Connectome-based predictive modelling of ageing, overall cognitive functioning and memory performance.

Item request has been placed! ×
Item request cannot be made. ×
loading   Processing Request
  • Additional Information
    • Corporate Authors:
    • Source:
      Publisher: Wiley-Blackwell Country of Publication: France NLM ID: 8918110 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1460-9568 (Electronic) Linking ISSN: 0953816X NLM ISO Abbreviation: Eur J Neurosci Subsets: MEDLINE
    • Publication Information:
      Publication: : Oxford : Wiley-Blackwell
      Original Publication: Oxford, UK : Published on behalf of the European Neuroscience Association by Oxford University Press, c1989-
    • Subject Terms:
    • Abstract:
      Resting-state functional magnetic resonance imaging (rs-fMRI) and brain functional connectome (we use 'brain connectome' hereafter for simplicity) have advanced our understanding of the ageing brain and age-related changes in cognitive function. Previous studies have investigated the association among brain connectome and age, global cognition, and memory function separately. However, very few have predicted age, overall cognitive functioning and memory performance in a single study to better understand their complex relationship. In this cross-sectional study, we applied an exploratory, data-driven method to investigate the brain connectome markers that could predict ageing, overall cognitive functioning assessed as intelligence quotient (IQ, measured by Wechsler Memory Scale) and memory performance assessed as memory quotient (MQ, measured by Wechsler Memory Scale) in a carefully designed, multicentre, normal ageing cohort (n = 313). Our results showed that brain connectome could predict ageing and IQ, but the association with MQ was weak. We found that the connectivity with orbital frontal cortex was associated with both ageing and IQ. Mediation analysis further showed that the brain connectome mediated the relationship between age and overall cognitive functioning, suggesting a protective brain connectomic mechanism for maintaining normal cognitive functions during healthy ageing. This work may shed light on the potential neural correlates of healthy ageing, overall cognitive functioning and memory performance.
      (© 2024 Federation of European Neuroscience Societies and John Wiley & Sons Ltd.)
    • References:
      Alfaro‐Almagro, F., Jenkinson, M., Bangerter, N. K., Andersson, J. L. R., Griffanti, L., Douaud, G., Sotiropoulos, S. N., Jbabdi, S., Hernandez‐Fernandez, M., Vallee, E., Vidaurre, D., Webster, M., McCarthy, P., Rorden, C., Daducci, A., Alexander, D. C., Zhang, H., Dragonu, I., Matthews, P. M., … Smith, S. M. (2018). Image processing and quality control for the first 10,000 brain imaging datasets from UK biobank. NeuroImage, 166, 400–424. https://doi.org/10.1016/j.neuroimage.2017.10.034.
      Allen, H. A., & Roberts, K. L. (2016). Editorial: Perception and cognition: Interactions in the aging brain. Frontiers in Aging Neuroscience, 8, 130. https://doi.org/10.3389/fnagi.2016.00130.
      Andrews‐Hanna, J. R., Snyder, A. Z., Vincent, J. L., Lustig, C., Head, D., Raichle, M., & Buckner, R. L. (2007). Disruption of large‐scale brain systems in advanced aging. Neuron, 56(5), 924–935. https://doi.org/10.1016/j.neuron.2007.10.038.
      Attems, J., Walker, L., & Jellinger, K. A. (2015). Olfaction and aging: A mini‐review. Gerontology (Basel), 61(6), 485–490.
      Boyle, P. A., Wilson, R. S., Yu, L., Barr, A. M., Honer, W. G., Schneider, J. A., & Bennett, D. A. (2013). Much of late life cognitive decline is not due to common neurodegenerative pathologies. Annals of Neurology, 74(3), 478–489. https://doi.org/10.1002/ana.23964.
      Boyle, R., Connaughton, M., McGlinchey, E., Knight, S. P., De Looze, C., Carey, D., & Whelan, R. (2023). Connectome‐based predictive modelling of cognitive reserve using task‐based functional connectivity. European Journal of Neuroscience, 57(3), 490–510. https://doi.org/10.1111/ejn.15896.
