BOLD and EEG signal variability at rest differently relate to aging in the human brain

Variability of neural activity is regarded as a crucial feature of healthy brain function, and several neuroimaging approaches have been employed to assess it noninvasively. Studies on the variability of both evoked brain response and spontaneous brain signals have shown remarkable changes with agin...

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Published inNeuroImage (Orlando, Fla.) Vol. 207; p. 116373
Main Authors Kumral, D., Şansal, F., Cesnaite, E., Mahjoory, K., Al, E., Gaebler, M., Nikulin, V.V., Villringer, A.
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 15.02.2020
Elsevier Limited
Elsevier
Subjects
Adult
Age
Age differences
Aged
Aging
Aging - physiology
BOLD
Brain
Brain - pathology
Brain - physiology
Brain mapping
Brain Mapping - methods
Brain signal variability
Default mode network
EEG
Electroencephalography
Electroencephalography - methods
Female
fMRI
Functional magnetic resonance imaging
Humans
Magnetic Resonance Imaging - methods
Male
Medical imaging
Metabolism
Methods
Middle Aged
Nerve Net - pathology
Neuroimaging
Oscillations
Physiology
Resting state
Sex
Sex differences
Studies
Time series
Young Adult
fMRI
Default mode network
Resting state
EEG
Sex
Aging
BOLD
Brain signal variability
Online AccessGet full text
ISSN1053-8119
1095-9572
1095-9572
DOI10.1016/j.neuroimage.2019.116373

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Abstract Variability of neural activity is regarded as a crucial feature of healthy brain function, and several neuroimaging approaches have been employed to assess it noninvasively. Studies on the variability of both evoked brain response and spontaneous brain signals have shown remarkable changes with aging but it is unclear if the different measures of brain signal variability – identified with either hemodynamic or electrophysiological methods – reflect the same underlying physiology. In this study, we aimed to explore age differences of spontaneous brain signal variability with two different imaging modalities (EEG, fMRI) in healthy younger (25 ​± ​3 years, N ​= ​135) and older (67 ​± ​4 years, N ​= ​54) adults. Consistent with the previous studies, we found lower blood oxygenation level dependent (BOLD) variability in the older subjects as well as less signal variability in the amplitude of low-frequency oscillations (1–12 ​Hz), measured in source space. These age-related reductions were mostly observed in the areas that overlap with the default mode network. Moreover, age-related increases of variability in the amplitude of beta-band frequency EEG oscillations (15–25 ​Hz) were seen predominantly in temporal brain regions. There were significant sex differences in EEG signal variability in various brain regions while no significant sex differences were observed in BOLD signal variability. Bivariate and multivariate correlation analyses revealed no significant associations between EEG- and fMRI-based variability measures. In summary, we show that both BOLD and EEG signal variability reflect aging-related processes but are likely to be dominated by different physiological origins, which relate differentially to age and sex. •Brain signal variability obtained with resting state fMRI and EEG.•A large sample of 135 younger and 54 older adults.•Distinct age and sex differences in brain signal variability.•No significant associations between fMRI vs EEG signal variability.•Both brain variability markers may provide complementary information.
AbstractList Variability of neural activity is regarded as a crucial feature of healthy brain function, and several neuroimaging approaches have been employed to assess it noninvasively. Studies on the variability of both evoked brain response and spontaneous brain signals have shown remarkable changes with aging but it is unclear if the different measures of brain signal variability – identified with either hemodynamic or electrophysiological methods – reflect the same underlying physiology. In this study, we aimed to explore age differences of spontaneous brain signal variability with two different imaging modalities (EEG, fMRI) in healthy younger (25 ​± ​3 years, N ​= ​135) and older (67 ​± ​4 years, N ​= ​54) adults. Consistent with the previous studies, we found lower blood oxygenation level dependent (BOLD) variability in the older subjects as well as less signal variability in the amplitude of low-frequency oscillations (1–12 ​Hz), measured in source space. These age-related reductions were mostly observed in the areas that overlap with the default mode network. Moreover, age-related increases of variability in the amplitude of beta-band frequency EEG oscillations (15–25 ​Hz) were seen predominantly in temporal brain regions. There were significant sex differences in EEG signal variability in various brain regions while no significant sex differences were observed in BOLD signal variability. Bivariate and multivariate correlation analyses revealed no significant associations between EEG- and fMRI-based variability measures. In summary, we show that both BOLD and EEG signal variability reflect aging-related processes but are likely to be dominated by different physiological origins, which relate differentially to age and sex.
