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Age-related decline in cognitive flexibility and inadequate preparation: evidence from task-state network analysis

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Abstract

Behavioral evidence showed decreased cognitive flexibility in older adults. However, task-based network mechanisms of cognitive flexibility in aging (CFA) remain unclear. Here, we provided the first task-state network evidence that CFA was associated with inadequate preparation for switching trials by revealing age-related changes in functional integration. We examined functional integration in a letter–number switch task that distinguished between the cue and target stages. Both young and older adults showed decreased functional integration from the cue stage to the target stage, indicating that control-related processes were executed as the task progressed. However, compared to young adults, older adults showed less cue-to-target reduction in functional integration, which was primarily driven by higher network integration in the target stage. Moreover, less cue-to-target reductions were correlated with age-related decreases in task performance in the switch task. To sum up, compared to young adults, older adults pre-executed less control-related processes in the cue stage and more control-related processes in the target stage. Therefore, the decline in cognitive flexibility in older adults was associated with inadequate preparation for the impending demands of cognitive switching. This study offered novel insights into network mechanisms underlying CFA. Furthermore, we highlighted that training the function of brain networks, in conjunction with providing more preparation time for older adults, may be beneficial to their cognitive flexibility.

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References

  1. Braem S, Egner T. Getting a grip on cognitive flexibility. Curr Dir Psychol Sci. 2018;27(6):470–6.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Dajani DR, Uddin LQ. Demystifying cognitive flexibility: implications for clinical and developmental neuroscience. Trends Neurosci. 2015;38(9):571–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Ging-Jehli NR, Ratcliff R. Effects of aging in a task-switch paradigm with the diffusion decision model. Psychol Aging. 2020;35(6):850–65.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Wasylyshyn C, Verhaeghen P, Sliwinski MJ. Aging and task switching: a meta-analysis. Psychol Aging. 2011;26(1):15–20.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Grady C. The cognitive neuroscience of ageing. Nat Rev Neurosci. 2012;13(7):491–505.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Ferreira LK, Busatto GF. Resting-state functional connectivity in normal brain aging. Neurosci Biobehav Rev. 2013;37(3):384–400.

    Article  PubMed  Google Scholar 

  7. Grady C, Sarraf S, Saverino C, Campbell K. Age differences in the functional interactions among the default, frontoparietal control, and dorsal attention networks. Neurobiol Aging. 2016;41:159–72.

    Article  PubMed  Google Scholar 

  8. Koen JD, Srokova S, Rugg MD. Age-related neural dedifferentiation and cognition. Curr Opin Behav Sci. 2020;32:7–14.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Malagurski B, Liem F, Oschwald J, Merillat S, Jancke L. Functional dedifferentiation of associative resting state networks in older adults - a longitudinal study. Neuroimage. 2020;214: 116680.

    Article  PubMed  Google Scholar 

  10. Dajani DR, Odriozola P, Winters M, Voorhies W, Marcano S, Baez A, et al. Measuring cognitive flexibility with the flexible item selection task: from fMRI adaptation to individual connectome mapping. J Cogn Neurosci. 2020;32(6):1026–45.

    Article  PubMed  Google Scholar 

  11. Cohen JR, D’Esposito M. The segregation and integration of distinct brain networks and their relationship to cognition. J Neurosci. 2016;36(48):12083–94.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Mohr H, Wolfensteller U, Betzel RF, Misic B, Sporns O, Richiardi J, et al. Integration and segregation of large-scale brain networks during short-term task automatization. Nat Commun. 2016;7:13217.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Sporns O. Network attributes for segregation and integration in the human brain. Curr Opin Neurobiol. 2013;23(2):162–71.

    Article  CAS  PubMed  Google Scholar 

  14. Xia H, He Q, Chen A. Understanding cognitive control in aging: a brain network perspective. Front Aging Neurosci. 2022;14:1038756.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Cole MW, Reynolds JR, Power JD, Repovs G, Anticevic A, Braver TS. Multi-task connectivity reveals flexible hubs for adaptive task control. Nat Neurosci. 2013;16(9):1348–55.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Cocchi L, Zalesky A, Fornito A, Mattingley JB. Dynamic cooperation and competition between brain systems during cognitive control. Trends Cogn Sci. 2013;17(10):493–501.

