Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-25T05:46:18.825Z Has data issue: false hasContentIssue false
  • English
  • Français

Cognitive Reserve Proxies Do Not Differentially Account for Cognitive Performance in Patients with Focal Frontal and Non-Frontal Lesions

Published online by Cambridge University Press:  21 April 2020

Sarah E. MacPherson Open the ORCID record for Sarah E. MacPherson [Opens in a new window] ,
Michael Allerhand ,
Sarah Gharooni ,
Daniela Smirni ,
Tim Shallice ,
Edgar Chan  and
Lisa Cipolotti
Sarah E. MacPherson*
Affiliation:
Centre for Cognitive Ageing and Cognitive Epidemiology, University of Edinburgh, Edinburgh, UK Human Cognitive Neuroscience, Department of Psychology, University of Edinburgh, Edinburgh, UK
Michael Allerhand
Affiliation:
Centre for Cognitive Ageing and Cognitive Epidemiology, University of Edinburgh, Edinburgh, UK Department of Psychology, University of Edinburgh, Edinburgh, UK
Sarah Gharooni
Affiliation:
Department of Neuropsychology, National Hospital for Neurology and Neurosurgery, London, UK
Daniela Smirni
Affiliation:
Dipartimento di Scienze Psicologiche, Pedagogiche e della Formazione, Università degli Studi di Palermo, Palermo, Italy
Tim Shallice
Affiliation:
Institute of Cognitive Neuroscience, University College London, UK International School for Advanced Studies (SISSA-ISAS), Trieste, Italy
Edgar Chan
Affiliation:
Department of Neuropsychology, National Hospital for Neurology and Neurosurgery, London, UK
Lisa Cipolotti
Affiliation:
Department of Neuropsychology, National Hospital for Neurology and Neurosurgery, London, UK
*
*Correspondence and reprint requests to: Sarah E. MacPherson, Department of Psychology, PPLS, University of Edinburgh, 7 George Square, Edinburgh, UK, EH8 9JZ. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Objective:

Cognitive reserve (CR) suggests that premorbid efficacy, aptitude, and flexibility of cognitive processing can aid the brain’s ability to cope with change or damage. Our previous work has shown that age and literacy attainment predict the cognitive performance of frontal patients on frontal-executive tests. However, it remains unknown whether CR also predicts the cognitive performance of non-frontal patients.

Method:

We investigated the independent effect of a CR proxy, National Adult Reading Test (NART) IQ, as well as age and lesion group (frontal vs. non-frontal) on measures of executive function, intelligence, processing speed, and naming in 166 patients with focal, unilateral frontal lesions; 91 patients with focal, unilateral non-frontal lesions; and 136 healthy controls.

Results:

Fitting multiple linear regression models for each cognitive measure revealed that NART IQ predicted executive, intelligence, and naming performance. Age also significantly predicted performance on the executive and processing speed tests. Finally, belonging to the frontal group predicted executive and naming performance, while membership of the non-frontal group predicted intelligence.

Conclusions:

These findings suggest that age, lesion group, and literacy attainment play independent roles in predicting cognitive performance following stroke or brain tumour. However, the relationship between CR and focal brain damage does not differ in the context of frontal and non-frontal lesions.

Keywords

Cognitive reserveFrontal lesionNon-frontal lesionNeuropsychological testsAgeAetiology
Type
Regular Research
Information
Journal of the International Neuropsychological Society , Volume 26 , Issue 8 , September 2020 , pp. 739 - 748
Copyright
Copyright © INS. Published by Cambridge University Press, 2020

