The neural basis of task-switching in working memory: effects of performance and aging.
Open accessAbstract
We studied the performance of young and senior subjects on a well known working memory task, the Operation Span. This is a dual-task in which subjects perform a memory task while simultaneously verifying simple equations. Positron-emission tomography scans were taken during performance. Both young and senior subjects demonstrated a cost in accuracy and latency in the Operation Span compared with performing each component task alone (math verification or memory only). Senior subjects were disproportionately impaired relative to young subjects on the dual-task. When brain activation was examined for senior subjects, we found regions in prefrontal cortex that were active in the dual-task, but not in the component tasks. Similar results were obtained for young subjects who performed relatively poorly on the dual-task; however, for young subjects who performed relatively well in the dual-task, we found no prefrontal regions that were active only in the dual-task. Results are discussed as they relate to the executive component of task switching.
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Dual tasking may require both WM capacity and IC mechanisms.
“suggesting that dual tasking may require both WM capacity and IC mechanisms (Towse et al., 2000; Smith et al., 2001; Unsworth, 2010; Chein et al., 2011).”
From Training on Working Memory and Inhibitory Control in Young Adults (2016) · cites this paper as Smith et al., 2001
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“One of the few labs to administer CWMS in an imaging environment (Smith et al., 2001) noted this juxtaposition: “…by and large the WM tasks used in neuroimaging are not the kinds of tasks that correlate with higher-level cognition.”
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“An interesting parallel to these findings is a study by Smith et al. (2001) involving task-switching in working memory.”
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“[54], in which only subjects with the lower dual-task performance recruited the left dorsolateral prefrontal cortex.”
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The Neural Basis for Categorization in Semantic Memory
Grossman, M., Smith, E. E., Koenig, P. L., Glosser, G., DeVita, C., Moore, P., & McMillan, C. T. (2002) · NeuroImage · doi:10.1006/nimg.2002.1273 · Cited by 126 · see citing works
“Other work associates dorsolateral prefrontal cortex with the strategic manipulation of information that is being held in working memory ( Smith et al., 1999, 2001 ) and with task switching (Paulus et al., 2001; Rowe and Passingham 2001; Savage et al., 2001; Seger et al., 2000a) in healthy subjects.”
BackgroundResting hippocampal blood flow, spatial memory and aging
Heo, S., Prakash, R. S., Voss, M. W., Erickson, K. I., Ouyang, C., Sutton, B. P., & Kramer, A. F. (2009) · Brain Research · doi:10.1016/j.brainres.2009.12.020 · Cited by 126 · see citing works
“This is in line with studies that have shown a differential detriment to older adults with increased task difficulty (Erickson et al, 2007; Prakash et al., 2009; Smith et al., 2001).”
ResultDifferential effects of age on subcomponents of response inhibition
Sebastian, A., Baldermann, C., Feige, B., Katzev, M., Scheller, E., Hellwig, B., Lieb, K., Weiller, C., Tüscher, O., & Klöppel, S. (2013) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2013.03.013 · Cited by 127 · see citing works
“…other studies indicating that high cognitive load might eventually result in reaching a resource ceiling in older adults, which is reflected in performance decline associated with hypoactivation of neural networks (Cappell et al., 2010; Mattay et al., 2006; Rypma et al., 2007; Smith et al., 2001).”
Changes in gait while backward counting in demented older adults with frontal lobe dysfunction
Allali, G., Kressig, R. W., Assal, F., Herrmann, F. R., Dubost, V., & Beauchet, O. (2007) · Gait & Posture · doi:10.1016/j.gaitpost.2006.12.011 · Cited by 121 · see citing works
CNTRICS Final Task Selection: Working Memory
Barch, D. M., Berman, M. G., Engle, R. F., Jones, J. H., Jonides, J., MacDonald, A. W., Nee, D. E., Redick, T. S., & Sponheim, S. R. (2008) · Schizophrenia Bulletin · doi:10.1093/schbul/sbn153 · Cited by 121 · see citing works
The missing link between action and cognition
Serrien, D. J., Ivry, R. B., & Swinnen, S. P. (2007) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2007.02.003 · Cited by 120 · see citing works
“, poor performing young or elderly subjects (Smith et al., 2001).”
