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      Dynamic functional network connectivity in patients with a mismatch between white matter hyperintensity and cognitive function

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          Abstract

          Objective

          White matter hyperintensity (WMH) in patients with cerebral small vessel disease (CSVD) is strongly associated with cognitive impairment. However, the severity of WMH does not coincide fully with cognitive impairment. This study aims to explore the differences in the dynamic functional network connectivity (dFNC) of WMH with cognitively matched and mismatched patients, to better understand the underlying mechanisms from a quantitative perspective.

          Methods

          The resting-state functional magnetic resonance imaging (rs-fMRI) and cognitive function scale assessment of the patients were acquired. Preprocessing of the rs-fMRI data was performed, and this was followed by dFNC analysis to obtain the dFNC metrics. Compared the dFNC and dFNC metrics within different states between mismatch and match group, we analyzed the correlation between dFNC metrics and cognitive function. Finally, to analyze the reasons for the differences between the mismatch and match groups, the CSVD imaging features of each patient were quantified with the assistance of the uAI Discover system.

          Results

          The 149 CSVD patients included 20 cases of “Type I mismatch,” 51 cases of Type I match, 38 cases of “Type II mismatch,” and 40 cases of “Type II match.” Using dFNC analysis, we found that the fraction time (FT) and mean dwell time (MDT) of State 2 differed significantly between “Type I match” and “Type I mismatch”; the FT of States 1 and 4 differed significantly between “Type II match” and “Type II mismatch.” Correlation analysis revealed that dFNC metrics in CSVD patients correlated with executive function and information processing speed among the various cognitive functions. Through quantitative analysis, we found that the number of perivascular spaces and bilateral medial temporal lobe atrophy (MTA) scores differed significantly between “Type I match” and “Type I mismatch,” while the left MTA score differed between “Type II match” and “Type II mismatch.”

          Conclusion

          Different mechanisms were implicated in these two types of mismatch: Type I affected higher-order networks, and may be related to the number of perivascular spaces and brain atrophy, whereas Type II affected the primary networks, and may be related to brain atrophy and the years of education.

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          Most cited references37

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          Neuroimaging standards for research into small vessel disease and its contribution to ageing and neurodegeneration

          Summary Cerebral small vessel disease (SVD) is a common accompaniment of ageing. Features seen on neuroimaging include recent small subcortical infarcts, lacunes, white matter hyperintensities, perivascular spaces, microbleeds, and brain atrophy. SVD can present as a stroke or cognitive decline, or can have few or no symptoms. SVD frequently coexists with neurodegenerative disease, and can exacerbate cognitive deficits, physical disabilities, and other symptoms of neurodegeneration. Terminology and definitions for imaging the features of SVD vary widely, which is also true for protocols for image acquisition and image analysis. This lack of consistency hampers progress in identifying the contribution of SVD to the pathophysiology and clinical features of common neurodegenerative diseases. We are an international working group from the Centres of Excellence in Neurodegeneration. We completed a structured process to develop definitions and imaging standards for markers and consequences of SVD. We aimed to achieve the following: first, to provide a common advisory about terms and definitions for features visible on MRI; second, to suggest minimum standards for image acquisition and analysis; third, to agree on standards for scientific reporting of changes related to SVD on neuroimaging; and fourth, to review emerging imaging methods for detection and quantification of preclinical manifestations of SVD. Our findings and recommendations apply to research studies, and can be used in the clinical setting to standardise image interpretation, acquisition, and reporting. This Position Paper summarises the main outcomes of this international effort to provide the STandards for ReportIng Vascular changes on nEuroimaging (STRIVE).
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            Control of goal-directed and stimulus-driven attention in the brain.

            We review evidence for partially segregated networks of brain areas that carry out different attentional functions. One system, which includes parts of the intraparietal cortex and superior frontal cortex, is involved in preparing and applying goal-directed (top-down) selection for stimuli and responses. This system is also modulated by the detection of stimuli. The other system, which includes the temporoparietal cortex and inferior frontal cortex, and is largely lateralized to the right hemisphere, is not involved in top-down selection. Instead, this system is specialized for the detection of behaviourally relevant stimuli, particularly when they are salient or unexpected. This ventral frontoparietal network works as a 'circuit breaker' for the dorsal system, directing attention to salient events. Both attentional systems interact during normal vision, and both are disrupted in unilateral spatial neglect.
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              The brain's default mode network.

              The brain's default mode network consists of discrete, bilateral and symmetrical cortical areas, in the medial and lateral parietal, medial prefrontal, and medial and lateral temporal cortices of the human, nonhuman primate, cat, and rodent brains. Its discovery was an unexpected consequence of brain-imaging studies first performed with positron emission tomography in which various novel, attention-demanding, and non-self-referential tasks were compared with quiet repose either with eyes closed or with simple visual fixation. The default mode network consistently decreases its activity when compared with activity during these relaxed nontask states. The discovery of the default mode network reignited a longstanding interest in the significance of the brain's ongoing or intrinsic activity. Presently, studies of the brain's intrinsic activity, popularly referred to as resting-state studies, have come to play a major role in studies of the human brain in health and disease. The brain's default mode network plays a central role in this work.
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                Author and article information

                Contributors
                URI : https://loop.frontiersin.org/people/2716739/overviewRole: Role: Role: Role: Role: Role:
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                Journal
                Front Aging Neurosci
                Front Aging Neurosci
                Front. Aging Neurosci.
                Frontiers in Aging Neuroscience
                Frontiers Media S.A.
                1663-4365
                17 July 2024
                2024
                : 16
                : 1418173
                Affiliations
                [1] 1Medical Imaging Center, The Affiliated Wuxi People’s Hospital of Nanjing Medical University, Wuxi Medical Center, Nanjing Medical University, Wuxi People’s Hospital , Wuxi, China
                [2] 2Department of Neurology, The Affiliated Wuxi People’s Hospital of Nanjing Medical University, Wuxi Medical Center, Nanjing Medical University, Wuxi People’s Hospital , Wuxi, China
                Author notes

                Edited by: Junhong Zhou, Harvard Medical School, United States

                Reviewed by: Cristiano Capurso, University of Foggia, Italy

                Matteo Cotta Ramusino, Neurological Institute Foundation Casimiro Mondino (IRCCS), Italy

                *Correspondence: Xiaoyun Hu, drxyh@ 123456foxmail.com
                Article
                10.3389/fnagi.2024.1418173
                11288916
                39086757
                921c3bc3-c019-49fd-9764-939c5895e224
                Copyright © 2024 Zeng, Ma, Mao, Shi, Xu, Gao, Kaidong, Li, Ding, Ji, Hu, Feng and Fang.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 16 April 2024
                : 03 July 2024
                Page count
                Figures: 5, Tables: 3, Equations: 0, References: 37, Pages: 13, Words: 7966
                Funding
                The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This study was supported by the Medical Expert Team Program of Wuxi Taihu Talent Plan 2021, 2021THRC-DJ-FXM-2023 and the Promotion Projects of Technological Achievements and Suitable Technology, T202335.
                Categories
                Aging Neuroscience
                Original Research
                Custom metadata
                Neurocognitive Aging and Behavior

                Neurosciences
                cerebral small vessel disease,resting-state functional magnetic resonance imaging,dynamic functional network connectivity,quantitative analysis,anatomy structure

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