Classifying Vulnerability to Sleep Deprivation Using Resting-State Functional MRI Graph Theory Metrics

Sleep deprivation (SD) has become very common in contemporary society, where people work around the clock. SD-induced cognitive deficits show large inter-individual differences and are trait-like with known neural correlates. However, few studies have used neuroimaging to predict vulnerability to SD...

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Published inFrontiers in neuroscience Vol. 15; p. 660365
Main Authors Xu, Yongqiang, Yu, Ping, Zheng, Jianmin, Wang, Chen, Hu, Tian, Yang, Qi, Xu, Ziliang, Guo, Fan, Tang, Xing, Ren, Fang, Zhu, Yuanqiang
Format Journal Article
LanguageEnglish
Published Switzerland Frontiers Research Foundation 07.06.2021
Frontiers Media S.A
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ISSN1662-453X
1662-4548
1662-453X
DOI10.3389/fnins.2021.660365

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Abstract Sleep deprivation (SD) has become very common in contemporary society, where people work around the clock. SD-induced cognitive deficits show large inter-individual differences and are trait-like with known neural correlates. However, few studies have used neuroimaging to predict vulnerability to SD. Here, resting state functional magnetic resonance imaging (fMRI) data and psychomotor vigilance task (PVT) data were collected from 60 healthy subjects after resting wakefulness and after one night of SD. The number of PVT lapses was then used to classify participants on the basis of whether they were vulnerable or resilient to SD. We explored the viability of graph-theory-based degree centrality to accurately classify vulnerability to SD. Compared with during resting wakefulness, widespread changes in degree centrality (DC) were found after SD, indicating significant reorganization of sleep homeostasis with respect to activity in resting state brain network architecture. Support vector machine (SVM) analysis using leave-one-out cross-validation achieved a correct classification rate of 84.75% [sensitivity 82.76%, specificity 86.67%, and area under the receiver operating characteristic curve (AUC) 0.94] for differentiating vulnerable subjects from resilient subjects. Brain areas that contributed most to the classification model were mainly located within the sensorimotor network, default mode network, and thalamus. Furthermore, we found a significantly negative correlation between changes in PVT lapses and DC in the thalamus after SD. These findings suggest that resting-state network measures combined with a machine learning algorithm could have broad potential applications in screening vulnerability to SD.
AbstractList Sleep deprivation (SD) has become very common in contemporary society, where people work around the clock. SD-induced cognitive deficits show large inter-individual differences and are trait-like with known neural correlates. However, few studies have used neuroimaging to predict vulnerability to SD. Here, resting state functional magnetic resonance imaging (fMRI) data and psychomotor vigilance task (PVT) data were collected from 60 healthy subjects after resting wakefulness and after one night of SD. The number of PVT lapses was then used to classify participants on the basis of whether they were vulnerable or resilient to SD. We explored the viability of graph-theory-based degree centrality to accurately classify vulnerability to SD. Compared with during resting wakefulness, widespread changes in degree centrality (DC) were found after SD, indicating significant reorganization of sleep homeostasis with respect to activity in resting state brain network architecture. Support vector machine (SVM) analysis using leave-one-out cross-validation achieved a correct classification rate of 84.75% [sensitivity 82.76%, specificity 86.67%, and area under the receiver operating characteristic curve (AUC) 0.94] for differentiating vulnerable subjects from resilient subjects. Brain areas that contributed most to the classification model were mainly located within the sensorimotor network, default mode network, and thalamus. Furthermore, we found a significantly negative correlation between changes in PVT lapses and DC in the thalamus after SD. These findings suggest that resting-state network measures combined with a machine learning algorithm could have broad potential applications in screening vulnerability to SD.Sleep deprivation (SD) has become very common in contemporary society, where people work around the clock. SD-induced cognitive deficits show large inter-individual differences and are trait-like with known neural correlates. However, few studies have used neuroimaging to predict vulnerability to SD. Here, resting state functional magnetic resonance imaging (fMRI) data and psychomotor vigilance task (PVT) data were collected from 60 healthy subjects after resting wakefulness and after one night of SD. The number of PVT lapses was then used to classify participants on the basis of whether they were vulnerable or resilient to SD. We explored the viability of graph-theory-based degree centrality to accurately classify vulnerability to SD. Compared with during resting wakefulness, widespread changes in degree centrality (DC) were found after SD, indicating significant reorganization of sleep homeostasis with respect to activity in resting state brain network architecture. Support vector machine (SVM) analysis using leave-one-out cross-validation achieved a correct classification rate of 84.75% [sensitivity 82.76%, specificity 86.67%, and area under the receiver operating characteristic curve (AUC) 0.94] for differentiating vulnerable subjects from resilient subjects. Brain areas that contributed most to the classification model were mainly located within the sensorimotor network, default mode network, and thalamus. Furthermore, we found a significantly negative correlation between changes in PVT lapses and DC in the thalamus after SD. These findings suggest that resting-state network measures combined with a machine learning algorithm could have broad potential applications in screening vulnerability to SD.
