Aberrant Multimodal Connectivity Pattern Involved in Default Mode Network and Limbic Network in Amyotrophic Lateral Sclerosis

Amyotrophic lateral sclerosis (ALS) is a neurodegenerative disorder that progressively affects bulbar and limb function. Despite increasing recognition of the disease as a multinetwork disorder characterized by aberrant structural and functional connectivity, its integrity agreement and its predicti...

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Main Authors: Haifeng Chen, Zheqi Hu, Zhihong Ke, Yun Xu, Feng Bai, Zhuo Liu
Format: Article
Language:English
Published: MDPI AG 2023-05-01
Series:Brain Sciences
Subjects:
Online Access:https://www.mdpi.com/2076-3425/13/5/803
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author Haifeng Chen
Zheqi Hu
Zhihong Ke
Yun Xu
Feng Bai
Zhuo Liu
author_facet Haifeng Chen
Zheqi Hu
Zhihong Ke
Yun Xu
Feng Bai
Zhuo Liu
author_sort Haifeng Chen
collection DOAJ
description Amyotrophic lateral sclerosis (ALS) is a neurodegenerative disorder that progressively affects bulbar and limb function. Despite increasing recognition of the disease as a multinetwork disorder characterized by aberrant structural and functional connectivity, its integrity agreement and its predictive value for disease diagnosis remain to be fully elucidated. In this study, we recruited 37 ALS patients and 25 healthy controls (HCs). High-resolution 3D T1-weighted imaging and resting-state functional magnetic resonance imaging were, respectively, applied to construct multimodal connectomes. Following strict neuroimaging selection criteria, 18 ALS and 25 HC patients were included. Network-based statistic (NBS) and the coupling of grey matter structural–functional connectivity (SC–FC coupling) were performed. Finally, the support vector machine (SVM) method was used to distinguish the ALS patients from HCs. Results showed that, compared with HCs, ALS individuals exhibited a significantly increased functional network, predominantly encompassing the connections between the default mode network (DMN) and the frontoparietal network (FPN). The increased structural connections predominantly involved the inter-regional connections between the limbic network (LN) and the DMN, the salience/ventral attention network (SVAN) and FPN, while the decreased structural connections mainly involved connections between the LN and the subcortical network (SN). We also found increased SC–FC coupling in DMN-related brain regions and decoupling in LN-related brain regions in ALS, which could differentiate ALS from HCs with promising capacity based on SVM. Our findings highlight that DMN and LN may play a vital role in the pathophysiological mechanism of ALS. Additionally, SC–FC coupling could be regarded as a promising neuroimaging biomarker for ALS and shows important clinical potential for early recognition of ALS individuals.
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spelling doaj.art-96d3e09a4c4a40e7934e781c8dc335862023-11-18T00:43:04ZengMDPI AGBrain Sciences2076-34252023-05-0113580310.3390/brainsci13050803Aberrant Multimodal Connectivity Pattern Involved in Default Mode Network and Limbic Network in Amyotrophic Lateral SclerosisHaifeng Chen0Zheqi Hu1Zhihong Ke2Yun Xu3Feng Bai4Zhuo Liu5Department of Neurology, Nanjing Drum Tower Hospital, The Affiliated Hospital of Nanjing University Medical School, Nanjing 210008, ChinaJiangsu Key Laboratory of Molecular Medicine, Medical School of Nanjing University, Nanjing 210008, ChinaJiangsu Key Laboratory of Molecular Medicine, Medical School of Nanjing University, Nanjing 210008, ChinaDepartment of Neurology, Nanjing Drum Tower Hospital, The Affiliated Hospital of Nanjing University Medical School, Nanjing 210008, ChinaDepartment of Neurology, Nanjing Drum Tower Hospital, The Affiliated Hospital of Nanjing University Medical School, Nanjing 210008, ChinaDepartment of Neurology, Nanjing Drum Tower Hospital, The Affiliated Hospital of Nanjing University Medical School, Nanjing 210008, ChinaAmyotrophic lateral sclerosis (ALS) is a neurodegenerative disorder that progressively affects bulbar and limb function. Despite increasing recognition of the disease as a multinetwork disorder characterized by aberrant structural and functional connectivity, its integrity agreement and its predictive value for disease diagnosis remain to be fully elucidated. In this study, we recruited 37 ALS patients and 25 healthy controls (HCs). High-resolution 3D T1-weighted imaging and resting-state functional magnetic resonance imaging were, respectively, applied to construct multimodal connectomes. Following strict neuroimaging selection criteria, 18 ALS and 25 HC patients were included. Network-based statistic (NBS) and the coupling of grey matter structural–functional connectivity (SC–FC coupling) were performed. Finally, the support vector machine (SVM) method was used to distinguish the ALS patients from HCs. Results showed that, compared with HCs, ALS individuals exhibited a significantly increased functional network, predominantly encompassing the connections between the default mode network (DMN) and the frontoparietal network (FPN). The increased structural connections predominantly involved the inter-regional connections between the limbic network (LN) and the DMN, the salience/ventral attention network (SVAN) and FPN, while the decreased structural connections mainly involved connections between the LN and the subcortical network (SN). We also found increased SC–FC coupling in DMN-related brain regions and decoupling in LN-related brain regions in ALS, which could differentiate ALS from HCs with promising capacity based on SVM. Our findings highlight that DMN and LN may play a vital role in the pathophysiological mechanism of ALS. Additionally, SC–FC coupling could be regarded as a promising neuroimaging biomarker for ALS and shows important clinical potential for early recognition of ALS individuals.https://www.mdpi.com/2076-3425/13/5/803amyotrophic lateral sclerosisbrain networkSC–FC couplingnetwork-based statistic
spellingShingle Haifeng Chen
Zheqi Hu
Zhihong Ke
Yun Xu
Feng Bai
Zhuo Liu
Aberrant Multimodal Connectivity Pattern Involved in Default Mode Network and Limbic Network in Amyotrophic Lateral Sclerosis
Brain Sciences
amyotrophic lateral sclerosis
brain network
SC–FC coupling
network-based statistic
title Aberrant Multimodal Connectivity Pattern Involved in Default Mode Network and Limbic Network in Amyotrophic Lateral Sclerosis
title_full Aberrant Multimodal Connectivity Pattern Involved in Default Mode Network and Limbic Network in Amyotrophic Lateral Sclerosis
title_fullStr Aberrant Multimodal Connectivity Pattern Involved in Default Mode Network and Limbic Network in Amyotrophic Lateral Sclerosis
title_full_unstemmed Aberrant Multimodal Connectivity Pattern Involved in Default Mode Network and Limbic Network in Amyotrophic Lateral Sclerosis
title_short Aberrant Multimodal Connectivity Pattern Involved in Default Mode Network and Limbic Network in Amyotrophic Lateral Sclerosis
title_sort aberrant multimodal connectivity pattern involved in default mode network and limbic network in amyotrophic lateral sclerosis
topic amyotrophic lateral sclerosis
brain network
SC–FC coupling
network-based statistic
url https://www.mdpi.com/2076-3425/13/5/803
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