    Article  PubMed  Google Scholar 

  17. Cocchi L, Halford GS, Zalesky A, Harding IH, Ramm BJ, Cutmore T, et al. Complexity in relational processing predicts changes in functional brain network dynamics. Cereb Cortex. 2014;24(9):2283–96.

    Article  PubMed  Google Scholar 

  18. Dosenbach NU, Fair DA, Miezin FM, Cohen AL, Wenger KK, Dosenbach RA, et al. Distinct brain networks for adaptive and stable task control in humans. Proc Natl Acad Sci U S A. 2007;104(26):11073–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Yin S, Deák G, Chen A. Coactivation of cognitive control networks during task switching. Neuropsychology. 2018;32(1):31.

    Article  PubMed  Google Scholar 

  20. Koch I, Kiesel A. Task switching: cognitive control in sequential multitasking. In: Kiesel A, Johannsen L, Koch I, Müller H, editors. Handbook of human multitasking. Cham: Springer; 2022. pp. 85–143.

  21. Koch I, Poljac E, Muller H, Kiesel A. Cognitive structure, flexibility, and plasticity in human multitasking-An integrative review of dual-task and task-switching research. Psychol Bull. 2018;144(6):557–83.

    Article  PubMed  Google Scholar 

  22. Monsell S. Task switching. Trends Cogn Sci. 2003;7(3):134–40.

    Article  PubMed  Google Scholar 

  23. Vandierendonck A, Liefooghe B, Verbruggen F. Task switching: interplay of reconfiguration and interference control. Psychol Bull. 2010;136(4):601–26.

    Article  PubMed  Google Scholar 

  24. Sporns O, Betzel RF. Modular brain networks. Annu Rev Psychol. 2016;67:613–40.

    Article  PubMed  Google Scholar 

  25. Kiesel A, Steinhauser M, Wendt M, Falkenstein M, Jost K, Philipp AM, et al. Control and interference in task switching–a review. Psychol Bull. 2010;136(5):849–74.

    Article  PubMed  Google Scholar 

  26. Schneider DW. Investigating a method for reducing residual switch costs in cued task switching. Mem Cognit. 2016;44:762–77.

    Article  PubMed  Google Scholar 

  27. Verbruggen F, Liefooghe B, Vandierendonck A, Demanet J. Short cue presentations encourage advance task preparation: a recipe to diminish the residual switch cost. J Exp Psychol Learn Mem Cogn. 2007;33(2):342.

    Article  PubMed  Google Scholar 

  28. Steyvers M, Hawkins GE, Karayanidis F, Brown SD. A large-scale analysis of task switching practice effects across the lifespan. Proc Natl Acad Sci U S A. 2019;116(36):17735–40.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Lawo V, Philipp AM, Schuch S, Koch I. The role of task preparation and task inhibition in age-related task-switching deficits. Psychol Aging. 2012;27(4):1130–7.

    Article  PubMed  Google Scholar 

  30. Lien M-C, Ruthruff E, Remington RW, Johnston JC. On the limits of advance preparation for a task switch: do people prepare all the task some of the time or some of the task all the time? J Exp Psychol Hum Percept Perform. 2005;31(2):299.

    Article  PubMed  Google Scholar 

  31. Cabeza R, Albert M, Belleville S, Craik FIM, Duarte A, Grady CL, et al. Maintenance, reserve and compensation: the cognitive neuroscience of healthy ageing. Nat Rev Neurosci. 2018;19(11):701–10.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Crowell CA, Davis SW, Beynel L, Deng L, Lakhlani D, Hilbig SA, et al. Older adults benefit from more widespread brain network integration during working memory. Neuroimage. 2020;218: 116959.

