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Effects of computerized cognitive training on structure‒function coupling and topology of multiple brain networks in people with mild cognitive impairment: a randomized controlled trial

BACKGROUND: People with mild cognitive impairment (MCI) experience a loss of cognitive functions, whose mechanism is characterized by aberrant structure‒function (SC-FC) coupling and topological attributes of multiple networks. This study aimed to reveal the network-level SC-FC coupling and internal...

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Autores principales: Wu, Jingsong, He, Youze, Liang, Shengxiang, Liu, Zhizhen, Huang, Jia, Liu, Weilin, Tao, Jing, Chen, Lidian, Chan, Chetwyn C. H., Lee, Tatia M. C.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10517473/
https://www.ncbi.nlm.nih.gov/pubmed/37742005
http://dx.doi.org/10.1186/s13195-023-01292-9
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author Wu, Jingsong
He, Youze
Liang, Shengxiang
Liu, Zhizhen
Huang, Jia
Liu, Weilin
Tao, Jing
Chen, Lidian
Chan, Chetwyn C. H.
Lee, Tatia M. C.
author_facet Wu, Jingsong
He, Youze
Liang, Shengxiang
Liu, Zhizhen
Huang, Jia
Liu, Weilin
Tao, Jing
Chen, Lidian
Chan, Chetwyn C. H.
Lee, Tatia M. C.
author_sort Wu, Jingsong
collection PubMed
description BACKGROUND: People with mild cognitive impairment (MCI) experience a loss of cognitive functions, whose mechanism is characterized by aberrant structure‒function (SC-FC) coupling and topological attributes of multiple networks. This study aimed to reveal the network-level SC-FC coupling and internal topological changes triggered by computerized cognitive training (CCT) to explain the therapeutic effects of this training in individuals with MCI. METHODS: In this randomized block experiment, we recruited 60 MCI individuals and randomly divided them into an 8-week multidomain CCT group and a health education control group. The neuropsychological outcome measures were the Montreal Cognitive Assessment (MoCA), Chinese Auditory Verbal Learning Test (CAVLT), Chinese Stroop Color–Word Test (SCWT), and Rey–Osterrieth Complex Figure Test (Rey CFT). The brain imaging outcome measures were SC-FC coupling and topological attributes using functional MRI and diffusion tensor imaging methods. We applied linear model analysis to assess the differences in the outcome measures and identify the correspondence between the changes in the brain networks and cognitive functions before and after the CCT. RESULTS: Fifty participants were included in the analyses after the exclusion of three dropouts and seven participants with low-quality MRI scans. Significant group × time effects were found on the changes in the MoCA, CAVLT, and Rey CFT recall scores. The changes in the SC-FC coupling values of the default mode network (DMN) and somatomotor network (SOM) were higher in the CCT group than in the control group (P(unc.) = 0.033, P(unc.) = 0.019), but opposite effects were found on the coupling values of the visual network (VIS) (P(unc.) = 0.039). Increasing clustering coefficients in the functional DMN and SOM and subtle changes in the nodal degree centrality and nodal efficiency of the right dorsal medial prefrontal cortex, posterior cingulate cortex, left parietal lobe, somatomotor area, and visual cortex were observed in the CCT group (P < 0.05, Bonferroni correction). Significant correspondences were found between global cognitive function and DMN coupling values (P(unc.) = 0.007), between immediate memory and SOM as well as FPC coupling values (P(unc.) = 0.037, P(unc.) = 0.030), between delayed memory and SOM coupling values (P(unc.) = 0.030), and between visual memory and VIS coupling values (P(unc.) = 0.007). CONCLUSIONS: Eight weeks of CCT effectively improved global cognitive and memory functions; these changes were correlated with increases in SC-FC coupling and changes in the topography of the DMN and SOM in individuals with MCI. The CCT regimen also modulated the clustering coefficient and the capacity for information transformation in functional networks; these effects appeared to underlie the cognitive improvement associated with CCT. TRIAL REGISTRATION: Chinese Clinical Trial Registry, ChiCTR2000034012. Registered on 21 June 2020. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13195-023-01292-9.
