Aging Gracefully: Compensatory Brain Activity in High-Performing Older Adults
Abstract
Whereas some older adults show significant cognitive deficits, others perform as well as young adults. We investigated the neural basis of these different aging patterns using positron emission tomography (PET). In PET and functional MRI (fMRI) studies, prefrontal cortex (PFC) activity tends to be less asymmetric in older than in younger adults (Hemispheric Asymmetry Reduction in Old Adults or HAROLD). This change may help counteract age-related neurocognitive decline (compensation hypothesis) or it may reflect an age-related difficulty in recruiting specialized neural mechanisms (dedifferentiation hypothesis). To compare these two hypotheses, we measured PFC activity in younger adults, low-performing older adults, and high-performing older adults during recall and source memory of recently studied words. Compared to recall, source memory was associated with right PFC activations in younger adults. Low-performing older adults recruited similar right PFC regions as young adults, but high-performing older adults engaged PFC regions bilaterally. Thus, consistent with the compensation hypothesis and inconsistent with the dedifferentiation hypothesis, a hemispheric asymmetry reduction was found in high-performing but not in low-performing older adults. The results suggest that low-performing older adults recruited a similar network as young adults but used it inefficiently, whereas high-performing older adults counteracted age-related neural decline through a plastic reorganization of neurocognitive networks.
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Aged individuals who exhibit delocalized activity show better cognitive performance than aged individuals with more localized activity, consistent with the idea that delocalization may be a compensatory response.
“Aged individuals who exhibit delocalized activity show better cognitive performance than aged individuals with more localized activity, consistent with the idea that delocalization may be a compensatory response (3,5).”
From Neural mechanisms of ageing and cognitive decline (2010) · cites this paper as [5]
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Hemispheric asymmetry reduction in older adults: the HAROLD model
Cabeza, R. (2002) · Psychology and Aging · doi:10.1037/0882-7974.17.1.85 · Cited by 2,125 · see citing works
Self-citationAge differences in the frontal lateralization of verbal and spatial working memory revealed by PET
Reuter-Lorenz, P. A., Jonides, J., Smith, E. E., Hartley, A., Miller, A., Marshuetz, C., & Koeppe, R. A. (2000) · Journal of Cognitive Neuroscience · doi:10.1162/089892900561814 · Cited by 998 · see citing works
Cortical Language Activation in Stroke Patients Recovering From Aphasia With Functional MRI
Cao, Y., Vikingstad, E. M., George, K. P., Johnson, A. F., & Welch, K. M. A. (1999) · Stroke · doi:10.1161/01.str.30.11.2331 · Cited by 299 · see citing works
Calautti, C., Serrati, C., & Baron, J.-C. (2001) · Stroke · doi:10.1161/01.str.32.1.139 · Cited by 164 · see citing works
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The adaptive brain: aging and neurocognitive scaffolding
Park, D. C., & Reuter-Lorenz, P. (2009) · Annual Review of Psychology · doi:10.1146/annurev.psych.59.103006.093656 · Cited by 2,790 · see citing works
Insights into the ageing mind: a view from cognitive neuroscience
Hedden, T., & Gabrieli, J. D. E. (2004) · Nature Reviews Neuroscience · doi:10.1038/nrn1323 · Cited by 2,223 · see citing works
The neural bases of momentary lapses in attention
Weissman, D. H., Roberts, K. C., Visscher, K. M., & Woldorff, M. G. (2006) · Nature Neuroscience · doi:10.1038/nn1727 · Cited by 1,566 · see citing works
The cognitive neuroscience of ageing
Grady, C. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3256 · Cited by 1,286 · see citing works
Neural mechanisms of ageing and cognitive decline
Bishop, N. A., Lu, T., & Yankner, B. A. (2010) · Nature · doi:10.1038/nature08983 · Cited by 1,323 · see citing works
Maintenance, reserve and compensation: the cognitive neuroscience of healthy ageing
Cabeza, R., Albert, M., Belleville, S., Craik, F. I. M., Duarte, A., Grady, C. L., Lindenberger, U., Nyberg, L., Park, D. C., Reuter-Lorenz, P. A., et al. (2018) · Nature Reviews Neuroscience · doi:10.1038/s41583-018-0068-2 · Cited by 1,289 · see citing works
Self-citationHarnessing neuroplasticity for clinical applications
Cramer, S. C., Sur, M., Dobkin, B. H., O'Brien, C., Sanger, T. D., Trojanowski, J. Q., Rumsey, J. M., Hicks, R., Cameron, J., Chen, D., et al. (2011) · Brain · doi:10.1093/brain/awr039 · Cited by 1,259 · see citing works
Cognitive Reserve and Alzheimer Disease
Stern, Y. (2006) · Alzheimer Disease & Associated Disorders · doi:10.1097/01.wad.0000213815.20177.19 · Cited by 838 · see citing works
A theoretical framework for the study of adult cognitive plasticity
Lövdén, M., Bäckman, L., Lindenberger, U., Schaefer, S., & Schmiedek, F. (2010) · Psychological Bulletin · doi:10.1037/a0020080 · Cited by 731 · see citing works
Flexible neural mechanisms of cognitive control within human prefrontal cortex.