    Article  CAS  PubMed  Google Scholar 

  33. Rieck JR, Baracchini G, Nichol D, Abdi H, Grady CL. Reconfiguration and dedifferentiation of functional networks during cognitive control across the adult lifespan. Neurobiol Aging. 2021;106:80–94.

    Article  CAS  PubMed  Google Scholar 

  34. Li T, Xia H, Li H, He Q, Chen A. Functional connectivity alterations of cognitive flexibility in aging: different patterns of global and local switch costs. J Gerontol Ser B. 2023;78(10):1651–8.

    Article  Google Scholar 

  35. Jimura K, Braver TS. Age-related shifts in brain activity dynamics during task switching. Cereb Cortex. 2010;20(6):1420–31.

    Article  PubMed  Google Scholar 

  36. Madden DJ, Costello MC, Dennis NA, Davis SW, Shepler AM, Spaniol J, et al. Adult age differences in functional connectivity during executive control. Neuroimage. 2010;52(2):643–57.

    Article  PubMed  Google Scholar 

  37. Menon V, D’Esposito M. The role of PFC networks in cognitive control and executive function. Neuropsychopharmacology. 2022;47(1):90–103.

    Article  PubMed  Google Scholar 

  38. Konstantinou N, Beal E, King JR, Lavie N. Working memory load and distraction: dissociable effects of visual maintenance and cognitive control. Atten Percept Psychophys. 2014;76(7):1985–97.

    Article  PubMed  PubMed Central  Google Scholar 

  39. Poldrack RA, Congdon E, Triplett W, Gorgolewski K, Karlsgodt K, Mumford J, et al. A phenome-wide examination of neural and cognitive function. Sci Data. 2016;3(1):1–12.

    Article  Google Scholar 

  40. Faul F, Erdfelder E, Buchner A, Lang A-G. Statistical power analyses using G* power 3.1: tests for correlation and regression analyses. Behav Res Methods. 2009;41(4):1149–60.

    Article  PubMed  Google Scholar 

  41. Nashiro K, Qin S, O’Connell MA, Basak C. Age-related differences in BOLD modulation to cognitive control costs in a multitasking paradigm: global switch, local switch, and compatibility-switch costs. Neuroimage. 2018;172:146–61.

    Article  PubMed  Google Scholar 

  42. Zhu Z, Hakun JG, Johnson NF, Gold BT. Age-related increases in right frontal activation during task switching are mediated by reaction time and white matter microstructure. Neuroscience. 2014;278:51–61.

    Article  CAS  PubMed  Google Scholar 

  43. Huettel SA. Event-related fMRI in cognition. Neuroimage. 2012;62(2):1152–6.

    Article  PubMed  Google Scholar 

  44. Kahana MJ, Ezzyat Y, Wanda PA, Solomon EA, Adamovich-Zeitlin R, Lega BC, et al. Biomarker-guided neuromodulation aids memory in traumatic brain injury. Brain Stimul. 2023;16(4):1086–93.

    Article  PubMed  Google Scholar 

  45. Burock MA, Buckner RL, Woldorff MG, Rosen BR, Dale AM. Randomized event-related experimental designs allow for extremely rapid presentation rates using functional MRI. NeuroReport. 1998;9(16):3735–9.

    Article  CAS  PubMed  Google Scholar 

  46. Mary A, Dayan J, Leone G, Postel C, Fraisse F, Malle C, et al. Resilience after trauma: the role of memory suppression. Science. 2020;367(6479):eaay8477.

    Article  CAS  PubMed  Google Scholar 

  47. Yan C-G, Wang X-D, Zuo X-N, Zang Y-F. DPABI: data processing & analysis for (resting-state) brain imaging. Neuroinformatics. 2016;14:339–51.

    Article  PubMed  Google Scholar 

  48. Shen X, Tokoglu F, Papademetris X, Constable RT. Groupwise whole-brain parcellation from resting-state fMRI data for network node identification. Neuroimage. 2013;82:403–15.

    Article  CAS  PubMed  Google Scholar 

  49. Yan X, Kong R, Xue A, Yang Q, Orban C, An L, et al. Homotopic local-global parcellation of the human cerebral cortex from resting-state functional connectivity. Neuroimage. 2023;273: 120010.

