear regression with unimodal imaging and EC measures (F4,25 = 5.63, p = 0.002, r2 = 0.47), we found that EC (β = 0.45, p = 0.012) was stronger associated with cognitive deficits in patients than any of the PET and fMRI measures alone. Our approach indicates specific disruptions of EC in the DMN of patients with AD and might be suitable to test molecular theories about downstream and upstream spreading of neuropathology in AD.
AbstractList A prominent finding of postmortem and molecular imaging studies on Alzheimer's disease (AD) is the accumulation of neuropathological proteins in brain regions of the default mode network (DMN). Molecular models suggest that the progression of disease proteins depends on the directionality of signaling pathways. At network level, effective connectivity (EC) reflects directionality of signaling pathways. We hypothesized a specific pattern of EC in the DMN of patients with AD, related to cognitive impairment. Metabolic connectivity mapping is a novel measure of EC identifying regions of signaling input based on neuroenergetics. We simultaneously acquired resting‐state functional MRI and FDG‐PET data from patients with early AD ( n  = 35) and healthy subjects ( n  = 18) on an integrated PET/MR scanner. We identified two distinct subnetworks of EC in the DMN of healthy subjects: an anterior part with bidirectional EC between hippocampus and medial prefrontal cortex and a posterior part with predominant input into medial parietal cortex. Patients had reduced input into the medial parietal system and absent input from hippocampus into medial prefrontal cortex ( p  < 0.05, corrected). In a multiple linear regression with unimodal imaging and EC measures ( F 4,25  = 5.63, p  = 0.002, r 2  = 0.47), we found that EC ( β  = 0.45, p  = 0.012) was stronger associated with cognitive deficits in patients than any of the PET and fMRI measures alone. Our approach indicates specific disruptions of EC in the DMN of patients with AD and might be suitable to test molecular theories about downstream and upstream spreading of neuropathology in AD.
A prominent finding of postmortem and molecular imaging studies on Alzheimer's disease (AD) is the accumulation of neuropathological proteins in brain regions of the default mode network (DMN). Molecular models suggest that the progression of disease proteins depends on the directionality of signaling pathways. At network level, effective connectivity (EC) reflects directionality of signaling pathways. We hypothesized a specific pattern of EC in the DMN of patients with AD, related to cognitive impairment. Metabolic connectivity mapping is a novel measure of EC identifying regions of signaling input based on neuroenergetics. We simultaneously acquired resting-state functional MRI and FDG-PET data from patients with early AD (n = 35) and healthy subjects (n = 18) on an integrated PET/MR scanner. We identified two distinct subnetworks of EC in the DMN of healthy subjects: an anterior part with bidirectional EC between hippocampus and medial prefrontal cortex and a posterior part with predominant input into medial parietal cortex. Patients had reduced input into the medial parietal system and absent input from hippocampus into medial prefrontal cortex (p < 0.05, corrected). In a multiple linear regression with unimodal imaging and EC measures (F[sub.4,25] = 5.63, p = 0.002, r[sup.2] = 0.47), we found that EC (β = 0.45, p = 0.012) was stronger associated with cognitive deficits in patients than any of the PET and fMRI measures alone. Our approach indicates specific disruptions of EC in the DMN of patients with AD and might be suitable to test molecular theories about downstream and upstream spreading of neuropathology in AD.