Variability of neural activity is regarded as a crucial feature of healthy brain function, and several neuroimaging approaches have been employed to assess it noninvasively. Studies on the variability of both evoked brain response and spontaneous brain signals have shown remarkable changes with aging but it is unclear if the different measures of brain signal variability – identified with either hemodynamic or electrophysiological methods – reflect the same underlying physiology. In this study, we aimed to explore age differences of spontaneous brain signal variability with two different imaging modalities (EEG, fMRI) in healthy younger (25 ​± ​3 years, N ​= ​135) and older (67 ​± ​4 years, N ​= ​54) adults. Consistent with the previous studies, we found lower blood oxygenation level dependent (BOLD) variability in the older subjects as well as less signal variability in the amplitude of low-frequency oscillations (1–12 ​Hz), measured in source space. These age-related reductions were mostly observed in the areas that overlap with the default mode network. Moreover, age-related increases of variability in the amplitude of beta-band frequency EEG oscillations (15–25 ​Hz) were seen predominantly in temporal brain regions. There were significant sex differences in EEG signal variability in various brain regions while no significant sex differences were observed in BOLD signal variability. Bivariate and multivariate correlation analyses revealed no significant associations between EEG- and fMRI-based variability measures. In summary, we show that both BOLD and EEG signal variability reflect aging-related processes but are likely to be dominated by different physiological origins, which relate differentially to age and sex. •Brain signal variability obtained with resting state fMRI and EEG.•A large sample of 135 younger and 54 older adults.•Distinct age and sex differences in brain signal variability.•No significant associations between fMRI vs EEG signal variability.•Both brain variability markers may provide complementary information.
Variability of neural activity is regarded as a crucial feature of healthy brain function, and several neuroimaging approaches have been employed to assess it noninvasively. Studies on the variability of both evoked brain response and spontaneous brain signals have shown remarkable changes with aging but it is unclear if the different measures of brain signal variability – identified with either hemodynamic or electrophysiological methods – reflect the same underlying physiology. In this study, we aimed to explore age differences of spontaneous brain signal variability with two different imaging modalities (EEG, fMRI) in healthy younger (25 ​± ​3 years, N ​= ​135) and older (67 ​± ​4 years, N ​= ​54) adults. Consistent with the previous studies, we found lower blood oxygenation level dependent (BOLD) variability in the older subjects as well as less signal variability in the amplitude of low-frequency oscillations (1–12 ​Hz), measured in source space. These age-related reductions were mostly observed in the areas that overlap with the default mode network. Moreover, age-related increases of variability in the amplitude of beta-band frequency EEG oscillations (15–25 ​Hz) were seen predominantly in temporal brain regions. There were significant sex differences in EEG signal variability in various brain regions while no significant sex differences were observed in BOLD signal variability. Bivariate and multivariate correlation analyses revealed no significant associations between EEG- and fMRI-based variability measures. In summary, we show that both BOLD and EEG signal variability reflect aging-related processes but are likely to be dominated by different physiological origins, which relate differentially to age and sex.