    Article  CAS  PubMed  Google Scholar 

  50. Rosenberg MD, Finn ES, Scheinost D, Papademetris X, Shen X, Constable RT, et al. A neuromarker of sustained attention from whole-brain functional connectivity. Nat Neurosci. 2016;19(1):165–71.

    Article  CAS  PubMed  Google Scholar 

  51. Di X, Biswal BB. Psychophysiological interactions in a visual checkerboard task: reproducibility, reliability, and the effects of deconvolution. Front Neurosci. 2017;11:573.

    Article  PubMed  PubMed Central  Google Scholar 

  52. McLaren DG, Ries ML, Xu G, Johnson SC. A generalized form of context-dependent psychophysiological interactions (gPPI): a comparison to standard approaches. Neuroimage. 2012;61(4):1277–86.

    Article  PubMed  Google Scholar 

  53. Aryani A, Hsu CT, Jacobs AM. Affective iconic words benefit from additional sound–meaning integration in the left amygdala. Hum Brain Mapp. 2019;40(18):5289–300.

    Article  PubMed  PubMed Central  Google Scholar 

  54. Kwon S-J, Turpyn CC, Prinstein MJ, Lindquist KA, Telzer EH. Self-oriented neural circuitry predicts other-oriented adaptive risks in adolescence: a longitudinal study. Soc Cognit Affect Neurosci. 2022;17(2):161–71.

    Article  Google Scholar 

  55. Economides M, Guitart-Masip M, Kurth-Nelson Z, Dolan RJ. Anterior cingulate cortex instigates adaptive switches in choice by integrating immediate and delayed components of value in ventromedial prefrontal cortex. J Neurosci. 2014;34(9):3340–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Gitelman DR, Penny WD, Ashburner J, Friston KJ. Modeling regional and psychophysiologic interactions in fMRI: the importance of hemodynamic deconvolution. Neuroimage. 2003;19(1):200–7.

    Article  PubMed  Google Scholar 

  57. Di X, Biswal BB. Toward task connectomics: examining whole-brain task modulated connectivity in different task domains. Cereb Cortex. 2019;29(4):1572–83.

    Article  PubMed  Google Scholar 

  58. Liang X, Zou Q, He Y, Yang Y. Topologically reorganized connectivity architecture of default-mode, executive-control, and salience networks across working memory task loads. Cereb Cortex. 2016;26(4):1501–11.

    Article  PubMed  Google Scholar 

  59. Xu P, Huang R, Wang J, Van Dam NT, Xie T, Dong Z, et al. Different topological organization of human brain functional networks with eyes open versus eyes closed. Neuroimage. 2014;90:246–55.

    Article  PubMed  Google Scholar 

  60. Marek S, Hwang K, Foran W, Hallquist MN, Luna B. The contribution of network organization and integration to the development of cognitive control. PLoS Biol. 2015;13(12): e1002328.

    Article  PubMed  PubMed Central  Google Scholar 

  61. Guimera R, Amaral LA. Cartography of complex networks: modules and universal roles. J Stat Mech. 2005;2005(P02001):nihpa35573.

    PubMed  Google Scholar 

  62. Rubinov M, Kötter R, Hagmann P, Sporns O. Brain connectivity toolbox: a collection of complex network measurements and brain connectivity datasets. Neuroimage. 2009;47:S169.

    Article  Google Scholar 

  63. Clapp WC, Rubens MT, Sabharwal J, Gazzaley A. Deficit in switching between functional brain networks underlies the impact of multitasking on working memory in older adults. Proc Natl Acad Sci U S A. 2011;108(17):7212–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Berry AS, Shah VD, Baker SL, Vogel JW, O’Neil JP, Janabi M, et al. Aging affects dopaminergic neural mechanisms of cognitive flexibility. J Neurosci. 2016;36(50):12559–69.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Fandakova Y, Sander MC, Werkle-Bergner M, Shing YL. Age differences in short-term memory binding are related to working memory performance across the lifespan. Psychol Aging. 2014;29(1):140–9.