Braver, T. S., Paxton, J. L., Locke, H. S., & Barch, D. M. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0808187106 · Cited by 689 · see citing works
Development of Anterior Cingulate Functional Connectivity from Late Childhood to Early Adulthood
Kelly, A. M. C., Di Martino, A., Uddin, L. Q., Shehzad, Z., Gee, D. G., Reiss, P. T., Margulies, D. S., Castellanos, F. X., & Milham, M. P. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhn117 · Cited by 572 · see citing works
Age-related alterations in default mode network: Impact on working memory performance
Sambataro, F., Murty, V. P., Callicott, J. H., Tan, H.-Y., Das, S., Weinberger, D. R., & Mattay, V. S. (2010) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2008.05.022 · Cited by 517 · see citing works
Rajah, M. N., & D'Esposito, M. (2005) · Brain · doi:10.1093/brain/awh608 · Cited by 513 · see citing works
Structure–function correlates of cognitive decline in aging
Persson, J., Nyberg, L., Lind, J., Larsson, A., Nilsson, L.-G., Ingvar, M., & Buckner, R. L. (2006) · Cerebral Cortex · doi:10.1093/cercor/bhj036 · Cited by 473 · see citing works
Brain networks associated with cognitive reserve in healthy young and old adults
Stern, Y. (2005) · Cerebral Cortex · doi:10.1093/cercor/bhh142 · Cited by 417 · see citing works
Environment and Brain Plasticity: Towards an Endogenous Pharmacotherapy
Sale, A., Berardi, N., & Maffei, L. (2014) · Physiological Reviews · doi:10.1152/physrev.00036.2012 · Cited by 402 · see citing works
Episodic memory in normal aging and Alzheimer disease: Insights from imaging and behavioral studies
Tromp, D., Dufour, A., Lithfous, S., Pebayle, T., & Després, O. (2015) · Ageing Research Reviews · doi:10.1016/j.arr.2015.08.006 · Cited by 390 · see citing works
Rojkova, K., Volle, E., Urbanski, M., Humbert, F., Dell’Acqua, F., & Thiebaut de Schotten, M. (2016) · Brain Structure and Function · doi:10.1007/s00429-015-1001-3 · Cited by 361 · see citing works
Effects of Healthy Aging on Hippocampal and Rhinal Memory Functions: An Event-Related fMRI Study
Daselaar, S. M., Fleck, M. S., Dobbins, I. G., Madden, D. J., & Cabeza, R. (2005) · Cerebral Cortex · doi:10.1093/cercor/bhj112 · Cited by 392 · see citing works
Self-citationEvolution of the Aging Brain Transcriptome and Synaptic Regulation
Loerch, P. M., Lu, T., Dakin, K. A., Vann, J. M., Isaacs, A., Geula, C., Wang, J., Pan, Y., Gabuzda, D. H., Li, C., et al. (2008) · PLoS ONE · doi:10.1371/journal.pone.0003329 · Cited by 334 · see citing works
Pruessner, J. C., Dedovic, K., Pruessner, M., Lord, C., Buss, C., Collins, L., Dagher, A., & Lupien, S. J. (2010) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2009.02.016 · Cited by 333 · see citing works
Much of late life cognitive decline is not due to common neurodegenerative pathologies
Boyle, P. A., Wilson, R. S., Yu, L., Barr, A. M., Honer, W. G., Schneider, J. A., & Bennett, D. A. (2013) · Annals of Neurology · doi:10.1002/ana.23964 · Cited by 323 · see citing works
Chou, Y.-H., Ton That, V., & Sundman, M. (2020) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2019.08.020 · Cited by 319 · see citing works
Longitudinal evidence for diminished frontal cortex function in aging
Nyberg, L., Salami, A., Andersson, M., Eriksson, J., Kalpouzos, G., Kauppi, K., Lind, J., Pudas, S., Persson, J., & Nilsson, L.-G. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1012651108 · Cited by 290 · see citing works
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Peelle, J. E., Troiani, V., Wingfield, A., & Grossman, M. (2010) · Cerebral Cortex · doi:10.1093/cercor/bhp142 · Cited by 245 · see citing works
Colcombe, S. J., Kramer, A. F., Erickson, K. I., & Scalf, P. (2005) · Psychology and Aging · doi:10.1037/0882-7974.20.3.363 · Cited by 234 · see citing works
Lifespan brain activity, β-amyloid, and Alzheimer's disease
Jagust, W. J., & Mormino, E. C. (2011) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2011.09.004 · Cited by 221 · see citing works
Age-related changes in brain activation during a delayed item recognition task
Zarahn, E., Rakitin, B., Abela, D., Flynn, J., & Stern, Y. (2007) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2006.03.002 · Cited by 179 · see citing works
Noack, H., Lövdén, M., Schmiedek, F., & Lindenberger, U. (2009) · Restorative Neurology and Neuroscience · doi:10.3233/rnn-2009-0496 · Cited by 180 · see citing works
Motor control and neural plasticity through interhemispheric interactions
