Neurophysiological trajectories in Alzheimer’s disease progression

Alzheimer’s disease (AD) is characterized by the accumulation of amyloid-β and misfolded tau proteins causing synaptic dysfunction, and progressive neurodegeneration and cognitive decline. Altered neural oscillations have been consistently demonstrated in AD. However, the trajectories of abnormal ne...

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Published ineLife Vol. 12
Main Authors Kudo, Kiwamu, Ranasinghe, Kamalini G, Morise, Hirofumi, Syed, Faatimah, Sekihara, Kensuke, Rankin, Katherine P, Miller, Bruce L, Kramer, Joel H, Rabinovici, Gil D, Vossel, Keith, Kirsch, Heidi E, Nagarajan, Srikantan S
Format Journal Article
LanguageEnglish
Published England eLife Sciences Publications Ltd 28.03.2024
eLife Sciences Publications, Ltd
Subjects
Alzheimer Disease
Alzheimer's disease
Amyloid beta-Peptides
Atrophy
Benchmarking
Biomarkers
Brain
Brain research
Cognition & reasoning
Cognitive ability
Dementia
Disease
electrophysiology
functional connectivity
Humans
Magnetoencephalography
Neural networks
Neurodegeneration
Neurodegenerative diseases
Neuropathology
Neuroscience
Oscillations
Sensors
Tau protein
tau Proteins
β-Amyloid
functional connectivity
electrophysiology
biomarkers
neuroscience
Alzheimer's disease
human
magnetoencephalography
Online AccessGet full text
ISSN2050-084X
2050-084X
DOI10.7554/eLife.91044

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Abstract Alzheimer’s disease (AD) is characterized by the accumulation of amyloid-β and misfolded tau proteins causing synaptic dysfunction, and progressive neurodegeneration and cognitive decline. Altered neural oscillations have been consistently demonstrated in AD. However, the trajectories of abnormal neural oscillations in AD progression and their relationship to neurodegeneration and cognitive decline are unknown. Here, we deployed robust event-based sequencing models (EBMs) to investigate the trajectories of long-range and local neural synchrony across AD stages, estimated from resting-state magnetoencephalography. The increases in neural synchrony in the delta-theta band and the decreases in the alpha and beta bands showed progressive changes throughout the stages of the EBM. Decreases in alpha and beta band synchrony preceded both neurodegeneration and cognitive decline, indicating that frequency-specific neuronal synchrony abnormalities are early manifestations of AD pathophysiology. The long-range synchrony effects were greater than the local synchrony, indicating a greater sensitivity of connectivity metrics involving multiple regions of the brain. These results demonstrate the evolution of functional neuronal deficits along the sequence of AD progression.
AbstractList Alzheimer’s disease (AD) is characterized by the accumulation of amyloid-β and misfolded tau proteins causing synaptic dysfunction, and progressive neurodegeneration and cognitive decline. Altered neural oscillations have been consistently demonstrated in AD. However, the trajectories of abnormal neural oscillations in AD progression and their relationship to neurodegeneration and cognitive decline are unknown. Here, we deployed robust event-based sequencing models (EBMs) to investigate the trajectories of long-range and local neural synchrony across AD stages, estimated from resting-state magnetoencephalography. The increases in neural synchrony in the delta-theta band and the decreases in the alpha and beta bands showed progressive changes throughout the stages of the EBM. Decreases in alpha and beta band synchrony preceded both neurodegeneration and cognitive decline, indicating that frequency-specific neuronal synchrony abnormalities are early manifestations of AD pathophysiology. The long-range synchrony effects were greater than the local synchrony, indicating a greater sensitivity of connectivity metrics involving multiple regions of the brain. These results demonstrate the evolution of functional neuronal deficits along the sequence of AD progression.
Alzheimer's disease (AD) is characterized by the accumulation of amyloid-β and misfolded tau proteins causing synaptic dysfunction, and progressive neurodegeneration and cognitive decline. Altered neural oscillations have been consistently demonstrated in AD. However, the trajectories of abnormal neural oscillations in AD progression and their relationship to neurodegeneration and cognitive decline are unknown. Here, we deployed robust event-based sequencing models (EBMs) to investigate the trajectories of long-range and local neural synchrony across AD stages, estimated from resting-state magnetoencephalography. The increases in neural synchrony in the delta-theta band and the decreases in the alpha and beta bands showed progressive changes throughout the stages of the EBM. Decreases in alpha and beta band synchrony preceded both neurodegeneration and cognitive decline, indicating that frequency-specific neuronal synchrony abnormalities are early manifestations of AD pathophysiology. The long-range synchrony effects were greater than the local synchrony, indicating a greater sensitivity of connectivity metrics involving multiple regions of the brain. These results demonstrate the evolution of functional neuronal deficits along the sequence of AD progression.Alzheimer's disease (AD) is characterized by the accumulation of amyloid-β and misfolded tau proteins causing synaptic dysfunction, and progressive neurodegeneration and cognitive decline. Altered neural oscillations have been consistently demonstrated in AD. However, the trajectories of abnormal neural oscillations in AD progression and their relationship to neurodegeneration and cognitive decline are unknown. Here, we deployed robust event-based sequencing models (EBMs) to investigate the trajectories of long-range and local neural synchrony across AD stages, estimated from resting-state magnetoencephalography. The increases in neural synchrony in the delta-theta band and the decreases in the alpha and beta bands showed progressive changes throughout the stages of the EBM. Decreases in alpha and beta band synchrony preceded both neurodegeneration and cognitive decline, indicating that frequency-specific neuronal synchrony abnormalities are early manifestations of AD pathophysiology. The long-range synchrony effects were greater than the local synchrony, indicating a greater sensitivity of connectivity metrics involving multiple regions of the brain. These results demonstrate the evolution of functional neuronal deficits along the sequence of AD progression.
Author Rabinovici, Gil D
Ranasinghe, Kamalini G
Sekihara, Kensuke
Kirsch, Heidi E
Nagarajan, Srikantan S
Morise, Hirofumi
Rankin, Katherine P
Kudo, Kiwamu
Syed, Faatimah
Kramer, Joel H
Vossel, Keith
Miller, Bruce L
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Keywords functional connectivity
electrophysiology
biomarkers
neuroscience
Alzheimer's disease
human
magnetoencephalography
Language English
License 2023, Kudo, Ranasinghe et al.
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Snippet Alzheimer’s disease (AD) is characterized by the accumulation of amyloid-β and misfolded tau proteins causing synaptic dysfunction, and progressive...
Alzheimer's disease (AD) is characterized by the accumulation of amyloid-β and misfolded tau proteins causing synaptic dysfunction, and progressive...
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SubjectTerms Alzheimer Disease
Alzheimer's disease
Amyloid beta-Peptides
Atrophy
Benchmarking
Biomarkers
Brain
Brain research
Cognition & reasoning
Cognitive ability
Dementia
Disease
electrophysiology
functional connectivity
Humans
Magnetoencephalography
Neural networks
Neurodegeneration
Neurodegenerative diseases
Neuropathology
Neuroscience
Oscillations
Sensors
Tau protein
tau Proteins
β-Amyloid
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Title Neurophysiological trajectories in Alzheimer’s disease progression
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