      Chen, Q., Xia, Y., Zhuang, K., Wu, X., Liu, G., & Qiu, J. (2019). Decreased inter‐hemispheric interactions but increased intra‐hemispheric integration during typical aging. Aging (Albany, NY), 11(22), 10100–10115, https://doi.org/10.18632/aging.102421.
      Cole, M. W., Yarkoni, T., Repovs, G., Anticevic, A., & Braver, T. S. (2012). Global connectivity of prefrontal cortex predicts cognitive control and intelligence. The Journal of Neuroscience, 32(26), 8988–8999. https://doi.org/10.1523/JNEUROSCI.0536-12.2012.
      Crinion, J., Turner, R., Grogan, A., Hanakawa, T., Noppeney, U., Devlin, J. T., Aso, T., Urayama, S., Fukuyama, H., Stockton, K., Usui, K., Green, D. W., & Price, C. J. (2006). Language control in the bilingual brain. Science, 312(5779), 1537–1540. https://doi.org/10.1126/science.1127761.
      Damoiseaux, J., Beckmann, C., Arigita, E. S., Barkhof, F., Scheltens, P., Stam, C., … Rombouts, S. (2007). Reduced resting‐state brain activity in the “default network” in normal aging. Cerebral Cortex, 18(8), 1856–1864. https://doi.org/10.1093/cercor/bhm207.
      Deary, I. J., Whalley, L. J., Lemmon, H., Crawford, J. R., & Starr, J. M. (2000). The stability of individual differences in mental ability from childhood to old age: Follow‐up of the 1932 Scottish mental survey. Intelligence, 28(1), 49–55. https://doi.org/10.1016/S0160-2896(99)00031-8.
      Efklides, A., Yiultsi, E., Kangellidou, T., Kounti, F., Dina, F., & Tsolaki, M. (2002). Wechsler memory scale, Rivermead behavioral memory test, and everyday memory questionnaire in healthy adults and Alzheimer's patients. European Journal of Psychological Assessment: Official Organ of the European Association of Psychological Assessment, 18(1), 63–77. https://doi.org/10.1027//1015-5759.18.1.63.
      Ferreira, L. K., & Busatto, G. F. (2013). Resting‐state functional connectivity in normal brain aging. Neuroscience and Biobehavioral Reviews, 37(3), 384–400. https://doi.org/10.1016/j.neubiorev.2013.01.017.
      Fitzhugh, M. C., Hemesath, A., Schaefer, S. Y., Baxter, L. C., & Rogalsky, C. (2019). Functional connectivity of Heschl's gyrus associated with age‐related hearing loss: A resting‐state fMRI study. Frontiers in Psychology, 10, 2485. https://doi.org/10.3389/fpsyg.2019.02485.
      Friston, K. J., Williams, S., Howard, R., Frackowiak, R. S., & Turner, R. (1996). Movement‐related effects in fMRI time‐series. Magnetic Resonance in Medicine, 35(3), 346–355. https://doi.org/10.1002/mrm.1910350312.
      Gluhm, S., Goldstein, J., Loc, K., Colt, A., Liew, C. V., & Corey‐Bloom, J. (2013). Cognitive performance on the mini‐mental state examination and the Montreal cognitive assessment across the healthy adult lifespan. Cognitive and Behavioral Neurology, 26(1), 1–5. https://doi.org/10.1097/WNN.0b013e31828b7d26.
      Gong, Y. X. (1982). Manual, for the Wechsler adult intelligence scale: Chinese revision. Hunan Medical College.
      Gong, Y. X. (1989). Manual, for the Wechsler adult intelligence scale: Chinese revision. Hunan Medical College.