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Alexander, G.E., Furey, M.L., Grady, C.L., Pietrini, P., Brady, D.R., Mentis, M.J., & Schapiro, M.B. (1997). Association of premorbid intellectual function with cerebral metabolism in Alzheimer’s disease: implications for the cognitive reserve hypothesis. American Journal of Psychiatry, 154(2), 165–172.Google ScholarPubMed
Anthony, M., & Lin, F. (2017). A systematic review for functional neuroimaging studies of cognitive reserve across the cognitive aging spectrum. Archives of Clinical Neuropsychology, 33(8), 937–948.10.1093/arclin/acx125CrossRefGoogle Scholar
Arenaza-Urquijo, E.M., Wirth, M., & Chételat, G. (2015). Cognitive reserve and lifestyle: moving towards preclinical Alzheimer’s disease. Frontiers in Aging Neuroscience, 7, 134.10.3389/fnagi.2015.00134CrossRefGoogle ScholarPubMed
Aridan, N., Pelletier, G., Fellows, L.K., & Schonberg, T. (2019). Is ventromedial prefrontal cortex critical for behavior change without external reinforcement? Neuropsychologia, 124, 208–215.10.1016/j.neuropsychologia.2018.12.008CrossRefGoogle ScholarPubMed
Aron, A.R., Monsell, S., Sahakian, B.J., & Robbins, T.W. (2004). A componential analysis of task-switching deficits associated with lesions of left and right frontal cortex. Brain, 127, 1561–1573.10.1093/brain/awh169CrossRefGoogle ScholarPubMed
Baldo, J.V., Schwartz, S., Wilkins, D., & Dronkers, N.F. (2006). Role of frontal versus temporal cortex in verbal fluency as revealed by voxel-based lesion symptom mapping. Journal of the International Neuropsychological Society, 12(6), 896–900.10.1017/S1355617706061078CrossRefGoogle ScholarPubMed
Barulli, D., & Stern, Y. (2013). Efficiency, capacity, compensation, maintenance, plasticity: emerging concepts in cognitive reserve. Trends in Cognitive Sciences, 17(10), 502–509.10.1016/j.tics.2013.08.012CrossRefGoogle ScholarPubMed
Bastin, C., Yakushev, I., Bahri, M.A., Fellgiebel, A., Eustache, F., Landeau, B., … Salmon, E. (2012). Cognitive reserve impacts on inter-individual variability in resting-state cerebral metabolism in normal aging. Neuroimage, 63(2), 713–722.10.1016/j.neuroimage.2012.06.074CrossRefGoogle ScholarPubMed
Baxendale, S. (2011). IQ and ability across the adult life span. Applied Neuropsychology, 18(3), 164–167.10.1080/09084282.2011.595442CrossRefGoogle ScholarPubMed
Bennett, D.A., Wilson, R.S., Schneider, J.A., Evans, D.A., Mendes de Leon, C.F., Arnold, S.E., … Bienias, J.L. (2003). Education modifies the relation of AD pathology to level of cognitive function in older persons. Neurology, 60(12), 1909–1915.10.1212/01.WNL.0000069923.64550.9FCrossRefGoogle ScholarPubMed
Bozzali, M., Dowling, C., Serra, L., Spano, B., Torso, M., Marra, C., … Cercignani, M. (2015). The impact of cognitive reserve on brain functional connectivity in Alzheimer’s disease. Journal of Alzheimer’s Disease, 44, 243–250.10.3233/JAD-141824CrossRefGoogle ScholarPubMed
Brickman, A.M., Siedlecki, K.L., Muraskin, J., Manly, J.J., Luchsinger, J.A., Yeung, L.K., … Stern, Y. (2011). White matter hyperintensities and cognition: testing the reserve hypothesis. Neurobiology of Aging, 32(9), 1588–1598.10.1016/j.neurobiolaging.2009.10.013CrossRefGoogle ScholarPubMed
Campanella, F., Skrap, M., & Vallesi, A. (2016). Speed-accuracy strategy regulations in prefrontal tumor patients. Neuropsychologia, 82, 1–10.10.1016/j.neuropsychologia.2016.01.008CrossRefGoogle ScholarPubMed