    Article  PubMed  Google Scholar 

  66. Hayes AF. PROCESS: A versatile computational tool for observed variable mediation, moderation, and conditional process modeling. KS: University of Kansas; 2012.

    Google Scholar 

  67. Lai H, Wang S, Zhao Y, Qiu C, Gong Q. Neurostructural correlates of optimism: gray matter density in the putamen predicts dispositional optimism in late adolescence. Hum Brain Mapp. 2020;41(6):1459–71.

    Article  PubMed  Google Scholar 

  68. Sdoia S, Ferlazzo F. Stimulus-related inhibition of task set during task switching. Exp Psychol. 2008;55(5):322–7.

    Article  PubMed  Google Scholar 

  69. Strobach T, Wendt M, Janczyk M. Multitasking: Executive functioning in dual-task and task switching situations. Front Psychol. 2018;9:344190.

  70. Cassady K, Gagnon H, Freiburger E, Lalwani P, Simmonite M, Park DC, et al. Network segregation varies with neural distinctiveness in sensorimotor cortex. Neuroimage. 2020;212: 116663.

    Article  PubMed  Google Scholar 

  71. Bassett DS, Yang M, Wymbs NF, Grafton ST. Learning-induced autonomy of sensorimotor systems. Nat Neurosci. 2015;18(5):744–51.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Tamber-Rosenau BJ, Asplund CL, Marois R. Functional dissociation of the inferior frontal junction from the dorsal attention network in top-down attentional control. J Neurophysiol. 2018;120(5):2498–512.

    Article  PubMed  PubMed Central  Google Scholar 

  73. Vossel S, Geng JJ, Fink GR. Dorsal and ventral attention systems: distinct neural circuits but collaborative roles. Neuroscientist. 2014;20(2):150–9.

    Article  PubMed  PubMed Central  Google Scholar 

  74. Zanto TP, Gazzaley A. Fronto-parietal network: flexible hub of cognitive control. Trends Cogn Sci. 2013;17(12):602–3.

    Article  PubMed  Google Scholar 

  75. Ruge H, Brass M, Koch I, Rubin O, Meiran N, Von Cramon DY. Advance preparation and stimulus-induced interference in cued task switching: further insights from BOLD fMRI. Neuropsychologia. 2005;43(3):340–55.

    Article  PubMed  Google Scholar 

  76. Paxton JL, Barch DM, Racine CA, Braver TS. Cognitive control, goal maintenance, and prefrontal function in healthy aging. Cereb Cortex. 2008;18(5):1010–28.

    Article  PubMed  Google Scholar 

  77. Braver TS. The variable nature of cognitive control: a dual mechanisms framework. Trends Cogn Sci. 2012;16(2):106–13.

    Article  PubMed  PubMed Central  Google Scholar 

  78. Zarahn E, Rakitin B, Abela D, Flynn J, Stern Y. Age-related changes in brain activation during a delayed item recognition task. Neurobiol Aging. 2007;28(5):784–98.

    Article  PubMed  Google Scholar 

  79. Kuhns D, Lien M-C, Ruthruff E. Proactive versus reactive task-set inhibition: evidence from flanker compatibility effects. Psychon Bull Rev. 2007;14(5):977–83.

    Article  PubMed  Google Scholar 

  80. Dosenbach NU, Nardos B, Cohen AL, Fair DA, Power JD, Church JA, et al. Prediction of individual brain maturity using fMRI. Science. 2010;329(5997):1358–61.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Braver TS, Kizhner A, Tang R, Freund MC, Etzel JA. The dual mechanisms of cognitive control project. J Cogn Neurosci. 2021;33(9):1990–2015.

    Google Scholar 

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This work is supported by a grant from the National Natural Science Foundation of China (32371105).

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Xia, H., Li, T., Hou, Y. et al. Age-related decline in cognitive flexibility and inadequate preparation: evidence from task-state network analysis. GeroScience (2024). https://doi.org/10.1007/s11357-024-01135-x

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