A prominent finding of postmortem and molecular imaging studies on Alzheimer's disease (AD) is the accumulation of neuropathological proteins in brain regions of the default mode network (DMN). Molecular models suggest that the progression of disease proteins depends on the directionality of signaling pathways. At network level, effective connectivity (EC) reflects directionality of signaling pathways. We hypothesized a specific pattern of EC in the DMN of patients with AD, related to cognitive impairment. Metabolic connectivity mapping is a novel measure of EC identifying regions of signaling input based on neuroenergetics. We simultaneously acquired resting-state functional MRI and FDG-PET data from patients with early AD (n = 35) and healthy subjects (n = 18) on an integrated PET/MR scanner. We identified two distinct subnetworks of EC in the DMN of healthy subjects: an anterior part with bidirectional EC between hippocampus and medial prefrontal cortex and a posterior part with predominant input into medial parietal cortex. Patients had reduced input into the medial parietal system and absent input from hippocampus into medial prefrontal cortex (p < 0.05, corrected). In a multiple linear regression with unimodal imaging and EC measures (F4,25  = 5.63, p = 0.002, r2  = 0.47), we found that EC (β = 0.45, p = 0.012) was stronger associated with cognitive deficits in patients than any of the PET and fMRI measures alone. Our approach indicates specific disruptions of EC in the DMN of patients with AD and might be suitable to test molecular theories about downstream and upstream spreading of neuropathology in AD.A prominent finding of postmortem and molecular imaging studies on Alzheimer's disease (AD) is the accumulation of neuropathological proteins in brain regions of the default mode network (DMN). Molecular models suggest that the progression of disease proteins depends on the directionality of signaling pathways. At network level, effective connectivity (EC) reflects directionality of signaling pathways. We hypothesized a specific pattern of EC in the DMN of patients with AD, related to cognitive impairment. Metabolic connectivity mapping is a novel measure of EC identifying regions of signaling input based on neuroenergetics. We simultaneously acquired resting-state functional MRI and FDG-PET data from patients with early AD (n = 35) and healthy subjects (n = 18) on an integrated PET/MR scanner. We identified two distinct subnetworks of EC in the DMN of healthy subjects: an anterior part with bidirectional EC between hippocampus and medial prefrontal cortex and a posterior part with predominant input into medial parietal cortex. Patients had reduced input into the medial parietal system and absent input from hippocampus into medial prefrontal cortex (p < 0.05, corrected). In a multiple linear regression with unimodal imaging and EC measures (F4,25  = 5.63, p = 0.002, r2  = 0.47), we found that EC (β = 0.45, p = 0.012) was stronger associated with cognitive deficits in patients than any of the PET and fMRI measures alone. Our approach indicates specific disruptions of EC in the DMN of patients with AD and might be suitable to test molecular theories about downstream and upstream spreading of neuropathology in AD.
A prominent finding of postmortem and molecular imaging studies on Alzheimer's disease (AD) is the accumulation of neuropathological proteins in brain regions of the default mode network (DMN). Molecular models suggest that the progression of disease proteins depends on the directionality of signaling pathways. At network level, effective connectivity (EC) reflects directionality of signaling pathways. We hypothesized a specific pattern of EC in the DMN of patients with AD, related to cognitive impairment. Metabolic connectivity mapping is a novel measure of EC identifying regions of signaling input based on neuroenergetics. We simultaneously acquired resting‐state functional MRI and FDG‐PET data from patients with early AD (n = 35) and healthy subjects (n = 18) on an integrated PET/MR scanner. We identified two distinct subnetworks of EC in the DMN of healthy subjects: an anterior part with bidirectional EC between hippocampus and medial prefrontal cortex and a posterior part with predominant input into medial parietal cortex. Patients had reduced input into the medial parietal system and absent input from hippocampus into medial prefrontal cortex (p < 0.05, corrected). In a multiple linear regression with unimodal imaging and EC measures (F4,25 = 5.63, p = 0.002, r2 = 0.47), we found that EC (β = 0.45, p = 0.012) was stronger associated with cognitive deficits in patients than any of the PET and fMRI measures alone. Our approach indicates specific disruptions of EC in the DMN of patients with AD and might be suitable to test molecular theories about downstream and upstream spreading of neuropathology in AD.
A prominent finding of postmortem and molecular imaging studies on Alzheimer's disease (AD) is the accumulation of neuropathological proteins in brain regions of the default mode network (DMN). Molecular models suggest that the progression of disease proteins depends on the directionality of signaling pathways. At network level, effective connectivity (EC) reflects directionality of signaling pathways. We hypothesized a specific pattern of EC in the DMN of patients with AD, related to cognitive impairment. Metabolic connectivity mapping is a novel measure of EC identifying regions of signaling input based on neuroenergetics. We simultaneously acquired resting-state functional MRI and FDG-PET data from patients with early AD (n = 35) and healthy subjects (n = 18) on an integrated PET/MR scanner. We identified two distinct subnetworks of EC in the DMN of healthy subjects: an anterior part with bidirectional EC between hippocampus and medial prefrontal cortex and a posterior part with predominant input into medial parietal cortex. Patients had reduced input into the medial parietal system and absent input from hippocampus into medial prefrontal cortex (p < 0.05, corrected). In a multiple linear regression with unimodal imaging and EC measures (F  = 5.63, p = 0.002, r  = 0.47), we found that EC (β = 0.45, p = 0.012) was stronger associated with cognitive deficits in patients than any of the PET and fMRI measures alone. Our approach indicates specific disruptions of EC in the DMN of patients with AD and might be suitable to test molecular theories about downstream and upstream spreading of neuropathology in AD.