Cipolotti, L., Healy, C., Chan, E., Bolsover, F., Lecce, F., White, M., … Bozzali, M. (2015a). The impact of different aetiologies on the cognitive performance of frontal patients. Neuropsychologia, 68, 21–30.10.1016/j.neuropsychologia.2014.12.025CrossRefGoogle ScholarPubMed
Cipolotti, L., Healy, C., Chan, E., MacPherson, S.E., White, M., Woollett, K., … Shallice, T. (2015b). The effect of age on cognitive performance of frontal patients. Neuropsychologia, 75, 233–241.10.1016/j.neuropsychologia.2015.06.011CrossRefGoogle ScholarPubMed
Cipolotti, L., Molenberghs, P., Dominguez, J., Smith, N., Smirni, D., Xu, T., … Chan, E. (2020). Fluency and rule breaking behaviour in the frontal cortex. Neuropsychologia, 137.10.1016/j.neuropsychologia.2019.107308CrossRefGoogle ScholarPubMed
Crawford, J. R., Parker, D.M., Stewart, L.E., Besson, J.A.O., & De Lacey, G. (1989a). Prediction of WAIS IQ with the National Adult Reading Test cross validation and extension. British Journal of Clinical Psychology, 28, 267–273.10.1111/j.2044-8260.1989.tb01376.xCrossRefGoogle Scholar
Crawford, J.R., Stewart, L.E., Cochrane, R.H.B., Parker, D.M., & Besson, J.A.O. (1989b). Construct validity of the National Adult Reading Test a factor analytic study. Personality and Individual Differences, 10, 585–587.10.1016/0191-8869(89)90043-3CrossRefGoogle Scholar
Darby, R.R., Brickhouse, M., Wolk, D.A., Dickerson, B.C. & Alzheimer’s Disease Neuroimaging Initiative (2017). Effects of cognitive reserve depend on executive and semantic demands of the task. Journal of Neurology, Neurosurgery & Psychiatry, 88(9), 794–802.10.1136/jnnp-2017-315719CrossRefGoogle ScholarPubMed
Deary, I.J., & Brett, C.E. (2015). Predicting and retrodicting intelligence between childhood and old age in the 6-Day Sample of the Scottish Mental Survey 1947. Intelligence, 50, 1–9.10.1016/j.intell.2015.02.002CrossRefGoogle ScholarPubMed
Dehcordi, S.R., Mariano, M., Mazza, M., & Galzio, R.J. (2013). Cognitive deficits in patients with low and high grade gliomas. Journal of Neurosurgical Sciences, 57, 259–266.Google Scholar
Elkins, J.S., Longstreth, W.T., Manolio, T.A., Newman, A.B., Bhadelia, R.A., & Johnston, S. C. (2006). Education and the cognitive decline associated with MRI-defined brain infarct. Neurology, 67(3), 435–440.10.1212/01.wnl.0000228246.89109.98CrossRefGoogle ScholarPubMed
Foubert-Samier, A., Catheline, G., Amieva, H., Dilharreguy, B., Helmer, C., Allard, M., … Dartigues, J.-F. (2012). Education, occupation, leisure activities, and brain reserve: a population-based study. Neurobiology of Aging, 33, 423.e15–423.e25.10.1016/j.neurobiolaging.2010.09.023CrossRefGoogle ScholarPubMed
Gläscher, J., Adolphs, R., Damasio, H., Bechara, A., Rudrauf, D., Calamia, M., … Tranel, D. (2012). Lesion mapping of cognitive control and value-based decision making in the prefrontal cortex. Proceedings of the National Academy of Sciences, 109(36), 14681–14686.10.1073/pnas.1206608109CrossRefGoogle ScholarPubMed
González-Fernández, M., Davis, C., Molitoris, J.J., Newhart, M., Leigh, R., & Hillis, A.E. (2011). Formal education, socioeconomic status, and the severity of aphasia after stroke. Archives of Physical Medicine and Rehabilitation, 92(11), 1809–1813.10.1016/j.apmr.2011.05.026CrossRefGoogle ScholarPubMed
Grafman, J., Salazar, A., Weingartner, H., Vance, S., & Amin, D. (1986). The relationship of brain-tissue loss volume and lesion location to cognitive deficit. The Journal of Neuroscience, 6(2), 301–307.10.1523/JNEUROSCI.06-02-00301.1986CrossRefGoogle ScholarPubMed