      Gow, A. J., Johnson, W., Pattie, A., Brett, C. E., Roberts, B., Starr, J. M., & Deary, I. J. (2011). Stability and change in intelligence from age 11 to ages 70, 79, and 87: The Lothian birth cohorts of 1921 and 1936. Psychology and Aging, 26(1), 232–240. https://doi.org/10.1037/a0021072.
      Grahn, J. A., Parkinson, J. A., & Owen, A. M. (2008). The cognitive functions of the caudate nucleus. Progress in Neurobiology, 86(3), 141–155. https://doi.org/10.1016/j.pneurobio.2008.09.004.
      Grazioplene, R. G. G., Ryman, S., Gray, J. R., Rustichini, A., Jung, R. E., & DeYoung, C. G. (2015). Subcortical intelligence: Caudate volume predicts IQ in healthy adults. Human Brain Mapping, 36(4), 1407–1416. https://doi.org/10.1002/hbm.22710.
      Haier, R. J., Jung, R. E., Yeo, R. A., Head, K., & Alkire, M. T. (2005). The neuroanatomy of general intelligence: Sex matters. NeuroImage, 25(1), 320–327. https://doi.org/10.1016/j.neuroimage.2004.11.019.
      Hayes, A. F. (2022). Introduction to mediation, moderation, and conditional process analysis: A regression‐based approach (Third ed.). The Guilford Press.
      Hedden, T., & Gabrieli, J. D. E. (2004). Insights into the ageing mind: A view from cognitive neuroscience. Nature Reviews. Neuroscience, 5(2), 87–96. https://doi.org/10.1038/nrn1323.
      Jiang, R., Calhoun, V. D., Fan, L., Zuo, N., Jung, R., Qi, S., Lin, D., Li, J., Zhuo, C., Song, M., Fu, Z., Jiang, T., & Sui, J. (2020). Gender differences in connectome‐based predictions of individualized intelligence quotient and sub‐domain scores. Cerebral Cortex, 30(3), 888–900. https://doi.org/10.1093/cercor/bhz134.
      Kareken, D. A., Mosnik, D. M., Doty, R. L., Dzemidzic, M., & Hutchins, G. D. (2003). Functional anatomy of human odor sensation, discrimination, and identification in health and aging. Neuropsychology, 17(3), 482–495. https://doi.org/10.1037/0894-4105.17.3.482.
      Karunanayaka, P. R., Wilson, D. A., Tobia, M. J., Martinez, B. E., Meadowcroft, M. D., Eslinger, P. J., & Yang, Q. X. (2017). Default mode network deactivation during odor–visual association. Human Brain Mapping, 38(3), 1125‐1139. https://doi.org/10.1002/hbm.23440.
      Kovacs, T. (2004). Mechanisms of olfactory dysfunction in aging and neurodegenerative disorders. Ageing Research Reviews, 3(2), 215–232. https://doi.org/10.1016/j.arr.2003.10.003.
      La Corte, V., Sperduti, M., Malherbe, C., Vialatte, F., Lion, S., Gallarda, T., Oppenheim, C., & Piolino, P. (2016). Cognitive decline and reorganization of functional connectivity in healthy aging: The pivotal role of the salience network in the prediction of age and cognitive performances. Frontiers in Aging Neuroscience, 8, 204. https://doi.org/10.3389/fnagi.2016.00204.
      Luck, D., Danion, J., Marrer, C., Pham, B., Gounot, D., & Foucher, J. (2010). The right parahippocampal gyrus contributes to the formation and maintenance of bound information in working memory. Brain and Cognition, 72(2), 255–263. https://doi.org/10.1016/j.bandc.2009.09.009.
      Maddock, R. J., Garrett, A. S., & Buonocore, M. H. (2001). Remembering familiar people: The posterior cingulate cortex and autobiographical memory retrieval. Neuroscience, 104(3), 667–676. https://doi.org/10.1016/S0306-4522(01)00108-7.
      Madhyastha, T. M., & Grabowski, T. J. (2014). Age‐related differences in the dynamic architecture of intrinsic networks. Brain Connectivity, 4(4), 231–241. https://doi.org/10.1089/brain.2013.0205.