Takeuchi, N., Oouchida, Y., & Izumi, S.-I. (2012) · Neural Plasticity · doi:10.1155/2012/823285 · Cited by 171 · see citing works
Changes in Cortical Plasticity Across the Lifespan
Freitas, C., Perez, J., Knobel, M., Tormos, J. M., Oberman, L., Eldaief, M., Bashir, S., Vernet, M., Peña-Gómez, C., & Pascual-Leone, A. (2011) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2011.00005 · Cited by 172 · see citing works
False memories with age: neural and cognitive underpinnings
Devitt, A. L., & Schacter, D. L. (2016) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2016.08.030 · Cited by 171 · see citing works
Goble, D. J., Coxon, J. P., Van Impe, A., De Vos, J., Wenderoth, N., & Swinnen, S. P. (2010) · Human Brain Mapping · doi:10.1002/hbm.20943 · Cited by 164 · see citing works
Slowing down: age-related neurobiological predictors of processing speed
Eckert, M. A. (2011) · Frontiers in Neuroscience · doi:10.3389/fnins.2011.00025 · Cited by 162 · see citing works
DELANO-WOOD, L., BONDI, M. W., SACCO, J., ABELES, N., JAK, A. J., LIBON, D. J., & BOZOKI, A. (2009) · Journal of the International Neuropsychological Society · doi:10.1017/s1355617709990257 · Cited by 155 · see citing works
Magnon, V., Dutheil, F., & Vallet, G. T. (2021) · Scientific Reports · doi:10.1038/s41598-021-98736-9 · Cited by 149 · see citing works
Brain Characteristics of Individuals Resisting Age-Related Cognitive Decline over Two Decades
Pudas, S., Persson, J., Josefsson, M., de Luna, X., Nilsson, L.-G., & Nyberg, L. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.2900-12.2013 · Cited by 126 · see citing works
MRI predictors of cognitive change in a diverse and carefully characterized elderly population
Carmichael, O., Mungas, D., Beckett, L., Harvey, D., Tomaszewski Farias, S., Reed, B., Olichney, J., Miller, J., & DeCarli, C. (2012) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2010.01.021 · Cited by 117 · see citing works
Bagarinao, E., Watanabe, H., Maesawa, S., Mori, D., Hara, K., Kawabata, K., Yoneyama, N., Ohdake, R., Imai, K., Masuda, M., et al. (2019) · Scientific Reports · doi:10.1038/s41598-019-47922-x · Cited by 108 · see citing works
Altered deactivation in individuals with genetic risk for Alzheimer's disease
Persson, J., Lind, J., Larsson, A., Ingvar, M., Sleegers, K., Van Broeckhoven, C., Adolfsson, R., Nilsson, L.-G., & Nyberg, L. (2008) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2008.01.026 · Cited by 102 · see citing works
Nissim, N. R., O’Shea, A., Indahlastari, A., Kraft, J. N., von Mering, O., Aksu, S., Porges, E., Cohen, R., & Woods, A. J. (2019) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2019.00340 · Cited by 99 · see citing works
Does subjective sleep affect cognitive function in healthy elderly subjects? The Proof cohort
Saint Martin, M., Sforza, E., Barthélémy, J. C., Thomas-Anterion, C., & Roche, F. (2012) · Sleep Medicine · doi:10.1016/j.sleep.2012.06.021 · Cited by 94 · see citing works
The impact of age-related changes on working memory functional activity
Steffener, J., Brickman, A. M., Rakitin, B. C., Gazes, Y., & Stern, Y. (2009) · Brain Imaging and Behavior · doi:10.1007/s11682-008-9056-x · Cited by 75 · see citing works
Albinet, C. T., Mandrick, K., Bernard, P. L., Perrey, S., & Blain, H. (2014) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2014.00272 · Cited by 65 · see citing works
I: Longitudinal changes in aging brain function
Beason-Held, L. L., Kraut, M. A., & Resnick, S. M. (2008) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2006.10.031 · Cited by 63 · see citing works
Nissim, N. R., O’Shea, A., Indahlastari, A., Telles, R., Richards, L., Porges, E., Cohen, R., & Woods, A. J. (2019) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2019.00051 · Cited by 63 · see citing works
The relationship between episodic long-term memory and white matter integrity in normal aging
Charlton, R. A., Barrick, T. R., Markus, H. S., & Morris, R. G. (2010) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2009.08.018 · Cited by 55 · see citing works
Dynamic functional reorganizations and relationship with working memory performance in healthy aging
Sala-Llonch, R., Arenaza-Urquijo, E. M., Valls-Pedret, C., Vidal-Piñeiro, D., Bargalló, N., Junqué, C., & Bartrés-Faz, D. (2012) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2012.00152 · Cited by 54 · see citing works
Meditation and cognitive ageing: the role of mindfulness meditation in building cognitive reserve.