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spelling pubmed-105174732023-09-24 Effects of computerized cognitive training on structure‒function coupling and topology of multiple brain networks in people with mild cognitive impairment: a randomized controlled trial Wu, Jingsong He, Youze Liang, Shengxiang Liu, Zhizhen Huang, Jia Liu, Weilin Tao, Jing Chen, Lidian Chan, Chetwyn C. H. Lee, Tatia M. C. Alzheimers Res Ther Research BACKGROUND: People with mild cognitive impairment (MCI) experience a loss of cognitive functions, whose mechanism is characterized by aberrant structure‒function (SC-FC) coupling and topological attributes of multiple networks. This study aimed to reveal the network-level SC-FC coupling and internal topological changes triggered by computerized cognitive training (CCT) to explain the therapeutic effects of this training in individuals with MCI. METHODS: In this randomized block experiment, we recruited 60 MCI individuals and randomly divided them into an 8-week multidomain CCT group and a health education control group. The neuropsychological outcome measures were the Montreal Cognitive Assessment (MoCA), Chinese Auditory Verbal Learning Test (CAVLT), Chinese Stroop Color–Word Test (SCWT), and Rey–Osterrieth Complex Figure Test (Rey CFT). The brain imaging outcome measures were SC-FC coupling and topological attributes using functional MRI and diffusion tensor imaging methods. We applied linear model analysis to assess the differences in the outcome measures and identify the correspondence between the changes in the brain networks and cognitive functions before and after the CCT. RESULTS: Fifty participants were included in the analyses after the exclusion of three dropouts and seven participants with low-quality MRI scans. Significant group × time effects were found on the changes in the MoCA, CAVLT, and Rey CFT recall scores. The changes in the SC-FC coupling values of the default mode network (DMN) and somatomotor network (SOM) were higher in the CCT group than in the control group (P(unc.) = 0.033, P(unc.) = 0.019), but opposite effects were found on the coupling values of the visual network (VIS) (P(unc.) = 0.039). Increasing clustering coefficients in the functional DMN and SOM and subtle changes in the nodal degree centrality and nodal efficiency of the right dorsal medial prefrontal cortex, posterior cingulate cortex, left parietal lobe, somatomotor area, and visual cortex were observed in the CCT group (P < 0.05, Bonferroni correction). Significant correspondences were found between global cognitive function and DMN coupling values (P(unc.) = 0.007), between immediate memory and SOM as well as FPC coupling values (P(unc.) = 0.037, P(unc.) = 0.030), between delayed memory and SOM coupling values (P(unc.) = 0.030), and between visual memory and VIS coupling values (P(unc.) = 0.007). CONCLUSIONS: Eight weeks of CCT effectively improved global cognitive and memory functions; these changes were correlated with increases in SC-FC coupling and changes in the topography of the DMN and SOM in individuals with MCI. The CCT regimen also modulated the clustering coefficient and the capacity for information transformation in functional networks; these effects appeared to underlie the cognitive improvement associated with CCT. TRIAL REGISTRATION: Chinese Clinical Trial Registry, ChiCTR2000034012. Registered on 21 June 2020. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13195-023-01292-9. BioMed Central 2023-09-23 /pmc/articles/PMC10517473/ /pubmed/37742005 http://dx.doi.org/10.1186/s13195-023-01292-9 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This 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/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Wu, Jingsong
He, Youze
Liang, Shengxiang
Liu, Zhizhen
Huang, Jia
Liu, Weilin
Tao, Jing
Chen, Lidian
Chan, Chetwyn C. H.
Lee, Tatia M. C.
Effects of computerized cognitive training on structure‒function coupling and topology of multiple brain networks in people with mild cognitive impairment: a randomized controlled trial
title Effects of computerized cognitive training on structure‒function coupling and topology of multiple brain networks in people with mild cognitive impairment: a randomized controlled trial
title_full Effects of computerized cognitive training on structure‒function coupling and topology of multiple brain networks in people with mild cognitive impairment: a randomized controlled trial
title_fullStr Effects of computerized cognitive training on structure‒function coupling and topology of multiple brain networks in people with mild cognitive impairment: a randomized controlled trial
title_full_unstemmed Effects of computerized cognitive training on structure‒function coupling and topology of multiple brain networks in people with mild cognitive impairment: a randomized controlled trial
title_short Effects of computerized cognitive training on structure‒function coupling and topology of multiple brain networks in people with mild cognitive impairment: a randomized controlled trial
title_sort effects of computerized cognitive training on structure‒function coupling and topology of multiple brain networks in people with mild cognitive impairment: a randomized controlled trial
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10517473/
https://www.ncbi.nlm.nih.gov/pubmed/37742005
http://dx.doi.org/10.1186/s13195-023-01292-9
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