Audience Academic
Author Utz, Lukas
Grimmer, Timo
Drzezga, Alexander
Riedl, Valentin
Scherr, Martin
Tahmasian, Masoud
Sorg, Christian
Pasquini, Lorenzo
Rauschecker, Josef P.
Grothe, Michel J.
AuthorAffiliation 11 Department of Nuclear Medicine Technische Universität München (TUM) München Germany
3 Department of Neurology, Christian Doppler Medical Centre Paracelsus Medical University Salzburg and Centre for Cognitive Neurosciences Salzburg Austria
6 Institute of Medical Science and Technology Shahid Beheshti University Tehran Iran
9 Laboratory of Integrative Neuroscience and Cognition Georgetown University Medical Center Washington District of Columbia
4 Department of Neuroradiology Technische Universität München (TUM) München Germany
10 Department of Nuclear Medicine Uniklinik Köln Köln Germany
7 Memory and Aging Center, Department of Neurology University of California San Francisco California
8 Department for Clinical Research, German Center for Neurodegenerative Diseases (DZNE) Rostock Germany
5 Institute for Advanced Study Technische Universität München (TUM) München Germany
1 Present address: Department of Psychiatry and Psychotherapy Technische Universität München (TUM) München Germany
2 TUM‐Neu
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/30697878$$D View this record in MEDLINE/PubMed
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Issue 13
Keywords simultaneous PET/fMRI
resting state
directional signaling
default mode network
energy metabolism
effective connectivity
Language English
License 2019 Wiley Periodicals, Inc.
LinkModel DirectLink
MergedId FETCHMERGED-LOGICAL-c5107-4186a0aed38a95da8f578f463a50cdcb014e3c24fe8ac593b8c949b20cf9605b3
Notes Funding information
Bundesministerium für Bildung und Forschung, Grant/Award Number: 01EV0710; Deutsche Forschungsgemeinschaft, Grant/Award Number: 273427765; German Research Foundation, Grant/Award Number: 273427765; European Union Seventh Framework Programme, Grant/Award Number: n 291763; Technische Universität Muenchen—Institute for Advanced Study; Federal Ministry of Education and Science, Grant/Award Number: BMBF 01EV0710
ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 14
content type line 23
Martin Scherr, Lukas Utz, Christian Sorg, and Valentin Riedl authors contributed equally to this study.
Funding information Bundesministerium für Bildung und Forschung, Grant/Award Number: 01EV0710; Deutsche Forschungsgemeinschaft, Grant/Award Number: 273427765; German Research Foundation, Grant/Award Number: 273427765; European Union Seventh Framework Programme, Grant/Award Number: n 291763; Technische Universität Muenchen—Institute for Advanced Study; Federal Ministry of Education and Science, Grant/Award Number: BMBF 01EV0710
ORCID 0000-0002-8304-2876
0000-0003-2600-9022
0000-0002-2861-8449
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PublicationTitle Human brain mapping
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Snippet A prominent finding of postmortem and molecular imaging studies on Alzheimer's disease (AD) is the accumulation of neuropathological proteins in brain regions...
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SubjectTerms Advertising executives
Aged
Alzheimer Disease - diagnostic imaging
Alzheimer Disease - metabolism
Alzheimer Disease - physiopathology
Alzheimer's disease
Brain mapping
Cerebral Cortex - diagnostic imaging
Cerebral Cortex - metabolism
Cerebral Cortex - physiopathology
Cognitive ability
Connectome - methods
Cortex (parietal)
default mode network
Default Mode Network - diagnostic imaging
Default Mode Network - metabolism
Default Mode Network - physiopathology
Development and progression
Diagnostic imaging
directional signaling
effective connectivity
energy metabolism
Functional magnetic resonance imaging
Hippocampus
Humans
Magnetic resonance imaging
Magnetic Resonance Imaging - methods
Medical imaging
Molecular modelling
Multimodal Imaging - methods
Neural networks
Neurodegenerative diseases
Neuroimaging
Positron emission
Positron emission tomography
Positron-Emission Tomography - methods
Prefrontal cortex
Proteins
resting state
Signal transduction
Signaling
simultaneous PET/fMRI
Tomography
Word of mouth advertising
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Title Effective connectivity in the default mode network is distinctively disrupted in Alzheimer's disease—A simultaneous resting‐state FDG‐PET/fMRI study
URI https://onlinelibrary.wiley.com/doi/abs/10.1002%2Fhbm.24517
https://www.ncbi.nlm.nih.gov/pubmed/30697878
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Volume 42
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