Default Mode Network Lateralization and Memory in Healthy Aging and Alzheimer’s Disease

Banks, Sarah J.; Zhuang, Xiaowei; Bayram, Ece; Bird, Chris M.; Cordes, Dietmar; Caldwell, Jessica; Cummings, Jeffrey L.; Initiative, Alzheimer’s Disease Neuroimaging

doi:10.3233/jad-180541

Cited by 41 publications

(32 citation statements)

References 50 publications

(48 reference statements)

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“…As evidence suggests cortical thinning partly reflects synaptic loss [42][43][44] , critical questions for future research concern the underlying neurobiological mechanisms, exact functional consequences, and indeed whether the principle that thicker cortex thins faster only applies to homotopy. And while it remains unclear how the phenomenon may be reflected in age-related asymmetry differences in electrophysiological 45 and functional magnetic resonance signals 46,47 , our findings may be in line with studies indicating decreased left-lateralization of frontal resting-state networks with higher age 48 . Regardless, our results illustrate a hitherto undescribed phenomenon that fits within the well-established dedifferentiation view of the aging brain [3][4][5] : the mirrored reduction of leftward and rightward asymmetry across adult life suggests a system-wide breakdown in the adaptive asymmetric organization of the cortex in aging.…”

Section: Discussionsupporting

confidence: 90%

Asymmetric thinning of the cerebral cortex across the adult lifespan is accelerated in Alzheimer’s Disease

Roe

Vidal-Piñeiro

Sørensen

et al. 2020

Preprint

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Normal aging and Alzheimer's Disease (AD) are accompanied by large-scale alterations in brain organization that undermine brain function. Although hemispheric asymmetry is a global organizing feature of cortex thought to promote brain efficiency, current descriptions of cortical thinning in aging and AD have largely overlooked cortical asymmetry. Consequently, the foundational question of whether and where the cerebral hemispheres change at different rates in aging and AD remains open. First, applying vertex-wise data-driven clustering in a longitudinal discovery sample (aged 20-89; 2577 observations; 1851 longitudinal) we identified cortical regions exhibiting similar age-trajectories of asymmetry across the adult lifespan. Next, we sought replication in 4 independent longitudinal aging cohorts. We show that higher-order regions of cortex that exhibit pronounced asymmetry at age ~20 also show asymmetry change in aging. Results revealed that both leftward and rightward asymmetry is progressively lost on a similar time-scale across adult life. Hence, faster thinning of the (previously) thicker homotopic hemisphere is a feature of aging. This simple organizational principle showed high consistency across multiple aging cohorts in the Lifebrain consortium, and both the topological patterns and temporal dynamics of asymmetry-loss were markedly similar across replicating samples. Finally, we show that regions exhibiting gradual asymmetry-loss over healthy adult life exhibit faster asymmetry-change in AD.Overall, our results suggest a system-wide breakdown in the adaptive asymmetric organization of cortex across adult life which is further accelerated in AD, and may implicate thickness asymmetry as a viable marker for declining hemispheric specialization in aging and AD. The brain becomes progressively disorganized with age, and brain alterations accelerated in Alzheimer's disease may occur gradually over the lifespan. Although hemispheric asymmetry aids efficient network organization, efforts to identify structural markers of age-related decline have largely overlooked cortical asymmetry. Here we show the hemisphere that is thicker when younger, thins faster. This leads to progressive system-wide loss of regional thickness asymmetry across life. In multiple aging cohorts, asymmetry-loss showed high reproducibility topologically across cortex and similar timing-of-change in aging. Asymmetry-change was further accelerated in AD. Our findings uncover a new principle of brain aging -thicker homotopic cortex thins faster -and suggest we may have unveiled a structural marker for a widely-hypothesized decline in hemispheric specialization in aging and AD.

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Section: Discussionsupporting

confidence: 90%

Asymmetric thinning of the cerebral cortex across the adult lifespan is accelerated in Alzheimer’s Disease

Roe

Vidal-Piñeiro

Sørensen

et al. 2020

Preprint

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“…Li et al (11) found that the disruption of DMN was frequency dependent. Banks et al (12) found that left lateralization of DMN was associated with an improvement in recall performance in patients with AD. Qi et al (13) found remarkable damages to the DMN subsystems in patients with AD.…”

Section: Introductionmentioning

confidence: 99%

Changes in Brain Function Networks in Patients With Amnestic Mild Cognitive Impairment: A Resting-State fMRI Study

Wang

Liu

et al. 2020

Front. Neurol.

