Abstract
Albeit cognitive flexibility is well known to decline in aging, it has not been considered that this ability often requires sequential task control. That is, one may re-use tasks that have previously been abandoned in favor of another task. It is unclear whether sequential cognitive flexibility is affected in aging and what neurophysiological mechanisms and functional neuroanatomical structures are associated with these effects. We examined this question in a system neurophysiological study using EEG and source localization in healthy and elderly adults. We show that elderly people reveal deficient sequential cognitive flexibility. Elderly people encounter increased costs to overcome the inhibition of the lately abandoned task set that becomes relevant again and needs to be re-used. The neurophysiological (EEG) data show that differences in sequential cognitive flexibility between young and elderly people emerge as a consequence of two independent, dysfunctional processes: (i) the ability to suppress task-irrelevant information and (ii) the ability to re-implement a previously abandoned task set during response selection. These independent processes were associated with activation differences in inferior frontal and inferior parietal regions. The study reveals a new facet of cognitive flexibility dysfunctions in healthy elderlies.
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References
Albrecht DS, Kareken DA, Christian BT et al (2014) Cortical dopamine release during a behavioral response inhibition task. Synap N Y N 68:266–274. https://doi.org/10.1002/syn.21736
Allport DA, Wylie G (1999) Task-switching: Positive and negative priming of task-set. In: Humphreys GW, Duncan J, Treisman A (eds) Attention, space, and action: studies in cognitive neuroscience. Oxford University Press, New York, pp 273–296
Allport A, Styles EA, Hsieh S (1994) Shifting intentional set: exploring the dynamic control of task. In: Umiltà C, Moscovitch M (eds) Attention and performance XV: conscious and nonconscious information processing. MIT Press, Cambridge, pp 421–452
Aron AR, Monsell S, Sahakian BJ, Robbins TW (2004a) A componential analysis of task-switching deficits associated with lesions of left and right frontal cortex. Brain 127:1561–1573. https://doi.org/10.1093/brain/awh169
Aron AR, Robbins TW, Poldrack RA (2004b) Inhibition and the right inferior frontal cortex. Trends Cogn Sci 8:170–177. https://doi.org/10.1016/j.tics.2004.02.010
Aron AR, Robbins TW, Poldrack RA (2014) Inhibition and the right inferior frontal cortex: one decade on. Trends Cogn Sci 18:177–185. https://doi.org/10.1016/j.tics.2013.12.003
Bäckman L, Nyberg L, Lindenberger U et al (2006) The correlative triad among aging, dopamine, and cognition: current status and future prospects. Neurosci Biobehav Rev 30:791–807. https://doi.org/10.1016/j.neubiorev.2006.06.005
Bäckman L, Lindenberger U, Li S-C, Nyberg L (2010) Linking cognitive aging to alterations in dopamine neurotransmitter functioning: recent data and future avenues. Neurosci Biobehav Rev 34:670–677. https://doi.org/10.1016/j.neubiorev.2009.12.008
Bari A, Robbins TW (2013) Inhibition and impulsivity: behavioral and neural basis of response control. Prog Neurobiol 108:44–79. https://doi.org/10.1016/j.pneurobio.2013.06.005
Berry AS, Shah VD, Baker SL et al (2016) Aging affects dopaminergic neural mechanisms of cognitive flexibility. J Neurosci 36:12559–12569. https://doi.org/10.1523/JNEUROSCI.0626-16.2016
Bodmer B, Beste C (2017) On the dependence of response inhibition processes on sensory modality. Hum Brain Mapp. https://doi.org/10.1002/hbm.23495
Bodmer B, Friedrich J, Roessner V, Beste C (2018a) Differences in response inhibition processes between adolescents and adults are modulated by sensory processes. Dev Cogn Neurosci 31:35–45. https://doi.org/10.1016/j.dcn.2018.04.008
Bodmer B, Mückschel M, Roessner V, Beste C (2018b) Neurophysiological variability masks differences in functional neuroanatomical networks and their effectiveness to modulate response inhibition between children and adults. Brain Struct Funct 223:1797–1810. https://doi.org/10.1007/s00429-017-1589-6