Malinowski, P., & Shalamanova, L. (2017) · Journal of Cognitive Enhancement · doi:10.1007/s41465-017-0022-7 · Cited by 50 · see citing works
Age-related neural changes during memory conjunction errors
Giovanello, K. S., Kensinger, E. A., Wong, A. T., & Schacter, D. L. (2010) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2009.21274 · Cited by 51 · see citing works
Mormino, E. C. (2014) · Neuropsychology Review · doi:10.1007/s11065-014-9267-4 · Cited by 44 · see citing works
Novel word learning in older adults: A role for sleep?
Kurdziel, L. B. F., Mantua, J., & Spencer, R. M. C. (2017) · Brain and Language · doi:10.1016/j.bandl.2016.05.010 · Cited by 39 · see citing works
The Effects of Amyloid and Tau on Functional Network Connectivity in Older Populations
Wales, R. M., & Leung, H.-C. (2021) · Brain Connectivity · doi:10.1089/brain.2020.0902 · Cited by 26 · see citing works
Li, G., Xia, H., Teng, G., & Chen, A. (2025) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2025.106008 · Cited by 24 · see citing works
Linnet, E., & Roser, M. E. (2012) · Psychology and Aging · doi:10.1037/a0024905 · Cited by 14 · see citing works
Krendl, A. C., & Kensinger, E. A. (2016) · PLOS ONE · doi:10.1371/journal.pone.0152698 · Cited by 11 · see citing works
Sato, S. D., Shah, V. A., Fettrow, T., Hall, K. G., Tays, G. D., Cenko, E., Roy, A., Clark, D. J., Ferris, D. P., Hass, C. J., et al. (2025) · NeuroImage · doi:10.1016/j.neuroimage.2025.121155 · Cited by 6 · see citing works
- Authors
- Cabeza, R., Anderson, N. D., Locantore, J. K., & McIntosh, A. R.
- Affiliations
- Duke University (US)
- University of Toronto (CA)
- Venue
- NeuroImage
- Publisher
- Elsevier BV
- Published
- 2002-11
- Volume
- 17
- Issue
- 3
- Pages
- 1394-1402
- ISSN
- 1053-8119 (ISSN-L)
- OpenAlex
- W2117800611
- Cited by
- 1,964
- References
- 4
- Citations by year
- 2026: 58 · 2025: 63 · 2024: 55 · 2023: 90 · 2022: 63 · 2021: 81 · 2020: 91 · 2019: 116 · 2018: 92 · 2017: 105 · 2016: 104 · 2015: 111 · 2014: 109 · 2013: 105 · 2012: 126
- FWCI
- 50.59
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- NeuroImage (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Alberta Heritage Foundation for Medical Research
- Topics
- Social Sciences › Psychology › Neuropsychology and Physiological Psychology › Aging and Gerontology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Hemispheric Asymmetry in Neuroscience
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neurobiology of Language and Bilingualism
- Keywords
- cognitive aging, compensatory brain activity, prefrontal cortex, hemispheric lateralization, compensation hypothesis, source memory, word recall, older adults, neuroplasticity, neurocognitive decline
- MeSH terms
- Adult, Aged, Aging, Brain Mapping, Cerebral Cortex, Discrimination Learning, Dominance, Cerebral, Face, Female, Humans, Image Processing, Computer-Assisted, Magnetic Resonance Imaging, Male, Memory, Short-Term, Middle Aged, Nerve Net, Neuropsychological Tests, Paired-Associate Learning, Pattern Recognition, Visual, Mental Recall, Reference Values, Retention, Psychology, Tomography, Emission-Computed, Verbal Learning, Prefrontal Cortex, Imaging, Three-Dimensional
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