      Manglani, H. R., Fountain‐Zaragoza, S., Shankar, A., Nicholas, J. A., & Prakash, R. S. (2022). Employing connectome‐based models to predict working memory in multiple sclerosis. Brain Connectivity, 12(6), 502–514. https://doi.org/10.1089/brain.2021.0037.
      Matarazzo, J. D., & Herman, D. O. (1984). Relationship of education and IQ in the WAIS‐R standardization sample. Journal of Consulting and Clinical Psychology, 52(4), 631–634. https://doi.org/10.1037/0022-006X.52.4.631.
      Meunier, D., Achard, S., Morcom, A., & Bullmore, E. (2009). Age‐related changes in modular organization of human brain functional networks. NeuroImage, 44(3), 715–723. https://doi.org/10.1016/j.neuroimage.2008.09.062.
      Mishra, S., Stenfelt, S., Lunner, T., Rönnberg, J., & Rudner, M. (2014). Cognitive spare capacity in older adults with hearing loss. Frontiers in Aging Neuroscience, 6, 96. https://doi.org/10.3389/fnagi.2014.00096.
      Mobley, A. S., Rodriguez‐Gil, D. J., Imamura, F., & Greer, C. A. (2014). Aging in the olfactory system. Trends in Neurosciences (Regular Ed.), 37(2), 77–84. https://doi.org/10.1016/j.tins.2013.11.004.
      Olson, I. R., Plotzker, A., & Ezzyat, Y. (2007). The enigmatic temporal pole: A review of findings on social and emotional processing. Brain, 130(7), 1718–1731. https://doi.org/10.1093/brain/awm052.
      Onoda, K., Ishihara, M., & Yamaguchi, S. (2012). Decreased functional connectivity by aging is associated with cognitive decline. Journal of Cognitive Neuroscience, 24(11), 2186–2198. https://doi.org/10.1162/jocn_a_00269.
      Oren, N., Ash, E. L., Shapira‐Lichter, I., Elkana, O., Reichman‐Eisikovits, O., Chomsky, L., & Lerner, Y. (2019). Changes in resting‐state functional connectivity of the hippocampus following cognitive effort predict memory decline at older age—A longitudinal fMRI study. Frontiers in Aging Neuroscience, 11, 163. https://doi.org/10.3389/fnagi.2019.00163.
      Owen, A. M., Milner, B., Petrides, M., & Evans, A. C. (1996). A specific role for the right parahippocampal gyrus in the retrieval of object‐location: A positron emission tomography study. Journal of Cognitive Neuroscience, 8(6), 588–602. https://doi.org/10.1162/jocn.1996.8.6.588.
      Power, J. D., Barnes, K. A., Snyder, A. Z., Schlaggar, B. L., & Petersen, S. E. (2012). Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. NeuroImage, 59(3), 2142–2154. https://doi.org/10.1016/j.neuroimage.2011.10.018.
      Rieckmann, A., Johnson, K. A., Sperling, R. A., Buckner, R. L., & Hedden, T. (2018). Dedifferentiation of caudate functional connectivity and striatal dopamine transporter density predict memory change in normal aging. Proceedings of the National Academy of Sciences ‐ PNAS, 115(40), 10160–10165. https://doi.org/10.1073/pnas.1804641115.
      Sambataro, F., Murty, V. P., Callicott, J. H., Tan, H., Das, S., Weinberger, D. R., & Mattay, V. S. (2010). Age‐related alterations in default mode network: Impact on working memory performance. Neurobiology of Aging, 31(5), 839–852. https://doi.org/10.1016/j.neurobiolaging.2008.05.022.
      Schaefer, A., Kong, R., Gordon, E. M., Laumann, T. O., Zuo, X., Holmes, A. J., Eickhoff, S. B., & Yeo, B. T. T. (2018). Local‐global parcellation of the human cerebral cortex from intrinsic functional connectivity MRI. Cerebral Cortex, 28(9), 3095–3114. https://doi.org/10.1093/cercor/bhx179.