BackgroundHaier, R. J., White, N. S., & Alkire, M. T. (2003) · Intelligence · doi:10.1016/s0160-2896(03)00025-4 · Cited by 119 · see citing works
“Also, deactivation with transcranial magnetic stimulation of the left but not the right BA 37 inhibits object naming (Stewart et al., 2001) and Smith et al. (2001) reported left but not right differences in BA 37/19 between good and poor performers on a task-switching test.”
Increased brain activation during verbal learning in obstructive sleep apnea
Ayalon, L., Ancoli‐Israel, S., Klemfuss, J. Z., Shalauta, M. D., & Drummond, S. P. A. (2006) · NeuroImage · doi:10.1016/j.neuroimage.2006.02.042 · Cited by 117 · see citing works
“For example, decreased activation has been reported in both older adults (Smith et al., 2001) and sleep deprived young adults (Drummond et al., 1999; Thomas et al., 2000) during arithmetic working memory tasks.”
Cerebellum and integration of neural networks in dual-task processing
Wu, T., Liu, J., Hallett, M., Zheng, Z., & Chan, P. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2012.10.004 · Cited by 121 · see citing works
“, 2002, 2006; Wu and Hallett, 2008), while others found no evidence that there are any areas related to dual-task performance (Adcock et al., 2000; Bunge et al., 2000; Jiang, 2004; Klingberg, 1998; Smith et al., 2001), or found”
BackgroundOverrecruitment in the Aging Brain as a Function of Task Demands: Evidence for a Compensatory View
Vallesi, A., McIntosh, A. R., & Stuss, D. T. (2010) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2010.21490 · Cited by 105 · see citing works
“…level, age-related overrecruitment of brain regions often accompanies more complex and demanding task conditions, such as dual versus single tasks (Smith et al., 2001), source versus item memory retrieval (Morcom et al., 2007), or high versus low selection demands in word generation tasks…”
Training on Working Memory and Inhibitory Control in Young Adults
Maraver, M. J., Bajo, M. T., & Gomez-Ariza, C. J. (2016) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2016.00588 · Cited by 96 · see citing works
Working memory capacity and resistance to interference
Oberauer, K., Lange, E. B., & Engle, R. W. (2004) · Journal of Memory and Language · doi:10.1016/j.jml.2004.03.003 · Cited by 97 · see citing works
“... have shown that complex span tasks can be dissociated from simple span tasks (i.e., serial recall tasks without additional processing demand) by factor analysis (Cantor, Engle, & Hamilton, 1991; Conway, Cowan, Bunting, Therriault, & Minkoff, 2002; Engle, Tuholski, Laughlin, & Conway, 1999; Kail & Hall, 2001; Obera…”
BackgroundAging is associated with changes in the neural circuits underlying empathy
Chen, Y.-C., Chen, C.-C., Decety, J., & Cheng, Y. (2013) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2013.10.080 · Cited by 91 · see citing works
“, 1997), and executive function (Smith et al., 2001) suggest that older adults tend to activate more brain regions than their younger counterparts, coinciding with the hemispheric asymmetry reduction in older adults model, which suggests that older adults attempt to compensate for cortical networks that have become le…”
BackgroundNiu, H., Li, X., Chen, Y., Ma, C., Zhang, J., & Zhang, Z. (2012) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.12046 · Cited by 91 · see citing works
“Successful performance is an influential factor in brain activation as measured by functional imaging [36,37].”
BackgroundDubost, V., Annweiler, C., Aminian, K., Najafi, B., Herrmann, F. R., & Beauchet, O. (2007) · Gait & Posture · doi:10.1016/j.gaitpost.2007.03.011 · Cited by 91 · see citing works
“Compared with enumerating animal names, backward counting out loud from 50 is a simple and automatic mental arithmetic task requiring low attention involvement in a sample of healthy young University students [10–12,18,19].”
BackgroundLaguë-Beauvais, M., Brunet, J., Gagnon, L., Lesage, F., & Bherer, L. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2012.09.042 · Cited by 89 · see citing works
“In linewith previous studies, thesefindings suggest a general slowing of RT in older adults, along with a larger age-related deficit in task-switching (e.g., Andrés et al., 2008; Bugg et al., 2007; Davidson et al., 2003; Smith et al., 2001; Verhaeghen and De Meersman, 1998).”
