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Sustaining Attention for a Prolonged Duration Affects Dynamic Organizations of Frequency-Specific Functional Connectivity

Sustained attention encompasses a cascade of fundamental functions. The human ability to implement a sustained attention task is supported by brain networks that dynamically formed and dissolved through oscillatory synchronization. The decrement of vigilance induced by prolonged task engagement affe...

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Detalles Bibliográficos
Autores principales: Liu, Jia, Zhu, Yongjie, Sun, Hongjin, Ristaniemi, Tapani, Cong, Fengyu
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Springer US 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7593315/
https://www.ncbi.nlm.nih.gov/pubmed/32929555
http://dx.doi.org/10.1007/s10548-020-00795-0
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author Liu, Jia
Zhu, Yongjie
Sun, Hongjin
Ristaniemi, Tapani
Cong, Fengyu
author_facet Liu, Jia
Zhu, Yongjie
Sun, Hongjin
Ristaniemi, Tapani
Cong, Fengyu
author_sort Liu, Jia
collection PubMed
description Sustained attention encompasses a cascade of fundamental functions. The human ability to implement a sustained attention task is supported by brain networks that dynamically formed and dissolved through oscillatory synchronization. The decrement of vigilance induced by prolonged task engagement affects sustained attention. However, little is known about which stage or combinations are affected by vigilance decrement. Here, we applied an analysis framework composed of weighted phase lag index (wPLI) and tensor component analysis (TCA) to an EEG dataset collected during 80 min sustained attention task to examine the electrophysiological basis of such effect. We aimed to characterize the phase-coupling networks to untangle different phases involved in sustained attention and study how they are modulated by vigilance decrement. We computed the time–frequency domain wPLI from each block and subject and constructed a fourth-order tensor, containing the time, frequency, functional connectivity (FC), and blocks × subjects. This tensor was subjected to the TCA to identify the interacted and low-dimensional components representing the frequency-specific dynamic FC (fdFC). We extracted four types of neuromakers during a sustained attention task, namely the pre-stimulus alpha right-lateralized parieto-occipital FC, the post-stimulus theta fronto-parieto-occipital FC, delta fronto-parieto-occipital FC, and beta right/left sensorimotor FCs. All these fdFCs were impaired by vigilance decrement. These fdFCs, except for the beta left sensorimotor network, were restored by rewards, although the restoration by reward in the beta right sensorimotor network was transient. These findings provide implications for dissociable effects of vigilance decrement on sustained attention by utilizing the tensor-based framework. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1007/s10548-020-00795-0) contains supplementary material, which is available to authorized users.
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spelling pubmed-75933152020-11-10 Sustaining Attention for a Prolonged Duration Affects Dynamic Organizations of Frequency-Specific Functional Connectivity Liu, Jia Zhu, Yongjie Sun, Hongjin Ristaniemi, Tapani Cong, Fengyu Brain Topogr Original Paper Sustained attention encompasses a cascade of fundamental functions. The human ability to implement a sustained attention task is supported by brain networks that dynamically formed and dissolved through oscillatory synchronization. The decrement of vigilance induced by prolonged task engagement affects sustained attention. However, little is known about which stage or combinations are affected by vigilance decrement. Here, we applied an analysis framework composed of weighted phase lag index (wPLI) and tensor component analysis (TCA) to an EEG dataset collected during 80 min sustained attention task to examine the electrophysiological basis of such effect. We aimed to characterize the phase-coupling networks to untangle different phases involved in sustained attention and study how they are modulated by vigilance decrement. We computed the time–frequency domain wPLI from each block and subject and constructed a fourth-order tensor, containing the time, frequency, functional connectivity (FC), and blocks × subjects. This tensor was subjected to the TCA to identify the interacted and low-dimensional components representing the frequency-specific dynamic FC (fdFC). We extracted four types of neuromakers during a sustained attention task, namely the pre-stimulus alpha right-lateralized parieto-occipital FC, the post-stimulus theta fronto-parieto-occipital FC, delta fronto-parieto-occipital FC, and beta right/left sensorimotor FCs. All these fdFCs were impaired by vigilance decrement. These fdFCs, except for the beta left sensorimotor network, were restored by rewards, although the restoration by reward in the beta right sensorimotor network was transient. These findings provide implications for dissociable effects of vigilance decrement on sustained attention by utilizing the tensor-based framework. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1007/s10548-020-00795-0) contains supplementary material, which is available to authorized users. Springer US 2020-09-14 2020 /pmc/articles/PMC7593315/ /pubmed/32929555 http://dx.doi.org/10.1007/s10548-020-00795-0 Text en © The Author(s) 2020 Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Original Paper
Liu, Jia
Zhu, Yongjie
Sun, Hongjin
Ristaniemi, Tapani
Cong, Fengyu
Sustaining Attention for a Prolonged Duration Affects Dynamic Organizations of Frequency-Specific Functional Connectivity
title Sustaining Attention for a Prolonged Duration Affects Dynamic Organizations of Frequency-Specific Functional Connectivity
title_full Sustaining Attention for a Prolonged Duration Affects Dynamic Organizations of Frequency-Specific Functional Connectivity
title_fullStr Sustaining Attention for a Prolonged Duration Affects Dynamic Organizations of Frequency-Specific Functional Connectivity
title_full_unstemmed Sustaining Attention for a Prolonged Duration Affects Dynamic Organizations of Frequency-Specific Functional Connectivity
title_short Sustaining Attention for a Prolonged Duration Affects Dynamic Organizations of Frequency-Specific Functional Connectivity
title_sort sustaining attention for a prolonged duration affects dynamic organizations of frequency-specific functional connectivity
topic Original Paper
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7593315/
https://www.ncbi.nlm.nih.gov/pubmed/32929555
http://dx.doi.org/10.1007/s10548-020-00795-0
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