Sleep deprivation (SD) has become very common in contemporary society, where people work around the clock. SD-induced cognitive deficits show large inter-individual differences and are trait-like with known neural correlates. However, few studies have used neuroimaging to predict vulnerability to SD. Here, resting state functional magnetic resonance imaging data and psychomotor vigilance task (PVT) data were collected from 60 healthy subjects after resting wakefulness and after one night of SD. The number of PVT lapses was then used to classify participants on the basis of whether they were vulnerable or resilient to SD. We explored the viability of graph-theory-based degree centrality to accurately classify vulnerability to SD. Compared with during resting wakefulness, widespread changes in degree centrality (DC) were found after SD, indicating significant reorganization of sleep homeostasis with respect to activity in resting state brain network architecture. Support Vector Machine analysis using leave-one-out cross-validation achieved a correct classification rate of 84.75% [sensitivity 82.76%, specificity 86.67%, and area under the receiver operating characteristic curve (AUC) 0.94] for differentiating vulnerable subjects from resilient subjects. Brain areas that contributed most to the classification model were mainly located within the sensorimotor network, default mode network, and thalamus. Furthermore, we found a significantly negative correlation between changes in PVT lapses and DC in the thalamus after SD. These findings suggest that resting-state network measures combined with a machine learning algorithm could have broad potential applications in screening vulnerability to SD.
Sleep deprivation (SD) has become very common in contemporary society, where people work around the clock. SD-induced cognitive deficits show large inter-individual differences and are trait-like with known neural correlates. However, few studies have used neuroimaging to predict vulnerability to SD. Here, resting state functional magnetic resonance imaging (fMRI) data and psychomotor vigilance task (PVT) data were collected from 60 healthy subjects after resting wakefulness and after one night of SD. The number of PVT lapses was then used to classify participants on the basis of whether they were vulnerable or resilient to SD. We explored the viability of graph-theory-based degree centrality to accurately classify vulnerability to SD. Compared with during resting wakefulness, widespread changes in degree centrality (DC) were found after SD, indicating significant reorganization of sleep homeostasis with respect to activity in resting state brain network architecture. Support vector machine (SVM) analysis using leave-one-out cross-validation achieved a correct classification rate of 84.75% [sensitivity 82.76%, specificity 86.67%, and area under the receiver operating characteristic curve (AUC) 0.94] for differentiating vulnerable subjects from resilient subjects. Brain areas that contributed most to the classification model were mainly located within the sensorimotor network, default mode network, and thalamus. Furthermore, we found a significantly negative correlation between changes in PVT lapses and DC in the thalamus after SD. These findings suggest that resting-state network measures combined with a machine learning algorithm could have broad potential applications in screening vulnerability to SD.
Author Yang, Qi
Tang, Xing
Zheng, Jianmin
Xu, Ziliang
Ren, Fang
Wang, Chen
Xu, Yongqiang
Guo, Fan
Yu, Ping
Hu, Tian
Zhu, Yuanqiang
AuthorAffiliation 1 Department of Radiology, Xijing Hospital, Fourth Military Medical University , Xi’an , China
2 Affiliated Wuhan Mental Health Center, Tongji Medical College, Huazhong University of Science and Technology , Wuhan , China
3 Department of Radiology, Yan’an University Affiliated Hospital , Yan’an , China
4 Department of Radiology, Affiliated Hospital of Shaanxi University of Traditional Chinese Medicine , Xianyang , China
AuthorAffiliation_xml – name: 3 Department of Radiology, Yan’an University Affiliated Hospital , Yan’an , China
– name: 1 Department of Radiology, Xijing Hospital, Fourth Military Medical University , Xi’an , China
– name: 4 Department of Radiology, Affiliated Hospital of Shaanxi University of Traditional Chinese Medicine , Xianyang , China
– name: 2 Affiliated Wuhan Mental Health Center, Tongji Medical College, Huazhong University of Science and Technology , Wuhan , China
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Copyright © 2021 Xu, Yu, Zheng, Wang, Hu, Yang, Xu, Guo, Tang, Ren and Zhu. 2021 Xu, Yu, Zheng, Wang, Hu, Yang, Xu, Guo, Tang, Ren and Zhu
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Keywords sleep deprivation
vulnerability
psychomotor vigilance task
machine learning
functional magnetic resonance imaging
Language English
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This article was submitted to Sleep and Circadian Rhythms, a section of the journal Frontiers in Neuroscience
Edited by: Leila Kheirandish-Gozal, University of Chicago, United States
Reviewed by: Kai Yuan, Xidian University, China; Yi Zhang, Xidian University, China
These authors have contributed equally to this work and share first authorship
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Snippet Sleep deprivation (SD) has become very common in contemporary society, where people work around the clock. SD-induced cognitive deficits show large...
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SubjectTerms Algorithms
Artificial intelligence
Brain architecture
Brain mapping
Classification
Cognitive ability
Functional magnetic resonance imaging
Homeostasis
Laboratories
Learning algorithms
Machine learning
Magnetic resonance imaging
Medical imaging
Neuroimaging
Neuroscience
psychomotor vigilance task
Sensorimotor system
Sleep and wakefulness
Sleep deprivation
Software
Support vector machines
Thalamus
Vigilance
vulnerability
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Title Classifying Vulnerability to Sleep Deprivation Using Resting-State Functional MRI Graph Theory Metrics
URI https://www.ncbi.nlm.nih.gov/pubmed/34163320
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https://doaj.org/article/31f77931b6ea43288de532ad0d22e14e
Volume 15
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