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Published in: Brain Structure and Function 6/2022

17-05-2022 | Magnetic Resonance Imaging | Original Article

Aberrant topological organization and age-related differences in the human connectome in subjective cognitive decline by using regional morphology from magnetic resonance imaging

Authors: Zhenrong Fu, Mingyan Zhao, Yirong He, Xuetong Wang, Xin Li, Guixia Kang, Ying Han, Shuyu Li

Published in: Brain Structure and Function | Issue 6/2022

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Abstract

Subjective cognitive decline (SCD) is characterized by self-experienced deficits in cognitive capacity with normal performance in objective cognitive tests. Previous structural covariance studies showed specific insights into understanding the structural alterations of the brain in neurodegenerative diseases. Moreover, in subjects with neurodegenerative diseases, accelerated brain degeneration with aging was shown. However, the age-related variations in coordinated topological patterns of morphological networks in individuals with SCD remain poorly understood. In this study, 77 individual morphological networks were constructed, including 42 normal controls (NCs) and 35 SCD individuals, from structural magnetic resonance imaging (sMRI). A stepwise linear regression model and partial correlation analysis were constructed to evaluate the differences in age-related alterations of the network properties in individuals with SCD compared with NCs. Compared with NC, the properties of integration and segregation in individuals with SCD were lower, and the aberrant metrics were negatively correlated with age in SCD. The rich-club connections persevered, but the paralimbic system connections were disrupted in individuals with SCD compared with NCs. In addition, age-related differences in nodal global efficiency are distributed mainly in prefrontal cortex regions. In conclusion, the age-related disruption of topological organizations in individuals with SCD may indicate that the degeneration of brain efficiency with aging was accelerated in individuals with SCD.
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Literature
go back to reference Botev ZI, Grotowski JF, Kroese DP (2010) Kernel density estimation via diffusion. Ann Statist 38(5):2916–2957CrossRef Botev ZI, Grotowski JF, Kroese DP (2010) Kernel density estimation via diffusion. Ann Statist 38(5):2916–2957CrossRef
go back to reference Dozeman E, van Schaik DJ, van Marwijk HW, Stek ML, van der Horst HE, Beekman AT (2011) The center for epidemiological studies depression scale (CES-D) is an adequate screening instrument for depressive and anxiety disorders in a very old population living in residential homes. Int J Geriatr Psychiatry 26(3):239–246. https://doi.org/10.1002/gps.2519CrossRefPubMed Dozeman E, van Schaik DJ, van Marwijk HW, Stek ML, van der Horst HE, Beekman AT (2011) The center for epidemiological studies depression scale (CES-D) is an adequate screening instrument for depressive and anxiety disorders in a very old population living in residential homes. Int J Geriatr Psychiatry 26(3):239–246. https://​doi.​org/​10.​1002/​gps.​2519CrossRefPubMed
go back to reference Fu Z, Zhao M, Wang X, He Y, Tian Y, Yang Y, Han Y, Li S (2021) Altered neuroanatomical asymmetries of subcortical structures in subjective cognitive decline, amnestic mild cognitive impairment, and Alzheimer’s disease. J Alzheimer’s Dis 79(3):1121–1132. https://doi.org/10.3233/jad-201116CrossRef Fu Z, Zhao M, Wang X, He Y, Tian Y, Yang Y, Han Y, Li S (2021) Altered neuroanatomical asymmetries of subcortical structures in subjective cognitive decline, amnestic mild cognitive impairment, and Alzheimer’s disease. J Alzheimer’s Dis 79(3):1121–1132. https://​doi.​org/​10.​3233/​jad-201116CrossRef
go back to reference Gaser C, Dahnke R (2016) CAT-A computational anatomy toolbox for the Analysis of Structural MRI Data. Paper presented at the HBM Gaser C, Dahnke R (2016) CAT-A computational anatomy toolbox for the Analysis of Structural MRI Data. Paper presented at the HBM
go back to reference Guo Q, Sun Y, Yu P, Hong Z, Lv C (2007) Norm of auditory verbal learning test in the normal aged in China community [in Chinese]. Chin J Clin Psychol 15(2):132–134 Guo Q, Sun Y, Yu P, Hong Z, Lv C (2007) Norm of auditory verbal learning test in the normal aged in China community [in Chinese]. Chin J Clin Psychol 15(2):132–134