Bourisly AK (2016) Effects of aging on P300 between late young-age and early middle-age adulthood: an electroencephalogram event-related potential study. NeuroReport 27:999–1003. https://doi.org/10.1097/WNR.0000000000000644
Bubb EJ, Metzler-Baddeley C, Aggleton JP (2018) The cingulum bundle: anatomy, function, and dysfunction. Neurosci Biobehav Rev 92:104–127. https://doi.org/10.1016/j.neubiorev.2018.05.008
Chmielewski WX, Mückschel M, Ziemssen T, Beste C (2017) The norepinephrine system affects specific neurophysiological subprocesses in the modulation of inhibitory control by working memory demands. Hum Brain Mapp 38:68–81. https://doi.org/10.1002/hbm.23344
Coxon JP, Goble DJ, Leunissen I et al (2016) Functional brain activation associated with inhibitory control deficits in older adults. Cereb Cortex 26:12–22. https://doi.org/10.1093/cercor/bhu165
Dajani DR, Uddin LQ (2015) Demystifying cognitive flexibility: implications for clinical and developmental neuroscience. Trends Neurosci 38:571–578
Davidson MC, Amso D, Anderson LC, Diamond A (2006) Development of cognitive control and executive functions from 4 to 13 years: evidence from manipulations of memory, inhibition, and task switching. Neuropsychologia 44:2037–2078. https://doi.org/10.1016/j.neuropsychologia.2006.02.006
Diamond A (2002) Normal development of prefrontal cortex from birth to young adulthood: cognitive functions, anatomy, and biochemistry. In: Stuss D, Knight R (eds) Principles of Frontal Lobe Function. Oxford University Press, New York
Diamond A (2013) Executive functions. Annu Rev Psychol 64:135–168. https://doi.org/10.1146/annurev-psych-113011-143750
Dippel G, Beste C (2015) A causal role of the right inferior frontal cortex in implementing strategies for multi-component behaviour. Nat Commun 6:6587. https://doi.org/10.1038/ncomms7587
Duncan J (2010) The multiple-demand (MD) system of the primate brain: mental programs for intelligent behaviour. Trends Cogn Sci 14:172–179. https://doi.org/10.1016/j.tics.2010.01.004
Fedorenko E, Duncan J, Kanwisher N (2013) Broad domain generality in focal regions of frontal and parietal cortex. Proc Natl Acad Sci 110:16616–16621. https://doi.org/10.1073/pnas.1315235110
Gajewski PD, Ferdinand NK, Kray J, Falkenstein M (2018) Understanding sources of adult age differences in task switching: evidence from behavioral and ERP studies. Neurosci Biobehav Rev 92:255–275. https://doi.org/10.1016/j.neubiorev.2018.05.029
Garrett DD, Samanez-Larkin GR, MacDonald SWS et al (2013) Moment-to-moment brain signal variability: a next frontier in human brain mapping? Neurosci Biobehav Rev 37:610–624. https://doi.org/10.1016/j.neubiorev.2013.02.015
Geng JJ, Vossel S (2013) Re-evaluating the role of TPJ in attentional control: contextual updating? Neurosci Biobehav Rev 37:2608–2620. https://doi.org/10.1016/j.neubiorev.2013.08.010
Giller F, Zhang R, Roessner V, Beste C (2019) The neurophysiological basis of developmental changes during sequential cognitive flexibility between adolescents and adults. Hum Brain Mapp 40:552–565. https://doi.org/10.1002/hbm.24394
Grady CL (2008) Cognitive neuroscience of aging. Ann N Y Acad Sci 1124:127–144. https://doi.org/10.1196/annals.1440.009
Hämmerer D, Eppinger B (2012) Dopaminergic and prefrontal contributions to reward-based learning and outcome monitoring during child development and aging. Dev Psychol 48:862–874. https://doi.org/10.1037/a0027342
Hershey T, Black KJ, Hartlein J et al (2004) Dopaminergic modulation of response inhibition: an fMRI study. Cogn Brain Res 20:438–448. https://doi.org/10.1016/j.cogbrainres.2004.03.018
Holtzer R, Epstein N, Mahoney JR et al (2014) Neuroimaging of mobility in aging: a targeted review. J Gerontol A Biol Sci Med Sci 69:1375–1388. https://doi.org/10.1093/gerona/glu052
Hu S, Li C-SR (2012) Neural processes of preparatory control for stop signal inhibition. Hum Brain Mapp 33:2785–2796. https://doi.org/10.1002/hbm.21399
Hu S, Ide JS, Chao HH et al (2018) Structural and functional cerebral bases of diminished inhibitory control during healthy aging. Hum Brain Mapp. https://doi.org/10.1002/hbm.24347