Green, R.E., Colella, B., Christensen, B., Johns, K., Frasca, D., Bayley, M., & Monette, G. (2008). Examining moderators of cognitive recovery trajectories after moderate to severe traumatic brain injury. Archives of Physical Medicine and Rehabilitation, 89(12 Supp), S16–224.10.1016/j.apmr.2008.09.551CrossRefGoogle ScholarPubMed
Greenfield, E.A., & Moorman, S.M. (2019). Childhood socioeconomic status and later life cognition: evidence from the Wisconsin Longitudinal Study. Journal of Aging and Health, 31(9), 1589–1615.10.1177/0898264318783489CrossRefGoogle ScholarPubMed
Henry, J.D., & Crawford, J.R. (2004). A meta-analytic review of verbal fluency performance following focal cortical lesions. Neuropsychology, 18, 284–295.10.1037/0894-4105.18.2.284CrossRefGoogle ScholarPubMed
Jefferson, A.L., Gibbons, L.E., Rentz, D.M., Carvalho, J.O., Manly, J., Bennett, D.A., & Jones, R.N. (2011). A Life Course Model of Cognitive Activities, Socioeconomic Status, Education, Reading Ability, and Cognition. Journal of the American Geriatrics Society, 59(8), 1403–1411.10.1111/j.1532-5415.2011.03499.xCrossRefGoogle ScholarPubMed
Jokinen, H., Melkas, S., Madureira, S., Verdelho, A., Ferro, J.M., Fazekas, F., … Erkinjuntti, T. (2016). Cognitive reserve moderates long-term cognitive and functional outcome in cerebral small vessel disease. Journal of Neurology, Neurosurgery, & Psychiatry, 87(12), 1296–1302.10.1136/jnnp-2016-313914CrossRefGoogle ScholarPubMed
Jones, R.N., Manly, J., Glymour, M.M., Rentz, D.M., Jefferson, A.L., & Stern, Y. (2011). Conceptual and Measurement Challenges in Research on Cognitive Reserve. Journal of the International Neuropsychological Society, 17(4), 593–601.10.1017/S1355617710001748CrossRefGoogle ScholarPubMed
Kaleita, T.A., Wellisch, D.K., Cloughesy, T.F., Ford, J.M., Freeman, D., Belin, T.R., & Goldman, J. (2004). Prediction of Neurocognitive Outcome in Adult Brain Tumor Patients. Journal of Neuro-Oncology, 67(1/2), 245–253.10.1023/B:NEON.0000021900.29176.58CrossRefGoogle ScholarPubMed
Kessels, R.P., Eikelboom, W.S., Schaapsmeerders, P., Maaijwee, N.A., Arntz, R.M., van Dijk, E.J., … de Leeuw, F.E. (2017). Effect of formal education on vascular cognitive impairment after stroke: a meta-analysis and study in young-stroke patients. Journal of the International Neuropsychological Society, 23(3), 223–238.10.1017/S1355617716001016CrossRefGoogle ScholarPubMed
Levi, Y., Rassovsky, Y., Agranov, E., Sela-Kaufman, M., & Vakil, E. (2013). Cognitive reserve components as expressed in traumatic brain injury. Journal of the International Neuropsychological Society, 19(6), 664–671.10.1017/S1355617713000192CrossRefGoogle ScholarPubMed
Lindenberger, U., Burzynska, A.Z., & Nagel, I.E. (2013). Heterogeneity in frontal lobe aging. In Stuss, D.T. & Knight, R.T. (Eds.,) Principles of Frontal Lobe Function (pp. 609–627). Oxford: Oxford University Press.Google Scholar
Liu, Y., Cai, Z.-L., Xue, S., Zhou, X., & Wu, F. (2013). Proxies of cognitive reserve and their effects on neuropsychological performance in patients with mild cognitive impairment. Journal of Clinical Neuroscience, 20(4), 548–553.10.1016/j.jocn.2012.04.020CrossRefGoogle ScholarPubMed
Lo, R.Y., & Jagust, W.J. (2013). Effect of cognitive reserve markers on Alzheimer pathologic progression. Alzheimer Disease and Associated Disorders, 27(4), 343–50.10.1097/WAD.0b013e3182900b2bCrossRefGoogle ScholarPubMed
MacPherson, S.E., Turner, M., Bozzali, M., Cipolotti, L., & Shallice, T. (2010). The Elevator Counting Task: Frontal subregions mediating sustained attention performance. Neuropsychologia, 48(12), 3679–3682.10.1016/j.neuropsychologia.2010.07.033CrossRefGoogle Scholar