      Schmithorst, V. J. (2009). Developmental sex differences in the relation of neuroanatomical connectivity to intelligence. Intelligence, 37(2), 164–173. https://doi.org/10.1016/j.intell.2008.07.001.
      Schmithorst, V. J., & Holland, S. K. (2007). Sex differences in the development of neuroanatomical functional connectivity underlying intelligence found using Bayesian connectivity analysis. NeuroImage, 35(1), 406–419. https://doi.org/10.1016/j.neuroimage.2006.11.046.
      Setton, R., Mwilambwe‐Tshilobo, L., Sheldon, S., Turner, G. R., & Spreng, R. N. (2022). Hippocampus and temporal pole functional connectivity is associated with age and individual differences in autobiographical memory. Proceedings of the National Academy of Sciences ‐ PNAS, 119(41), e2203039119. https://doi.org/10.1073/pnas.2203039119.
      Shen, X., Finn, E. S., Scheinost, D., Rosenberg, M. D., Chun, M. M., Papademetris, X., & Constable, R. T. (2017). Using connectome‐based predictive modeling to predict individual behavior from brain connectivity. Nature Protocols, 12(3), 506–518. https://doi.org/10.1038/nprot.2016.178.
      Sinnett, E. R., & Holen, M. C. (1999). Assessment of memory functioning among an aging sample. Psychological Reports, 84(1), 339–350. https://doi.org/10.2466/pr0.1999.84.1.339.
      Song, M., Zhou, Y., Li, J., Liu, Y., Tian, L., Yu, C., & Jiang, T. (2008). Brain spontaneous functional connectivity and intelligence. NeuroImage, 41(3), 1168–1176. https://doi.org/10.1016/j.neuroimage.2008.02.036.
      Strick, P. L., Dum, R. P., & Fiez, J. A. (2009). Cerebellum and nonmotor function. Annual Review of Neuroscience, 32(1), 413–434. https://doi.org/10.1146/annurev.neuro.31.060407.125606.
      Toussaint, P. J., Maiz, S., Coynel, D., Messe, A., Perlbarg, V., Habert, M. O., & Benali, H. (2011). Characterization of the default mode functional connectivity in normal aging and Alzheimer's disease: An approach combining entropy‐based and graph theoretical measurements. Paper presented at the 853–856.
      Tzourio‐Mazoyer, N., Landeau, B., Papathanassiou, D., Crivello, F., Etard, O., Delcroix, N., Mazoyer, B., & Joliot, M. (2002). Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single‐subject brain. NeuroImage, 15(1), 273–289. https://doi.org/10.1006/nimg.2001.0978.
      United Nations Population Division Publications. (2017). World population ageing 2017 report. http://www.un.org/en/development/desa/population/publications/pdf/ageing/WPA2017_Highlights.pdf.
      Vergun, S., Deshpande, A. S., Meier, T. B., Song, J., Tudorascu, D. L., Nair, V. A., Singh, V., Biswal, B. B., Meyerand, M. E., Birn, R. M., & Prabhakaran, V. (2013). Characterizing functional connectivity differences in aging adults using machine learning on resting state fMRI data. Frontiers in Computational Neuroscience, 7, 38. https://doi.org/10.3389/fncom.2013.00038.
      Wang, J., Eslinger, P. J., Smith, M. B., & Yang, Q. X. (2005). Functional magnetic resonance imaging study of human olfaction and normal aging. The Journals of Gerontology. Series A, Biological Sciences and Medical Sciences, 60(4), 510–514. https://doi.org/10.1093/gerona/60.4.510.
      Wang, Z., Yang, J., Zheng, Z., Cao, W., Dong, L., Li, H., Wen, X., Luo, C., Cai, Q., Jian, W., & Yao, D. (2023). Trait‐ and state‐dependent changes in cortical–subcortical functional networks across the adult lifespan. Journal of Magnetic Resonance Imaging, 58(3), 720–731.