Variability of neural activity is regarded as a crucial feature of healthy brain function, and several neuroimaging approaches have been employed to assess it noninvasively. Studies on the variability of both evoked brain response and spontaneous brain signals have shown remarkable changes with aging but it is unclear if the different measures of brain signal variability - identified with either hemodynamic or electrophysiological methods - reflect the same underlying physiology. In this study, we aimed to explore age differences of spontaneous brain signal variability with two different imaging modalities (EEG, fMRI) in healthy younger (25 ​± ​3 years, N ​= ​135) and older (67 ​± ​4 years, N ​= ​54) adults. Consistent with the previous studies, we found lower blood oxygenation level dependent (BOLD) variability in the older subjects as well as less signal variability in the amplitude of low-frequency oscillations (1-12 ​Hz), measured in source space. These age-related reductions were mostly observed in the areas that overlap with the default mode network. Moreover, age-related increases of variability in the amplitude of beta-band frequency EEG oscillations (15-25 ​Hz) were seen predominantly in temporal brain regions. There were significant sex differences in EEG signal variability in various brain regions while no significant sex differences were observed in BOLD signal variability. Bivariate and multivariate correlation analyses revealed no significant associations between EEG- and fMRI-based variability measures. In summary, we show that both BOLD and EEG signal variability reflect aging-related processes but are likely to be dominated by different physiological origins, which relate differentially to age and sex.Variability of neural activity is regarded as a crucial feature of healthy brain function, and several neuroimaging approaches have been employed to assess it noninvasively. Studies on the variability of both evoked brain response and spontaneous brain signals have shown remarkable changes with aging but it is unclear if the different measures of brain signal variability - identified with either hemodynamic or electrophysiological methods - reflect the same underlying physiology. In this study, we aimed to explore age differences of spontaneous brain signal variability with two different imaging modalities (EEG, fMRI) in healthy younger (25 ​± ​3 years, N ​= ​135) and older (67 ​± ​4 years, N ​= ​54) adults. Consistent with the previous studies, we found lower blood oxygenation level dependent (BOLD) variability in the older subjects as well as less signal variability in the amplitude of low-frequency oscillations (1-12 ​Hz), measured in source space. These age-related reductions were mostly observed in the areas that overlap with the default mode network. Moreover, age-related increases of variability in the amplitude of beta-band frequency EEG oscillations (15-25 ​Hz) were seen predominantly in temporal brain regions. There were significant sex differences in EEG signal variability in various brain regions while no significant sex differences were observed in BOLD signal variability. Bivariate and multivariate correlation analyses revealed no significant associations between EEG- and fMRI-based variability measures. In summary, we show that both BOLD and EEG signal variability reflect aging-related processes but are likely to be dominated by different physiological origins, which relate differentially to age and sex.
ArticleNumber 116373
Author Kumral, D.
Cesnaite, E.
Nikulin, V.V.
Al, E.
Mahjoory, K.
Villringer, A.
Şansal, F.
Gaebler, M.
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/31759114$$D View this record in MEDLINE/PubMed
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Keywords fMRI
Default mode network
Resting state
EEG
Sex
Aging
BOLD
Brain signal variability
Language English
License This is an open access article under the CC BY-NC-ND license.
Copyright © 2019 Elsevier Inc. All rights reserved.
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Snippet Variability of neural activity is regarded as a crucial feature of healthy brain function, and several neuroimaging approaches have been employed to assess it...
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StartPage 116373
SubjectTerms Adult
Age
Age differences
Aged
Aging
Aging - physiology
BOLD
Brain
Brain - pathology
Brain - physiology
Brain mapping
Brain Mapping - methods
Brain signal variability
Default mode network
EEG
Electroencephalography
Electroencephalography - methods
Female
fMRI
Functional magnetic resonance imaging
Humans
Magnetic Resonance Imaging - methods
Male
Medical imaging
Metabolism
Methods
Middle Aged
Nerve Net - pathology
Neuroimaging
Oscillations
Physiology
Resting state
Sex
Sex differences
Studies
Time series
Young Adult
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Title BOLD and EEG signal variability at rest differently relate to aging in the human brain
URI https://www.clinicalkey.com/#!/content/1-s2.0-S1053811919309644
https://dx.doi.org/10.1016/j.neuroimage.2019.116373
https://www.ncbi.nlm.nih.gov/pubmed/31759114
https://www.proquest.com/docview/2346359905
https://www.proquest.com/docview/2317587484
https://doaj.org/article/433bb8c46e144212b6510d4477237e7d
Volume 207
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