MacPherson, S.E., Turner, M., Bozzali, M., Cipolotti, L., & Shallice, T. (2016). The Doors and People Test: The effect of frontal lobe lesions on recall and recognition memory performance. Neuropsychology, 30(3), 332–337.10.1037/neu0000240CrossRefGoogle ScholarPubMed
MacPherson, S.E., Healy, C., Allerhand, M., Spano, B., Chan, E., Tudor-Sfetea, C., … Cipolotti, L. (2017). Cognitive reserve and cognitive performance of patients with focal frontal lesions. Neuropsychologia, 96, 19–28.10.1016/j.neuropsychologia.2016.12.028CrossRefGoogle ScholarPubMed
Makin, S.D.J., Doubal, F.N., Shuler, K., Chappell, F.M., Staals, J., Dennis, M.S., … Wardlaw, J.M. (2018). The impact of early-life intelligence quotient on post stroke cognitive impairment. European Stroke Journal, 3(2), 145–156.10.1177/2396987317750517CrossRefGoogle ScholarPubMed
McKenna, P. & Warrington, E.K. (1983). Graded Naming Test. Windsor, Berks: NFER-Nelson Publishing Co. Ltd.Google Scholar
Meng, X., & D’Arcy, C. (2012). Education and dementia in the context of the cognitive reserve hypothesis: a systematic review with meta-analyses and qualitative analyses. PLoS One, 7(6), e38268.10.1371/journal.pone.0038268CrossRefGoogle ScholarPubMed
Milner, B. (1964). Some effects of frontal lobectomay in man. In Warren, J.M. & Akert, K. (Eds.,) The Frontal Granular Cortex And Behaviour (pp. 313–334). New York: McGraw-Hill.Google Scholar
Miotto, E.C., Junior, A.S., Silva, C.C., Cabrera, H.N., Machado, M.A., Benute, G.R., … Teixeira, M.J. (2011). Cognitive impairments in patients with low grade gliomas and high grade gliomas. Arquivos de Neuro-psiquiatria, 69(4), 596–601.10.1590/S0004-282X2011000500005CrossRefGoogle ScholarPubMed
Morbelli, S., & Nobili, F. (2014). Cognitive reserve and clinical expression of Alzheimer’s disease: evidence and implications for brain PET imaging. American Journal of Nuclear Medicine and Molecular Imaging, 4, 239–247.Google ScholarPubMed
Morris, J.C. (2005). Early-stage and preclinical Alzheimer disease. Alzheimer Disease and Associated Disorders, 19(3), 163–165.Google ScholarPubMed
Murphy, P., Shallice, T., Robinson, G., MacPherson, S.E., Turner, M., Woollett, K., Bozzali, M., & Cipolotti, L. (2013). Impairments in proverb interpretation following focal frontal lobe lesions. Neuropsychologia, 51, 2075–2086.10.1016/j.neuropsychologia.2013.06.029CrossRefGoogle ScholarPubMed
Murray, A.D., Staff, R.T., McNeil, C.J., Salarirad, S., Ahearn, T.S., Mustafa, N., & Whalley, L.J. (2011). The balance between cognitive reserve and brain imaging biomarkers of cerebrovascular and Alzheimer’s diseases. Brain, 134(12), 3687–3696.10.1093/brain/awr259CrossRefGoogle ScholarPubMed
Nelson, H.E. (1982). National Adult Reading Test. Windsor, UK: NFER-Nelson.Google Scholar
Nelson, H.E., & Willison, J. (1991). National Adult Reading Test (NART). Windsor, UK: NFER-Nelson.Google Scholar
Nunnari, D., Bramanti, P., & Marino, S. (2014). Cognitive reserve in stroke and traumatic brain injury patients. Neurological Sciences, 35(10), 1513–1518.10.1007/s10072-014-1897-zCrossRefGoogle ScholarPubMed
O’Carroll, R.E. (1987). The inter-rater reliability of the National Adult Reading Test (NART): a pilot study. British Journal of Clinical Psychology, 26, 229–230.10.1111/j.2044-8260.1987.tb01352.xCrossRefGoogle ScholarPubMed
Okonkwo, O.C., Schultz, S.A., Oh, J.M., Larson, J., Edwards, D., Cook, D., … Sager, M.A. (2014). Physical activity attenuates age-related biomarker alterations in preclinical AD. Neurology, 83(19), 1753–1760.10.1212/WNL.0000000000000964CrossRefGoogle ScholarPubMed