      Warrier, C., Wong, P., Penhune, V., Zatorre, R., Parrish, T., Abrams, D., & Kraus, N. (2009). Relating structure to function: Heschl's gyrus and acoustic processing. The Journal of Neuroscience, 29(1), 61–69. https://doi.org/10.1523/JNEUROSCI.3489-08.2009.
      Wechsler, D. (2008). Wechsler adult intelligence scale‐fourth edition (WAIS‐IV) manual. Pearson.
      Wechsler, D. (2009). Wechsler memory scale–fourth edition (WMS–IV) technical and interpretive manual. Pearson.
      Wikenheiser, A. M., & Schoenbaum, G. (2016). Over the river, through the woods: Cognitive maps in the hippocampus and orbitofrontal cortex. Nature Reviews Neuroscience, 17(8), 513–523. https://doi.org/10.1038/nrn.2016.56.
      Wilson, R. C., Takahashi, Y. K., Schoenbaum, G., & Niv, Y. (2014). Orbitofrontal cortex as a cognitive map of task space. Neuron, 81(2), 267–279. https://doi.org/10.1016/j.neuron.2013.11.005.
      Yan, C., & Zang, Y. (2010). DPARSF: A MATLAB toolbox for “pipeline” data analysis of resting‐state fMRI. Frontiers in Systems Neuroscience, 4, 13. https://doi.org/10.3389/fnsys.2010.00013.
      Zald, D. H., McHugo, M., Ray, K. L., Glahn, D. C., Eickhoff, S. B., & Laird, A. R. (2014). Meta‐analytic connectivity modeling reveals differential functional connectivity of the medial and lateral orbitofrontal cortex. Cerebral Cortex, 24(1), 232–248. https://doi.org/10.1093/cercor/bhs308.
      Zhu, J., Li, Y., Fang, Q., Shen, Y., Qian, Y., Cai, H., & Yu, Y. (2021). Dynamic functional connectome predicts individual working memory performance across diagnostic categories. NeuroImage: Clinical, 30, 102593. https://doi.org/10.1016/j.nicl.2021.102593.
      Zhu, Y., Zang, F., Wang, Q., Zhang, Q., Tan, C., Zhang, S., Hu, T., Qi, L., Xu, S., Ren, Q., & Xie, C. (2021). Connectome‐based model predicts episodic memory performance in individuals with subjective cognitive decline and amnestic mild cognitive impairment. Behavioural Brain Research, 411, 113387. https://doi.org/10.1016/j.bbr.2021.113387.
    • Grant Information:
      2022ZD0209000 STI 2030-Major Projects; ZJ2018-ZD-012 Shanghai Zhangjiang National Innovation Demonstration Zone Special Funds for Major Projects "Human Brain Research Imaging Equipment Development and Demonstration Application Platform"; JCYJ-SHFY-2022-014 Shanghai Pilot Program for Basic Research-Chinese Academy of Science, Shanghai Branch; NMED2021ZD-01-001 Open Research Fund Program of National Innovation Center for Advanced Medical Devices; KCXFZ20211020163408012 Shenzhen Science and Technology Program; 2021B0909050004 Special Fund for Science-Technology Innovation Strategy of Guangdong Province; CIFMS Chinese Academy of Medical Sciences (CAMS) Innovation Fund for Medical Science; 2019-I2M-5-082 Chinese Academy of Medical Sciences (CAMS) Innovation Fund for Medical Science; 21PJ1421400 Shanghai Pujiang Program
    • Contributed Indexing:
      Keywords: ageing; brain connectivity; connectome‐based predictive modelling; intelligence quotient; memory quotient; resting‐state fMRI
    • Publication Date:
      Date Created: 20241111 Date Completed: 20241203 Latest Revision: 20241203
    • Publication Date:
      20241204
    • Accession Number:
      10.1111/ejn.16559
    • Accession Number:
      39523689