Disrupted functional and structural connectivity within default mode network contribute to WMH-related cognitive impairment

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Disconnective DMN contribute to impaired cognition

Abstract

Aims

The prevalence of white matter hyperintensities (WMH) rises dramatically with aging. Both the progression of WMH and changing patterns of default mode network (DMN) have been proven to be closely associated with cognitive function. The present study hypothesized that changes in functional connectivity and structural connectivity of DMN contributed to WMH related cognitive impairment.

Methods

A total of 116 subjects were enrolled from the Cerebral Small Vessel Disease Register in Drum Tower Hospital of Nanjing University, and were distributed across three categories according to Fazekas rating scale: WMH I ( n = 57), WMH II ( n = 34), and WMH III( n = 25). All participants underwent neuropsychological tests and multimodal MRI scans, including diffusion tensor imaging and resting-state fMRI imaging. The alterations of functional connectivity and structural connectivity within the DMN were further explored.

Results

Age and hypertension were risk factors for WMH progression. Subjects with a higher WMH burden displayed higher DMN functional connectivity in the medial frontal gyrus, while lower DMN functional connectivity in the thalamus. After adjusting for aging, gender, and education, the increased DMN functional connectivity in the medial frontal gyrus, and the increased mean diffusivity of the white matter tracts between the hippocampus and posterior cingulate cortex were independent indicators of worse performance in memory. Moreover, the decreased DMN functional connectivity in the thalamus and increased mean diffusivity of the white matter tracts between the thalamus and posterior cingulate cortex were independent risk factors for a slower processing speed.

Conclusion

The changes in functional connectivity and structural connectivity within the DMN attributed to WMH progression were responsible for the development of cognitive impairment.

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Most cited references 35

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A new rating scale for age-related white matter changes applicable to MRI and CT.

L Wahlund, F. Barkhof, F Fazekas … (2001)

MRI is more sensitive than CT for detection of age-related white matter changes (ARWMC). Most rating scales estimate the degree and distribution of ARWMC either on CT or on MRI, and they differ in many aspects. This makes it difficult to compare CT and MRI studies. To be able to study the evolution and possible effect of drug treatment on ARWMC in large patient samples, it is necessary to have a rating scale constructed for both MRI and CT. We have developed and evaluated a new scale and studied ARWMC in a large number of patients examined with both MRI and CT. Seventy-seven patients with ARWMC on either CT or MRI were recruited and a complementary examination (MRI or CT) performed. The patients came from 4 centers in Europe, and the scans were rated by 4 raters on 1 occasion with the new ARWMC rating scale. The interrater reliability was evaluated by using kappa statistics. The degree and distribution of ARWMC in CT and MRI scans were compared in different brain areas. Interrater reliability was good for MRI (kappa=0.67) and moderate for CT (kappa=0.48). MRI was superior in detection of small ARWMC, whereas larger lesions were detected equally well with both CT and MRI. In the parieto-occipital and infratentorial areas, MRI detected significantly more ARWMC than did CT. In the frontal area and basal ganglia, no differences between modalities were found. When a fluid-attenuated inversion recovery sequence was used, MRI detected significantly more lesions than CT in frontal and parieto-occipital areas. No differences were found in basal ganglia and infratentorial areas. We present a new ARWMC scale applicable to both CT and MRI that has almost equal sensitivity, except for certain regions. The interrater reliability was slightly better for MRI, as was the detectability of small lesions.