Park, D.C., & Reuter-Lorenz, P. (2009). The adaptive brain: aging and neurocognitive scaffolding. Annual Review of Psychology, 60, 173–196.10.1146/annurev.psych.59.103006.093656CrossRefGoogle ScholarPubMed
Perneczky, R., Drzezga, A., Diehl-Schmid, J., Schmid, G., Wohlschläger, A., Kars, S., … Kurz, A. (2006). Schooling mediates brain reserve in Alzheimer’s disease: findings of fluoro-deoxy-glucose-positron emission tomography. Journal of Neurology, Neurosurgery & Psychiatry, 77(9), 1060–1063.10.1136/jnnp.2006.094714CrossRefGoogle ScholarPubMed
Perret, E. (1974). The left frontal lobe of man and the suppression of habitual responses in verbal categorical behaviour. Neuropsychologia, 12, 323–330.10.1016/0028-3932(74)90047-5CrossRefGoogle ScholarPubMed
Raven, J.C. (1976). Manual for The Advanced Progressive Matrices: Set 1. San Antonio: Psychological Corporation.Google Scholar
Reitan, R.M. (1992). Trail Making Test: Manual For Administration And Scoring. Tucson, AZ: Reitan Neuropsychology Laboratory.Google Scholar
Reuter-Lorenz, P.A., & Park, D.C. (2014). How does it STAC up? Revisiting the scaffolding theory of aging and cognition. Neuropsychology Review, 24(3), 355–370.10.1007/s11065-014-9270-9CrossRefGoogle ScholarPubMed
Robertson, I.H. (2014). A right hemisphere role in cognitive reserve. Neurobiology of Aging, 35(6), 1375–1385.10.1016/j.neurobiolaging.2013.11.028CrossRefGoogle ScholarPubMed
Robinson, G., Shallice, T., Bozzali, M., & Cipolotti, L. (2012). The differing roles of the frontal cortex in fluency tests. Brain, 135(7), 2202–2214.10.1093/brain/aws142CrossRefGoogle ScholarPubMed
Robinson, G.A., Cipolotti, L., Walker, D.G., Biggs, V., Bozzali, M., & Shallice, T. (2015). Verbal suppression and strategy use: a role for the right lateral prefrontal cortex? Brain, 138(4), 1084–1096.10.1093/brain/awv003CrossRefGoogle ScholarPubMed
Roca, M., Parr, A., Thompson, R., Woolgar, A., Torralva, T., Antoun, N., … Duncan, J., (2010). Executive function and fluid intelligence after frontal lobe lesions. Brain, 133(1), 234–247.10.1093/brain/awp269CrossRefGoogle ScholarPubMed
Ryan, N.S., & Rossor, M.N. (2011). Defining and describing the pre-dementia stages of familial Alzheimer’s disease. Alzheimer’s Research & Therapy, 3(5), 29.10.1186/alzrt91CrossRefGoogle ScholarPubMed
Rzezak, P., Squarzoni, P., Duran, F.L., Alves, T. de T.F., Tamashiro-Duran, J., Bottino, C.M., … Busatto, G.F. (2015) Relationship between brain age-related reduction in gray matter and educational attainment. PLoS One, 10, e0140945.10.1371/journal.pone.0140945CrossRefGoogle ScholarPubMed
Sachdev, P.S., Brodaty, H., Valenzuela, M.J., Lorentz, L., & Koschera, A. (2004). Progression of cognitive impairment in stroke patients. Neurology, 63(9), 1618–1623.10.1212/01.WNL.0000142964.83484.DECrossRefGoogle ScholarPubMed
Scarmeas, N., Albert, S.M., Manly, J.J., & Stern, Y. (2006). Education and rates of cognitive decline in incident Alzheimer’s disease. Journal of Neurology, Neurosurgery & Psychiatry, 77(3), 308–316.10.1136/jnnp.2005.072306CrossRefGoogle ScholarPubMed
Schlosser, B., & Ivison, N.D. (1989). Assessing memory deterioration with the Wechsler Memory Scale, the National Adult Reading Test, and the Schonell Graded Word Reading Test. Journal of Clinical and Experimental Neuropsychology, 11, 785–792.10.1080/01688638908400935CrossRefGoogle ScholarPubMed
Schmand, B., Smit, J.H., Geerlings, M.I., & Lindeboom, J. (1997). The effects of intelligence and education on the development of dementia. A test of the brain reserve hypothesis. Psychological Medicine, 27(6), 1337–1344.10.1017/S0033291797005461CrossRefGoogle ScholarPubMed