Hübner M, Dreisbach G, Haider H, Kluwe RH (2003) Backward inhibition as a means of sequential task-set control: evidence for reduction of task competition. J Exp Psychol Learn Mem Cogn 29:289–297. https://doi.org/10.1037/0278-7393.29.2.289
Hultsch DF, Strauss E, Hunter MA, MacDonald SWS (2008) Intraindividual variability, cognition and aging. In: Craik FIM, Salthouse TA (eds) The handbook of aging and cognition, 3rd edn. Psychology Press, New York
Kayser J, Tenke CE (2015) On the benefits of using surface Laplacian (current source density) methodology in electrophysiology. Int J Psychophysiol 97:171–173. https://doi.org/10.1016/j.ijpsycho.2015.06.001
Kievit RA, Davis SW, Mitchell DJ et al (2014) Distinct aspects of frontal lobe structure mediate age-related differences in fluid intelligence and multitasking. Nat Commun. https://doi.org/10.1038/ncomms6658
Klimesch W (2011) Evoked alpha and early access to the knowledge system: the P1 inhibition timing hypothesis. Brain Res 1408:52–71. https://doi.org/10.1016/j.brainres.2011.06.003
Koch I, Gade M, Philipp AM (2004) Inhibition of response mode in task switching. Exp Psychol 51:52–58. https://doi.org/10.1027/1618-3169.51.1.52
Kok A (2000) Age-related changes in involuntary and voluntary attention as reflected in components of the event-related potential (ERP). Biol Psychol 54:107–143. https://doi.org/10.1016/S0301-0511(00)00054-5
Lee H-H, Hsieh S (2017) Resting-State fMRI Associated with stop-signal task performance in healthy middle-aged and elderly people. Front Psychol. https://doi.org/10.3389/fpsyg.2017.00766
Li S-C, Rieckmann A (2014) Neuromodulation and aging: implications of aging neuronal gain control on cognition. Curr Opin Neurobiol 29:148–158. https://doi.org/10.1016/j.conb.2014.07.009
Li S-C, Lindenberger U, Bäckman L (2010) Dopaminergic modulation of cognition across the life span. Neurosci Biobehav Rev 34:625–630. https://doi.org/10.1016/j.neubiorev.2010.02.003
Lockhart SN, DeCarli C (2014) Structural imaging measures of brain aging. Neuropsychol Rev 24:271–289. https://doi.org/10.1007/s11065-014-9268-3
MacDonald SWS, Nyberg L, Bäckman L (2006) Intra-individual variability in behavior: links to brain structure, neurotransmission and neuronal activity. Trends Neurosci 29:474–480. https://doi.org/10.1016/j.tins.2006.06.011
Marco-Pallarés J, Grau C, Ruffini G (2005) Combined ICA-LORETA analysis of mismatch negativity. NeuroImage 25:471–477. https://doi.org/10.1016/j.neuroimage.2004.11.028
Mayr U, Keele SW (2000) Changing internal constraints on action: the role of backward inhibition. J Exp Psychol Gen 129:4–26
Mückschel M, Stock A-K, Beste C (2014) Psychophysiological mechanisms of interindividual differences in goal activation modes during action cascading. Cereb Cortex N Y N 24:2120–2129. https://doi.org/10.1093/cercor/bht066
Mückschel M, Chmielewski W, Ziemssen T, Beste C (2017) The norepinephrine system shows information-content specific properties during cognitive control—evidence from EEG and pupillary responses. NeuroImage 149:44–52. https://doi.org/10.1016/j.neuroimage.2017.01.036
Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113
Ouyang G, Herzmann G, Zhou C, Sommer W (2011) Residue iteration decomposition (RIDE): a new method to separate ERP components on the basis of latency variability in single trials. Psychophysiology 48:1631–1647. https://doi.org/10.1111/j.1469-8986.2011.01269.x
Ouyang G, Sommer W, Zhou C (2015a) A toolbox for residue iteration decomposition (RIDE)—a method for the decomposition, reconstruction, and single trial analysis of event related potentials. J Neurosci Methods 250:7–21. https://doi.org/10.1016/j.jneumeth.2014.10.009
Ouyang G, Sommer W, Zhou C (2015b) Updating and validating a new framework for restoring and analyzing latency-variable ERP components from single trials with residue iteration decomposition (RIDE). Psychophysiology 52:839–856. https://doi.org/10.1111/psyp.12411
Pascual-Marqui RD (2002) Standardized low-resolution brain electromagnetic tomography (sLORETA): technical details. Methods Find Exp Clin Pharmacol 24(Suppl D):5–12
Schuch S (2016) Task inhibition and response inhibition in older vs. younger adults: a diffusion model analysis. Front Psychol. https://doi.org/10.3389/fpsyg.2016.01722