Resolving sentence ambiguity with planning and working memory resources: Evidence from fMRI
Novais-Santos, S., Gee, J. C., Shah, M., Troiani, V., Work, M., & Grossman, M. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2007.03.077 · Cited by 85 · see citing works
“Non-linguistic studies of planning and switching implicate dorsolateral prefrontal cortex (dlPFC) (Braver and Bongiolatti, 2002; Paulus et al., 2001; Rowe and Passingham, 2001; Savage et al., 2001; Seger et al., 2000; Smith et al., 2001; Sylvester et al., 2003).”
BackgroundCognitive Ability, Expertise, and Age Differences in Following Air-Traffic Control Instructions.
Taylor, J. L., O'Hara, R. M., Mumenthaler, M. S., Rosen, A. C., & Yesavage, J. A. (2005) · Psychology and Aging · doi:10.1037/0882-7974.20.1.117 · Cited by 88 · see citing works
“Age differences in inhibitory control, task switching, and interference suppression in WM tasks have been related to age differences in measures of frontal lobe integrity, as measured by functional (Jonides et al., 2000; Smith et al., 2001) and structural MRI (Raz, Gunning-Dixon, Head, Dupuis, & Acker, 1998).”
MethodNeural bases of focusing attention in working memory: An fMRI study based on group differences
Osaka, M., KOMORI, M., MORISHITA, M., & Osaka, N. (2007) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/cabn.7.2.130 · Cited by 87 · see citing works
“Brain-imaging studies have also suggested that the central executive system is located in both DLPFC and anterior cingulate cortex (ACC) (Bunge et al., 2000; D’Esposito et al., 1995; M. Osaka et al., 2003; N. Osaka et al., 2004; Smith et al., 2001; Smith & Jonides, 1999).”
BackgroundFalse working memories? Semantic distortion in a mere 4 seconds
Atkins, A. S., & Reuter‐Lorenz, P. A. (2008) · Memory & Cognition · doi:10.3758/mc.36.1.74 · Cited by 87 · see citing works
“A math equation verification task based on the operation span task (Turner & Engle, 1989) was adapted from Smith et al. (2001).”
MethodNeural basis for generalized quantifier comprehension
McMillan, C. T., Clark, R., Moore, P., DeVita, C., & Grossman, M. (2005) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2005.02.012 · Cited by 84 · see citing works
Working memory capacity and inhibition: Cognitive and social consequences.
Redick, T. S., Heitz, R. P., & Engle, R. W. (2008) · American Psychological Association eBooks · doi:10.1037/11587-007 · Cited by 81 · see citing works
Altered brain activity in healthy seniors: what does it mean?
Persson, J., & Nyberg, L. H. (2006) · Progress in brain research · doi:10.1016/s0079-6123(06)57004-9 · Cited by 77 · see citing works
“Second, observations of less activation in older adults are found in several studies, and this pattern of less activation is most consistent for left VLPFC (e.g., Grady et al., 1998; Jonides et al., 2000; Smith et al., 2001).”
Does Change in Gait while Counting Backward Predict the Occurrence of a First Fall in Older Adults?