Serra, L., Musicco, M., Cercignani, M., Torso, M., Spanò, B., Mastropasqua, C., … Bozzali, M. (2014). Cognitive reserve and the risk for Alzheimer’s disease: a longitudinal study. Neurobiology of Aging, 36(2), 592–600.10.1016/j.neurobiolaging.2014.10.010CrossRefGoogle ScholarPubMed
Siedlecki, K.L., Stern, Y., Reuben, A., Sacco, R.L., Elkind, M.S., & Wright, C.B. (2009). Construct validity of cognitive reserve in a multiethnic cohort: The Northern Manhattan Study. Journal of the International Neuropsychological Society, 15(4), 558–569.10.1017/S1355617709090857CrossRefGoogle Scholar
Singh-Manoux, A., Marmot, M.G., Glymour, M., Sabia, S., Kivimäki, M., & Dugravot, A. (2011). Does cognitive reserve shape cognitive decline? Annals of Neurology, 70(2), 296–304.CrossRefGoogle ScholarPubMed
Sperber, C., & Karnath, H.O. (2017). Impact of correction factors in human brain lesion behavior inference. Human Brain Mapping, 38(3), 1692–1701.10.1002/hbm.23490CrossRefGoogle ScholarPubMed
Staff, R.T., Murray, A.D., Ahearn, T.S., Mustafa, N., Fox, H.C., & Whalley, L.J. (2012). Childhood socioeconomic status and adult brain size: childhood socioeconomic status influences adult hippocampal size. Annals of Neurology, 71, 653–660.10.1002/ana.22631CrossRefGoogle ScholarPubMed
Stamenova, V., Gao, F., Black, S.E., Schwartz, M.L., Kovacevic, N., Alexander, M.P., … Levine, B. (2017). The effect of focal cortical frontal and posterior lesions on recollection and familiarity in recognition memory. Cortex, 91, 316–326.10.1016/j.cortex.2017.04.003CrossRefGoogle ScholarPubMed
Stern, Y. (2002). What is cognitive reserve? Theory and research application of the reserve concept. Journal of the International Neuropsychological Society, 8(3), 448–460.10.1017/S1355617702813248CrossRefGoogle ScholarPubMed
Stern, Y. (2006). Cognitive reserve and Alzheimer disease. Alzheimer Disease & Associated Disorders, 20(2), 112–117.10.1097/01.wad.0000213815.20177.19CrossRefGoogle ScholarPubMed
Stern, Y. (2009). Cognitive reserve. Neuropsychologia, 47(10), 2015–2028.CrossRefGoogle ScholarPubMed
Stern, Y. (2012). Cognitive reserve in ageing and Alzheimer’s disease. Lancet Neurology, 11(11), 1006–1012.10.1016/S1474-4422(12)70191-6CrossRefGoogle ScholarPubMed
Stern, Y., Zarahn, E., Habeck, C., Holtzer, R., Rakitin, B.C., Kumar, A., … Brown, T. (2008). A common neural network for cognitive reserve in verbal and object working memory in young but not old. Cerebral Cortex, 18, 959–967.10.1093/cercor/bhm134CrossRefGoogle Scholar
Stuss, D.T., Alexander, M.P., Hamer, L., Palumbo, C., Dempster, R., Binns, M., … Izukawa, D. (1998). The effects of focal anterior and posterior brain lesions on verbal fluency. Journal of the International Neuropsychological Society, 4, 265–278.10.1017/S1355617798002653CrossRefGoogle ScholarPubMed
Stuss, D.T., Alexander, M.P., Shallice, T., Picton, T.W., Binns, M.A., Macdonald, R., … Katz, D.I. (2005). Multiple frontal systems controlling response speed. Neuropsychologia, 43(3), 396–417.10.1016/j.neuropsychologia.2004.06.010CrossRefGoogle ScholarPubMed
Suchy, Y., Kraybill, M.L., & Franchow, E. (2011). Instrumental activities of daily living among community-dwelling older adults: discrepancies between self-report and performance are mediated by cognitive reserve. Journal of Clinical and Experimental Neuropsychology, 33(1), 92–100.10.1080/13803395.2010.493148CrossRefGoogle ScholarPubMed