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Patients with amnestic mild cognitive impairment (aMCI) are at high risk of developing dementia. This study used resting-state functional magnetic resonance imaging (rs-fMRI) and an independent component analysis (ICA) approach to explore changes in functional connectivity (FC) in the default mode network (DMN), executive control network (ECN), and salience network (SN). Thirty patients with aMCI and 30 healthy controls (HCs) were enrolled. All the participants underwent an rs-fMRI scan. The brain FC in DMN, ECN, and SN was calculated using the ICA approach. We found that the FC of brain regions in DMN decreased significantly and that of brain regions in ECN increased, which was in accordance with the findings of previous studies on Alzheimer's disease (AD) and aMCI. We also found that the FC of brain regions in SN increased, which was different from the findings of previous studies on AD. The increase in FC in brain regions in SN might result from different pathophysiological states in AD and aMCI, indicating that a decrease in FC in SN does not occur in a person with aMCI. These results are consistent with those of previous studies using the voxel-mirrored homotopic connectivity approach and seed-based correlation analysis. We therefore considered that the decrease in FC in DMN and the increase in FC in ECN and SN might be peculiar patterns observed on the rs-fMRI of a person with aMCI. These findings may contribute to the development of imaging biomarkers for the diagnosis of aMCI.

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“…In recent years, resting state functional magnetic resonance imaging (rs-fMRI) has become the main means of cognitive research, while the default mode network (DMN) has been the most studied network (Cai et al, 2017; Banks et al, 2018). The DMN, anatomically distributed in different areas of the brain, can be divided into two subnetworks, the anterior and posterior subnetworks.…”

Section: Introductionmentioning

confidence: 99%

Distinct Disruptive Patterns of Default Mode Subnetwork Connectivity Across the Spectrum of Preclinical Alzheimer’s Disease

Xue

Yuan

Yue

et al. 2019

Front. Aging Neurosci.

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Background: The early progression continuum of Alzheimer’s disease (AD) has been considered to advance through subjective cognitive decline (SCD), non-amnestic mild cognitive impairment (naMCI), and amnestic mild cognitive impairment (aMCI). Altered functional connectivity (FC) in the default mode network (DMN) is regarded as a hallmark of AD. Furthermore, the DMN can be divided into two subnetworks, the anterior and posterior subnetworks. However, little is known about distinct disruptive patterns in the subsystems of the DMN across the preclinical AD spectrum. This study investigated the connectivity patterns of anterior DMN (aDMN) and posterior DMN (pDMN) across the preclinical AD spectrum.Methods: Resting-state functional magnetic resonance imaging (rs-fMRI) was used to investigate the FC in the DMN subnetworks in 20 healthy controls (HC), eight SCD, 11 naMCI, and 28 aMCI patients. Moreover, a correlation analysis was used to examine associations between the altered connectivity of the DMN subnetworks and the neurocognitive performance.Results: Compared to the HC, SCD patients showed increased FC in the bilateral superior frontal gyrus (SFG), naMCI patients showed increased FC in the left inferior parietal lobule (IPL), and aMCI patients showed increased FC in the bilateral IPL in the aDMN; while SCD patients showed decreased FC in the precuneus, naMCI patients showed increased FC in the left middle temporal gyrus (MTG), and aMCI patients also showed increased FC in the right middle frontal gyrus (MFG) in the pDMN. Notably, the FC between the ventromedial prefrontal cortex (vmPFC) and the left MFG and the IPL in the aDMN was associated with episodic memory in the SCD and aMCI groups. Interestingly, the FC between the posterior cingulated cortex (PCC) and several regions in the pDMN was associated with other cognitive functions in the SCD and naMCI groups.Conclusions: This study demonstrates that the three preclinical stages of AD exhibit distinct FC alternations in the DMN subnetworks. Furthermore, the patient group data showed that the altered FC involves cognitive function. These findings can provide novel insights for tailored clinical intervention across the preclinical AD spectrum.

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Default Mode Network Lateralization and Memory in Healthy Aging and Alzheimer’s Disease

Cited by 41 publications

References 50 publications

Asymmetric thinning of the cerebral cortex across the adult lifespan is accelerated in Alzheimer’s Disease

Asymmetric thinning of the cerebral cortex across the adult lifespan is accelerated in Alzheimer’s Disease

Changes in Brain Function Networks in Patients With Amnestic Mild Cognitive Impairment: A Resting-State fMRI Study

Distinct Disruptive Patterns of Default Mode Subnetwork Connectivity Across the Spectrum of Preclinical Alzheimer’s Disease

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