Beauchet, O., Allali, G., Annweiler, C., Berrut, G., Maarouf, N., Herrmann, F. R., & Dubost, V. (2008) · Gerontology · doi:10.1159/000127318 · Cited by 70 · see citing works
Toosizadeh, N., Najafi, B., Reiman, E. M., Mager, R. M., Veldhuizen, J., O’Connor, K., ZAMRINI, E. Y., & Mohler, J. M. (2016) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2016.00167 · Cited by 68 · see citing works
Ehsani, H., Mohler, M. J., O’Connor, K., ZAMRINI, E. Y., Tirambulo, C. V. G., & Toosizadeh, N. (2019) · Clinical Interventions in Aging · doi:10.2147/cia.s198697 · Cited by 66 · see citing works
“Firstly, counting involves working memory,(19) and in contrast to some other popular tasks such as naming objects/animals, is more directly related to executive function.(20,21) Secondly, since counting is a rhythmic task, it may substantially interfere with rhythmic tasks of a different frequency such as walking or r…”
BackgroundPrilipko, O., Huynh, N. T., Schwartz, S., Tantrakul, V., Kim, J. H., Peralta, A. R., Kushida, C. A., Paiva, T., & Guilleminault, C. (2011) · SLEEP · doi:10.1093/sleep/34.3.293 · Cited by 64 · see citing works
Sentence Processing Strategies in Healthy Seniors with Poor Comprehension: An fMRI Study
Grossman, M., Cooke, A., DeVita, C., Chen, W., Moore, P., Detre, J. A., Alsop, D. C., & Gee, J. C. (2002) · Brain and Language · doi:10.1006/brln.2001.2581 · Cited by 64 · see citing works
Neural correlates of working memory performance in adolescents and young adults with dyslexia
Vasić, N., Lohr, C., Steinbrink, C., Martin, C., & Wolf, R. C. (2007) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2007.09.002 · Cited by 58 · see citing works
The prefrontal cortex: insights from functional neuroimaging using cognitive activation tasks
Goethals, I., Audenaert, K., de Wiele, C. V., & Dierckx, R. A. J. O. (2003) · European Journal of Nuclear Medicine and Molecular Imaging · doi:10.1007/s00259-003-1382-z · Cited by 55 · see citing works
“Also, Smith et al. [ 81 ] indicated that no supplementary foci of activation were found in a group of participants performing well in the dual task.”
BackgroundSelective Vulnerability Related to Aging in Large-Scale Resting Brain Networks
Zhang, H., Chen, W., Jiao, Y., Xu, Y. Q., Zhang, X., & Wu, J. (2014) · PLoS ONE · doi:10.1371/journal.pone.0108807 · Cited by 52 · see citing works
Quantifier comprehension in corticobasal degeneration
McMillan, C. T., Clark, R., Moore, P., & Grossman, M. (2006) · Brain and Cognition · doi:10.1016/j.bandc.2006.06.005 · Cited by 50 · see citing works
Watanabe, K., & Funahashi, S. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.08.008 · Cited by 50 · see citing works
“Notably, when the same dual task was performed by good and poor performers (i.e., those who showed a weak and strong dual-task interference effect, respectively), dual-task-specific activation in the DLPFC was observed only in the poor performers (Smith et al., 2001).”
Heckner, M. K., Cieslik, E. C., Eickhoff, S. B., Camilleri, J. A., Hoffstaedter, F., & Langner, R. (2020) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_01616 · Cited by 48 · see citing works
Toosizadeh, N., Ehsani, H., Wendel, C. S., ZAMRINI, E. Y., Connor, K. O., & Mohler, J. M. (2019) · Scientific Reports · doi:10.1038/s41598-019-46925-y · Cited by 49 · see citing works
Neural mechanisms of auditory awareness underlying verbal transformations
Kondo, H. M., & Kashino, M. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2007.02.024 · Cited by 47 · see citing works
“, 2000), shifting of attention for task management (Kondo et al., 2004a,b; Smith et al., 2001), and error detection (Gehring and Knight, 2000; Swick and Turken, 2002).”
BackgroundSzameitat, A. J., Schubert, T., & Müller, H. J. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.07.069 · Cited by 48 · see citing works
“, 2006, 2002), others concluded that there are no specific neural correlates of dual-task performance (Adcock et al., 2000; Bunge et al., 2000; Jiang et al., 2004; Klingberg, 1998; Smith et al., 2001), and sometimes even reduced neural activity associated with dual-task performance was reported (Jaeggi et al.”
BackgroundAge-related changes in neural activity during performance matched working memory manipulation
Emery, L., Heaven, T. J., Paxton, J. L., & Braver, T. S. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2008.06.021 · Cited by 46 · see citing works
“These types of divided attention effects are the hallmark of complex WM span tasks, and are well-established to engage DLPFC regions (e.g., DiPisapia et al., 2007; Iidaka, Anderson, Kapur, Cabeza, and Craik, 2000; Smith et al., 2001).”
