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 in | Frontiers in neuroscience Vol. 15; p. 660365 |
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Main Authors | , , , , , , , , , , |
Format | Journal Article |
Language | English |
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07.06.2021
Frontiers Media S.A |
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ISSN | 1662-453X 1662-4548 1662-453X |
DOI | 10.3389/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. |
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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 |
Author_xml | – sequence: 1 givenname: Yongqiang surname: Xu fullname: Xu, Yongqiang – sequence: 2 givenname: Ping surname: Yu fullname: Yu, Ping – sequence: 3 givenname: Jianmin surname: Zheng fullname: Zheng, Jianmin – sequence: 4 givenname: Chen surname: Wang fullname: Wang, Chen – sequence: 5 givenname: Tian surname: Hu fullname: Hu, Tian – sequence: 6 givenname: Qi surname: Yang fullname: Yang, Qi – sequence: 7 givenname: Ziliang surname: Xu fullname: Xu, Ziliang – sequence: 8 givenname: Fan surname: Guo fullname: Guo, Fan – sequence: 9 givenname: Xing surname: Tang fullname: Tang, Xing – sequence: 10 givenname: Fang surname: Ren fullname: Ren, Fang – sequence: 11 givenname: Yuanqiang surname: Zhu fullname: Zhu, Yuanqiang |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/34163320$$D View this record in MEDLINE/PubMed |
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Copyright | Copyright © 2021 Xu, Yu, Zheng, Wang, Hu, Yang, Xu, Guo, Tang, Ren, Zheng and Zhu. 2021. This work is licensed under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. 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 |
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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 |
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