go back to reference Jack CR Jr, Bennett DA, Blennow K, Carrillo MC, Dunn B, Haeberlein SB, Holtzman DM, Jagust W, Jessen F, Karlawish J, Liu E, Molinuevo JL, Montine T, Phelps C, Rankin KP, Rowe CC, Scheltens P, Siemers E, Snyder HM, Sperling R (2018) NIA-AA Research framework: toward a biological definition of Alzheimer’s disease. Alzheimer’s Dement 14(4):535–562. https://doi.org/10.1016/j.jalz.2018.02.018CrossRef Jack CR Jr, Bennett DA, Blennow K, Carrillo MC, Dunn B, Haeberlein SB, Holtzman DM, Jagust W, Jessen F, Karlawish J, Liu E, Molinuevo JL, Montine T, Phelps C, Rankin KP, Rowe CC, Scheltens P, Siemers E, Snyder HM, Sperling R (2018) NIA-AA Research framework: toward a biological definition of Alzheimer’s disease. Alzheimer’s Dement 14(4):535–562. https://​doi.​org/​10.​1016/​j.​jalz.​2018.​02.​018CrossRef
go back to reference Jessen F, Amariglio RE, van Boxtel M, Breteler M, Ceccaldi M, Chételat G, Dubois B, Dufouil C, Ellis KA, van der Flier WM, Glodzik L, van Harten AC, de Leon MJ, McHugh P, Mielke MM, Molinuevo JL, Mosconi L, Osorio RS, Perrotin A, Petersen RC, Rabin LA, Rami L, Reisberg B, Rentz DM, Sachdev PS, de la Sayette V, Saykin AJ, Scheltens P, Shulman MB, Slavin MJ, Sperling RA, Stewart R, Uspenskaya O, Vellas B, Visser PJ, Wagner M (2014) A conceptual framework for research on subjective cognitive decline in preclinical Alzheimer’s disease. Alzheimer’s Dement 10(6):844–852. https://doi.org/10.1016/j.jalz.2014.01.001CrossRef Jessen F, Amariglio RE, van Boxtel M, Breteler M, Ceccaldi M, Chételat G, Dubois B, Dufouil C, Ellis KA, van der Flier WM, Glodzik L, van Harten AC, de Leon MJ, McHugh P, Mielke MM, Molinuevo JL, Mosconi L, Osorio RS, Perrotin A, Petersen RC, Rabin LA, Rami L, Reisberg B, Rentz DM, Sachdev PS, de la Sayette V, Saykin AJ, Scheltens P, Shulman MB, Slavin MJ, Sperling RA, Stewart R, Uspenskaya O, Vellas B, Visser PJ, Wagner M (2014) A conceptual framework for research on subjective cognitive decline in preclinical Alzheimer’s disease. Alzheimer’s Dement 10(6):844–852. https://​doi.​org/​10.​1016/​j.​jalz.​2014.​01.​001CrossRef
go back to reference Kupper LL, Stewart JR, Williams KA (1976) A note on controlling significance levels in stepwise regression. Am J Epidemiol 1:13CrossRef Kupper LL, Stewart JR, Williams KA (1976) A note on controlling significance levels in stepwise regression. Am J Epidemiol 1:13CrossRef
go back to reference Schultz SA, Oh JM, Koscik RL, Dowling NM, Gallagher CL, Carlsson CM, Bendlin BB, LaRue A, Hermann BP, Rowley HA, Asthana S, Sager MA, Johnson SC, Okonkwo OC (2015) Subjective memory complaints, cortical thinning, and cognitive dysfunction in middle-aged adults at risk for AD. Alzheimer’s Dement (Amsterdam, Netherlands) 1(1):33–40. https://doi.org/10.1016/j.dadm.2014.11.010CrossRef Schultz SA, Oh JM, Koscik RL, Dowling NM, Gallagher CL, Carlsson CM, Bendlin BB, LaRue A, Hermann BP, Rowley HA, Asthana S, Sager MA, Johnson SC, Okonkwo OC (2015) Subjective memory complaints, cortical thinning, and cognitive dysfunction in middle-aged adults at risk for AD. Alzheimer’s Dement (Amsterdam, Netherlands) 1(1):33–40. https://​doi.​org/​10.​1016/​j.​dadm.​2014.​11.​010CrossRef
go back to reference Verfaillie SCJ, Slot RER, Dicks E, Prins ND, Overbeek JM, Teunissen CE, Scheltens P, Barkhof F, van der Flier WM, Tijms BM (2018) A more randomly organized grey matter network is associated with deteriorating language and global cognition in individuals with subjective cognitive decline. Hum Brain Mapp 39(8):3143–3151. https://doi.org/10.1002/hbm.24065CrossRefPubMedPubMedCentral Verfaillie SCJ, Slot RER, Dicks E, Prins ND, Overbeek JM, Teunissen CE, Scheltens P, Barkhof F, van der Flier WM, Tijms BM (2018) A more randomly organized grey matter network is associated with deteriorating language and global cognition in individuals with subjective cognitive decline. Hum Brain Mapp 39(8):3143–3151. https://​doi.​org/​10.​1002/​hbm.​24065CrossRefPubMedPubMedCentral
go back to reference Yin RH, Tan L, Liu Y, Wang WY, Wang HF, Jiang T, Radua J, Zhang Y, Gao J, Canu E, Migliaccio R, Filippi M, Gorno-Tempini ML, Yu JT (2015) Multimodal voxel-based meta-analysis of white matter abnormalities in Alzheimer’s disease. J Alzheimer’s Dis 47(2):495–507. https://doi.org/10.3233/jad-150139CrossRef Yin RH, Tan L, Liu Y, Wang WY, Wang HF, Jiang T, Radua J, Zhang Y, Gao J, Canu E, Migliaccio R, Filippi M, Gorno-Tempini ML, Yu JT (2015) Multimodal voxel-based meta-analysis of white matter abnormalities in Alzheimer’s disease. J Alzheimer’s Dis 47(2):495–507. https://​doi.​org/​10.​3233/​jad-150139CrossRef
Metadata
Title
Aberrant topological organization and age-related differences in the human connectome in subjective cognitive decline by using regional morphology from magnetic resonance imaging
Authors
Zhenrong Fu
Mingyan Zhao
Yirong He
Xuetong Wang
Xin Li
Guixia Kang
Ying Han
Shuyu Li
Publication date
17-05-2022
Publisher
Springer Berlin Heidelberg
Published in
Brain Structure and Function / Issue 6/2022
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-022-02488-9

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