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The Human Thalamus Is an Integrative Hub for Functional Brain Networks

Kai Hwang, Maxwell A Bertolero, William Liu … (2017)

The thalamus is globally connected with distributed cortical regions, yet the functional significance of this extensive thalamocortical connectivity remains largely unknown. By performing graph-theoretic analyses on thalamocortical functional connectivity data collected from human participants, we found that most thalamic subdivisions display network properties that are capable of integrating multimodal information across diverse cortical functional networks. From a meta-analysis of a large dataset of functional brain-imaging experiments, we further found that the thalamus is involved in multiple cognitive functions. Finally, we found that focal thalamic lesions in humans have widespread distal effects, disrupting the modular organization of cortical functional networks. This converging evidence suggests that the human thalamus is a critical hub region that could integrate diverse information being processed throughout the cerebral cortex as well as maintain the modular structure of cortical functional networks. SIGNIFICANCE STATEMENT The thalamus is traditionally viewed as a passive relay station of information from sensory organs or subcortical structures to the cortex. However, the thalamus has extensive connections with the entire cerebral cortex, which can also serve to integrate information processing between cortical regions. In this study, we demonstrate that multiple thalamic subdivisions display network properties that are capable of integrating information across multiple functional brain networks. Moreover, the thalamus is engaged by tasks requiring multiple cognitive functions. These findings support the idea that the thalamus is involved in integrating information across cortical networks.

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White matter hyperintensities in vascular contributions to cognitive impairment and dementia (VCID): Knowledge gaps and opportunities

Jessica Alber, Suvarna Alladi, Hee-Joon Bae … (2019)

White matter hyperintensities (WMHs) are frequently seen on brain magnetic resonance imaging scans of older people. Usually interpreted clinically as a surrogate for cerebral small vessel disease, WMHs are associated with increased likelihood of cognitive impairment and dementia (including Alzheimer's disease [AD]). WMHs are also seen in cognitively healthy people. In this collaboration of academic, clinical, and pharmaceutical industry perspectives, we identify outstanding questions about WMHs and their relation to cognition, dementia, and AD. What molecular and cellular changes underlie WMHs? What are the neuropathological correlates of WMHs? To what extent are demyelination and inflammation present? Is it helpful to subdivide into periventricular and subcortical WMHs? What do WMHs signify in people diagnosed with AD? What are the risk factors for developing WMHs? What preventive and therapeutic strategies target WMHs? Answering these questions will improve prevention and treatment of WMHs and dementia.

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Author and article information

Contributors

Yun Xu

Journal

Journal ID (nlm-ta): Neuroimage Clin

Journal ID (iso-abbrev): Neuroimage Clin

Title: NeuroImage : Clinical

Publisher: Elsevier

ISSN (Electronic): 2213-1582

Publication date PMC-release: 12 November 2019

Publication date Collection: 2019

Publication date (Electronic): 12 November 2019

Volume: 24

Electronic Location Identifier: 102088

Affiliations

[a ]Department of Neurology, Affiliated Drum Tower Hospital, Jiangsu Key Laboratory for Molecular Medicine, Nanjing University Medical School, Nanjing, 210008, China

[b ]Jiangsu Province Stroke Center for Diagnosis and Therapy, Nanjing, 210008, China

[c ]Nanjing Neuropsychiatry Clinic Medical Center, Nanjing, 210008, China

[d ]Department of Radiology, Affiliated Drum Tower Hospital, Nanjing University Medical School, Nanjing, 210008, China

Author notes

[* ]Corresponding author at: Department of Neurology, Affiliated Drum Tower Hospital, Jiangsu Key Laboratory for Molecular Medicine, Nanjing University Medical School, Nanjing, 210008, China xuyun20042001@ 123456aliyun.com

[1]

These authors have contributed equally to this work.

Article

Publisher ID: S2213-1582(19)30435-8 Publisher ID: 102088

DOI: 10.1016/j.nicl.2019.102088

PMC ID: 6861557

PubMed ID: 31795048

SO-VID: 3246dde2-9f12-4b8a-9675-475cde720b54

License:

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

History

Date received : 8 August 2019

Date revision received : 7 November 2019

Date accepted : 9 November 2019

Disrupted functional and structural connectivity within default mode network contribute to WMH-related cognitive impairment

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Most cited references 35

A new rating scale for age-related white matter changes applicable to MRI and CT.

The Human Thalamus Is an Integrative Hub for Functional Brain Networks

White matter hyperintensities in vascular contributions to cognitive impairment and dementia (VCID): Knowledge gaps and opportunities

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