Sekihara K, Sahani M, Nagarajan SS (2005) Localization bias and spatial resolution of adaptive and non-adaptive spatial filters for MEG source reconstruction. NeuroImage 25:1056–1067. https://doi.org/10.1016/j.neuroimage.2004.11.051
Stock A-K, Popescu F, Neuhaus AH, Beste C (2016) Single-subject prediction of response inhibition behavior by event-related potentials. J Neurophysiol 115:1252–1262. https://doi.org/10.1152/jn.00969.2015
Tschentscher N, Mitchell D, Duncan J (2017) Fluid intelligence predicts novel rule implementation in a distributed frontoparietal control network. J Neurosci 37:4841–4847. https://doi.org/10.1523/JNEUROSCI.2478-16.2017
Verhaeghen P, Cerella J (2002) Aging, executive control, and attention: a review of meta-analyses. Neurosci Biobehav Rev 26:849–857. https://doi.org/10.1016/S0149-7634(02)00071-4
Verleger R, Metzner MF, Ouyang G et al (2014) Testing the stimulus-to-response bridging function of the oddball-P3 by delayed response signals and residue iteration decomposition (RIDE). NeuroImage 100:271–280. https://doi.org/10.1016/j.neuroimage.2014.06.036
Whitmer AJ, Banich MT (2012) Brain activity related to the ability to inhibit previous task sets: an fMRI study. Cogn Affect Behav Neurosci 12:661–670. https://doi.org/10.3758/s13415-012-0118-6
Williams BR, Hultsch DF, Strauss EH et al (2005) Inconsistency in reaction time across the life span. Neuropsychology 19:88–96. https://doi.org/10.1037/0894-4105.19.1.88
Wolff N, Buse J, Tost J et al (2017a) Modulations of cognitive flexibility in obsessive compulsive disorder reflect dysfunctions of perceptual categorization. J Child Psychol Psychiatry. https://doi.org/10.1111/jcpp.12733
Wolff N, Mückschel M, Beste C (2017b) Neural mechanisms and functional neuroanatomical networks during memory and cue-based task switching as revealed by residue iteration decomposition (RIDE) based source localization. Brain Struct Funct 222:3819–3831. https://doi.org/10.1007/s00429-017-1437-8
Wolff N, Zink N, Stock A-K, Beste C (2017c) On the relevance of the alpha frequency oscillation’s small-world network architecture for cognitive flexibility. Sci Rep 7:13910. https://doi.org/10.1038/s41598-017-14490-x
Wolff N, Giller F, Buse J et al (2018) When repetitive mental sets increase cognitive flexibility in adolescent obsessive-compulsive disorder. J Child Psychol Psychiatry. https://doi.org/10.1111/jcpp.12901
Zanto TP, Toy B, Gazzaley A (2010) Delays in neural processing during working memory encoding in normal aging. Neuropsychologia 48:13–25. https://doi.org/10.1016/j.neuropsychologia.2009.08.003
Zhang R, Stock A-K, Beste C (2016a) The neurophysiological basis of reward effects on backward inhibition processes. NeuroImage 142:163–171. https://doi.org/10.1016/j.neuroimage.2016.05.080
Zhang R, Stock A-K, Fischer R, Beste C (2016b) The system neurophysiological basis of backward inhibition. Brain Struct Funct 221:4575–4587. https://doi.org/10.1007/s00429-016-1186-0
Zink N, Bensmann W, Arning L et al (2019) CHRM2 genotype affects inhibitory control mechanisms during cognitive flexibility. Mol Neurobiol. https://doi.org/10.1007/s12035-019-1521-6
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This work was supported by a Grant from the BMBF 01GL1741C and partly by SFB 940 project B8.
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The research involved young (mean age 24.52, all > 18 years) and elderly (mean age 60.10 years) human participants. Before any of the study’s procedures started, written informed consent was obtained from all subjects. All participants were treated according to the Declaration of Helsinki. The ethics committee of the TU Dresden approved the study. There were no conflicts of interest. The present study was supported by a Grant from the BMBF 01GL1741C and partly by SFB 940 project B8.
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Giller, F., Beste, C. Effects of aging on sequential cognitive flexibility are associated with fronto-parietal processing deficits. Brain Struct Funct 224, 2343–2355 (2019). https://doi.org/10.1007/s00429-019-01910-z
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DOI: https://doi.org/10.1007/s00429-019-01910-z