Suo, C., Lèon, I., Brodaty, H., Trollor, J., Wen, W., Sachdev, P., & Valenzuela, M.J. (2012). Supervisory experience at work is linked to low rate of hippocampal atrophy in late life. NeuroImage, 63, 1542–1551.10.1016/j.neuroimage.2012.08.015CrossRefGoogle ScholarPubMed
Thompson-Schill, S.L., Swick, D., Farah, M.J., D’Esposito, M., Kan, I.P., & Knight, R.T. (1998). Verb generation in patients with focal frontal lesions: a neuropsychological test of neuroimaging findings. Proceedings of the National Academy of Sciences, U.S.A., 95(26), 15855–15860.10.1073/pnas.95.26.15855CrossRefGoogle ScholarPubMed
Tombaugh, T.N., Kozak, J., Rees, L. (1999) Normative data stratified by age and education for two measures of verbal fluency: FAS and animal naming. Archives of Clinical Neuropsychology, 14(2), 167–177.Google ScholarPubMed
Troyer, A.K., Moscovitch, M., Winocur, G., Alexander, M.P., & Stuss, D. (1998). Clustering and switching on verbal fluency: the effects of focal frontal and temporal-lobe lesions. Neuropsychologia, 36, 499–504.10.1016/S0028-3932(97)00152-8CrossRefGoogle ScholarPubMed
Tucker, A.M. & Stern, Y. (2011). Cognitive reserve in aging. Current Alzheimer Research, 8(4), 354–360.10.2174/156720511795745320CrossRefGoogle Scholar
Urbanski, M., Brechemier, M.L., Garcin, B., Bendetowicz, D., Thiebaut de Schotten, M., Foulon, C., & Volle, E. (2016). Reasoning by analogy requires the left frontal pole: lesion-deficit mapping and clinical implications. Brain, 139(6), 1783–1799.10.1093/brain/aww072CrossRefGoogle ScholarPubMed
van Kessel, E., Emons, M.A.C., Wajer, I.H., van Baarsen, K.M., Broekman, M.L., Robe, P.A., …Van Zandvoort, M.J.E. (2019). Tumor-related neurocognitive dysfunction in patients with diffuse glioma: a retrospective cohort study prior to antitumor treatment. Neuro-oncology Practice, 6(6), 463–472.CrossRefGoogle ScholarPubMed
Vaqué-Alcázar, L., Sala-Llonch, R., Valls-Pedret, C., Vidal-Piñeiro, D., Fernández-Cabello, S., Bargalló, N., … Bartrés-Faz, D. (2017) Differential age-related gray and white matter impact mediates educational influence on elders’ cognition. Brain Imaging and Behavior, 11, 318–332.CrossRefGoogle ScholarPubMed
Varjačić, A., Mantini, D., Levenstein, J., Slavkova, E.D., Demeyere, N., & Gillebert, C.R. (2018). The role of left insula in executive set-switching: lesion evidence from an acute stroke cohort. Cortex, 107, 92–101.10.1016/j.cortex.2017.11.009CrossRefGoogle ScholarPubMed
Von Hippel, P.T. (2007). Regression with missing Ys: an improved strategy for analyzing multiply imputed data. Sociological Methodology, 37, 83–117.CrossRefGoogle Scholar
Wechsler, D. (1997). WAIS-III: Administration And Scoring Manual: Wechsler Adult Intelligence Scale. San Antonio: Psychological Corporation.Google Scholar
Wechsler, D. (1981). WAIS-R Manual: Wechsler Adult Intelligence Scale-Revised. San Antonio: Psychological Corporation.Google Scholar
Xu, W., Yu, J.-T., Tan, M.-S., & Tan, L. (2015). Cognitive reserve and Alzheimer’s disease. Molecular Neurobiology, 51(1), 187–208.10.1007/s12035-014-8720-yCrossRefGoogle ScholarPubMed
Zieren, N., Duering, M., Peters, N., Reyes, S., Jouvent, E., Hervé, D., … Dichgans, M. (2013). Education modifies the relation of vascular pathology to cognitive function: cognitive reserve in cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy. Neurobiology of Aging, 34(2), 400–407.10.1016/j.neurobiolaging.2012.04.019CrossRefGoogle ScholarPubMed
Supplementary material: File

MacPherson et al. supplementary material

Tables S1-S2

Download MacPherson et al. supplementary material(File)
File 43 KB