BackgroundFraser, S., & Bherer, L. (2013) · Wiley Interdisciplinary Reviews Cognitive Science · doi:10.1002/wcs.1252 · Cited by 45 · see citing works
Working Memory and Intelligence
Conway, A. R. A., Getz, S. J., Macnamara, B. N., & de Abreu, P. E. (2011) · Cambridge University Press eBooks · doi:10.1017/cbo9780511977244.021 · Cited by 42 · see citing works
Neural mechanisms of two different verbal working memory tasks: A VLSM study
Ivanova, M. V., Dragoy, O., Kuptsova, S. V., Akinina, S. Y., Петрушевский, А. Г., Николаевна, Ф. О., Turken, A. U., Shklovsky, V. M., & Dronkers, N. F. (2018) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2018.03.003 · Cited by 41 · see citing works
Rypma, B. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.07.062 · Cited by 39 · see citing works
“A number of studies by now indicate that strategic organization and strategy-shifting processes are mediated by dorsolateral PFC (Bor et al., 2003; Prabhakaran et al., 1997, 2001; Smith et al., 2001; Jenkins et al., 1994; Deiber et al., 1991).”
Gilmour, G., Porcelli, S., Bertaina‐Anglade, V., Arce, E., Dukart, J., Hayen, A., Lobo, A., López‐Antón, R., Pich, E. M., Pemberton, D. J., et al. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.09.025 · Cited by 37 · see citing works
“recall, cued recall, recognition) have been conducted, they potentially suggest a common recruitment of lateral prefrontal cortex, anterior cingulate and posterior parietal cingulate areas during task performance (Bunge et al., 2000; Chein et al., 2011; Kondo et al., 2004; Osaka & Osaka, 2002; Osaka et al., 2004; Smit…”
Adult age differences in the effects of processing on storage in working memory: A meta-analysis.
Graham, A. J., & Rhodes, S. (2019) · Psychology and Aging · doi:10.1037/pag0000358 · Cited by 38 · see citing works
Age differences in the neural correlates of distraction regulation: A network interaction approach
Amer, T., Anderson, J. A. E., Campbell, K. L., Hasher, L., & Grady, C. L. (2016) · NeuroImage · doi:10.1016/j.neuroimage.2016.06.036 · Cited by 41 · see citing works
“Conversely, increased activation of the same control areas in younger adults related to worse cognitive performance, suggesting that recruitment of the same control regions in younger adults, at least at this level of demand, reflects less efficient neural functioning (e.g., Park & Reuter-Lorenz, 2009; Reuter-Lorenz &…”
BackgroundDecreased activation of anterior cingulate cortex in the working memory of the elderly
Otsuka, Y., Osaka, N., Morishita, M., Kondo, H. M., & Osaka, M. (2006) · Neuroreport · doi:10.1097/01.wnr.0000236852.63092.9f · Cited by 35 · see citing works
Stimulating aged brains with transcranial direct current stimulation: Opportunities and challenges.
Habich, A., Fehér, K., Antonenko, D., Boraxbekk, C., Flöel, A., Nissen, C., Siebner, H., Thielscher, A., & Klöppel, S. (2020) · Psychiatry research. Neuroimaging · doi:10.1016/j.pscychresns.2020.111179 · Cited by 32 · see citing works
“switching performance in older adults reflect a lower flexibility in allocating the fewer available resources to the relevant task at hand (Smith et al., 2001).”
Background
- Authors
- Smith, E. E., Geva, A., Jonides, J., Miller, A., Reuter-Lorenz, P., & Koeppe, R. A.
- Affiliations
- University of Michigan (US)
- Department of Psychology and Department of Nuclear Medicine, University of Michigan, Ann Arbor, MI 48109
- ORCID
- Koeppe, Robert A.
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2001-02-13
- Volume
- 98
- Issue
- 4
- Pages
- 2095-2100
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC29387
- OpenAlex
- W2097263602
- Cited by
- 200
- References
- 22
- Citations by year
- 2026: 2 · 2025: 3 · 2024: 2 · 2023: 8 · 2022: 5 · 2021: 10 · 2020: 6 · 2019: 6 · 2018: 3 · 2017: 6 · 2016: 5 · 2015: 8 · 2014: 6 · 2013: 9 · 2012: 7
- FWCI
- 5.94
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Cognitive Abilities and Testing
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Cognitive Functions and Memory
- Keywords
- task switching, working memory, operation span, aging, dual-task performance, prefrontal cortex, brain activation, executive function, older adults, individual differences in performance
- MeSH terms
- Adult, Aged, Aging, Brain, Female, Humans, Male, Memory, Neurons, Task Performance and Analysis, Tomography, Emission-Computed
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