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

Abstract 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...

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Main Authors: Jingsong Wu, Youze He, Shengxiang Liang, Zhizhen Liu, Jia Huang, Weilin Liu, Jing Tao, Lidian Chen, Chetwyn C. H. Chan, Tatia M. C. Lee
Format: Article
Language:English
Published: BMC 2023-09-01
Series:Alzheimer’s Research & Therapy
Subjects:
Online Access:https://doi.org/10.1186/s13195-023-01292-9
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author Jingsong Wu
Youze He
Shengxiang Liang
Zhizhen Liu
Jia Huang
Weilin Liu
Jing Tao
Lidian Chen
Chetwyn C. H. Chan
Tatia M. C. Lee
author_facet Jingsong Wu
Youze He
Shengxiang Liang
Zhizhen Liu
Jia Huang
Weilin Liu
Jing Tao
Lidian Chen
Chetwyn C. H. Chan
Tatia M. C. Lee
author_sort Jingsong Wu
collection DOAJ
description Abstract 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.
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spelling doaj.art-8aa5663af8eb4966832d69ccfe2476672023-11-19T12:35:59ZengBMCAlzheimer’s Research & Therapy1758-91932023-09-0115111310.1186/s13195-023-01292-9Effects of computerized cognitive training on structure‒function coupling and topology of multiple brain networks in people with mild cognitive impairment: a randomized controlled trialJingsong Wu0Youze He1Shengxiang Liang2Zhizhen Liu3Jia Huang4Weilin Liu5Jing Tao6Lidian Chen7Chetwyn C. H. Chan8Tatia M. C. Lee9College of Rehabilitation Medicine, Fujian University of Traditional Chinese MedicineCollege of Rehabilitation Medicine, Fujian University of Traditional Chinese MedicineThe Academy of Rehabilitation Industry, Fujian University of Traditional Chinese MedicineThe Academy of Rehabilitation Industry, Fujian University of Traditional Chinese MedicineCollege of Rehabilitation Medicine, Fujian University of Traditional Chinese MedicineThe Academy of Rehabilitation Industry, Fujian University of Traditional Chinese MedicineNational-Local Joint Engineering Research Center of Rehabilitation Medicine Technology, Fujian University of Traditional Chinese MedicineNational-Local Joint Engineering Research Center of Rehabilitation Medicine Technology, Fujian University of Traditional Chinese MedicineDepartment of Psychology, The Education University of Hong KongState Key Laboratory of Brain and Cognitive Sciences, The University of Hong KongAbstract 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.https://doi.org/10.1186/s13195-023-01292-9Mild cognitive impairmentComputerized cognitive trainingStructural‒functional couplingTopological attributeCognition
spellingShingle Jingsong Wu
Youze He
Shengxiang Liang
Zhizhen Liu
Jia Huang
Weilin Liu
Jing Tao
Lidian Chen
Chetwyn C. H. Chan
Tatia M. C. Lee
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
Alzheimer’s Research & Therapy
Mild cognitive impairment
Computerized cognitive training
Structural‒functional coupling
Topological attribute
Cognition
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 Mild cognitive impairment
Computerized cognitive training
Structural‒functional coupling
Topological attribute
Cognition
url https://doi.org/10.1186/s13195-023-01292-9
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