Cognitive reserve impacts on inter-individual variability in resting-state cerebral metabolism in normal aging

[en] There is a great deal of heterogeneity in the impact of aging on cognition and cerebral functioning. One potential factor contributing to individual differences among the elders is the cognitive reserve, which designates the partial protection from the deleterious effects of aging that lifetime experience provides. Neuroimaging studies examining task-related activation in elderly people suggested that cognitive reserve takes the form of more efficient use of brain networks and/or greater ability to recruit alternative networks to compensate for age-related cerebral changes. In this multi-centre study, we examined the relationships between cognitive reserve, as measured by education and verbal intelligence, and cerebral metabolism at rest (FDG-PET) in a sample of 74 healthy older participants. Higher degree of education and verbal intelligence was associated with less metabolic activity in the right posterior temporoparietal cortex and the left anterior intraparietal sulcus. Functional connectivity analyses of resting-state fMRI images in a subset of 41 participants indicated that these regions belong to the default mode network and the dorsal attention network respectively. Lower metabolism in the temporoparietal cortex was also associated with better memory abilities. The findings provide evidence for an inverse relationship between cognitive reserve and resting-state activity in key regions of two functional networks respectively involved in internal mentation and goal-directed attention.

Disciplines :

Neurosciences & behavior

Author, co-author :

Bastin, Christine ; Université de Liège - ULiège > Centre de recherches du cyclotron

Yakushev, Igor

Bahri, Mohamed Ali ; Université de Liège - ULiège > Centre de recherches du cyclotron

Fellgiebel, Andreas

Eustache, Francis

Landeau, Brigitte

Scheurich, Armin

Feyers, Dorothée ; Université de Liège - ULiège > Département Psychologies et cliniques des systèmes humains > Psychologie de la sénescence

Collette, Fabienne ; Université de Liège - ULiège > Département de Psychologie : cognition et comportement > Neuropsychologie

Chételat, Gael

Salmon, Eric ; Université de Liège - ULiège > Département des sciences cliniques > Neuroimagerie des troubles de la mémoire et révalid. cogn.

Language :

English

Title :

Cognitive reserve impacts on inter-individual variability in resting-state cerebral metabolism in normal aging

Publication date :

2012

Journal title :

NeuroImage

ISSN :

1053-8119

eISSN :

1095-9572

Publisher :

Elsevier Science, Orlando, United States - Florida

Volume :

Pages :

713-722

Peer reviewed :

Peer Reviewed verified by ORBi

Commentary :

Gael Chételat and Eric Salmon equally contributed to this work.

Available on ORBi :

since 06 September 2012

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Bibliography

Albert M.S., Jones K., Savage C.R., Berkman L., Seeman T., Blazer D., Rowe J.W. Predictors of cognitive change in older persons: MacArthur studies of successful aging. Psychol. Aging 1995, 10(4):578-589.
Alexander G.E., Furey M.L., Grady C.L., Pietrini P., Brady D.R., Mentis M.J., Schapiro M.B. Association of premorbid intellectual function with cerebral metabolism in Alzheimer's disease: implications for the cognitive reserve hypothesis. Am. J. Psychiatry 1997, 154(2):165-172.
Andrés P., Van der Linden M. Age-related differences in supervisory attentional system functions. J. Gerontol. B Psychol. Sci. Soc. Sci. 2000, 55B:373-380.
Andrews-Hanna J.R., Snyder A.Z., Vincent J.L., Lustig C., Head D., Raichle M.E., Buckner R.L. Disruption of large-scale brain systems in advanced aging. Neuron 2007, 56(5):924-935.
Andrews-Hanna J.R., Reidler J.S., Sepulcre J., Poulin R., Buckner R.L. Functional-anatomic fractionation of the brain's default network. Neuron 2010, 65:550-562.
Bartrés-Faz D., Arenaza-Urquijo E.M. Structural and functional imaging correlates of cognitive and brain reserve hypotheses in healthy and pathological aging. Brain Topogr. 2011, 24(3-4):340-357.
Bartrés-Faz D., Solé-Padullés C., Junque C., Rami L., Bosch B., Bargallo N., Falcon C., Sanchez-Valle R., Molinuevo J.L. Interactions of cognitive reserve with regional brain anatomy and brain function during a working memory task in healthy elders. Biol. Psychol. 2009, 80(2):256-259.
Bastin C., Feyers D., Jedidi H., Bahri M.A., Degueldre C., Lemaire C., Colette F., Salmon E. Episodic autobiographical memory in amnestic mild cognitive impairment: what are the neural correlates?. Hum. Brain Mapp. 2012, 10.1002/hbm.22032.
Boivin M.J., Giordani B., Berent S., Amato D.A., Lehtinen S., Koeppe R.A., Buchtel H.A., Foster N.L., Kuhl D.E. Verbal fluency and positron emission tomographic mapping of regional cerebral glucose metabolism. Cortex 1992, 28(2):231-239.
Boly M., Tshibanda L., Vanhaudenhuyse A., Noirhomme Q., Schnakers C., Ledoux D., Boveroux P., Garweg C., Lambermont B., Phillips C., Luxen A., Moonen M., Bassetti C., Maquet P., Laureys S. Functional connectivity in the default network during resting state is preserved in a vegetative but not in a brain dead patient. Hum. Brain Mapp. 2009, 30(8):2393-2400.
Bosch B., Bartrés-Faz D., Rami L., Arenaza-Urquijo E.M., Fernandez-Espejo D., Junqué C., Solé-Padulles C., Sanchez-Valle R., Bargallo N., Falcon C., Molinuevo J.L. Cognitive reserve modulates task-induced activations and deactivations in healthy elders, amnestic mild cognitive impairment and mild Alzheimer's disease. Cortex 2010, 46(4):451-461.
Buckner R.L., Andrews-Hanna J.R., Schacter D.L. The brain's default network. Ann. N. Y. Acad. Sci. 2008, 1124:1-38.
Buckner R.L., Sepulcre J., Talukdar T., Krienen F.M., Liu H., Hedden T., Andrews-Hanna J.R., Sperling R.A., Johnson K.A. Cortical hubs revealed by intrinsic functional connectivity: mapping, assessment of stability, and relation to Alzheimer's disease. J. Neurosci. 2009, 29(6):1860-1873.
Cabeza R., Anderson N.D., Locantore J.K., McIntosh A.R. Aging gracefully: compensatory brain activity in high-performing older adults. NeuroImage 2002, 17:1394-1402.
Christensen H. What cognitive changes can be expected in normal ageing?. Aust. N. Z. J. Psychiatry 2001, 35:768-775.
Christensen H., Mackinnon A.J., Korten A.E., Jorm A.F., Henderson A.S., Jacomb P., Rodgers B. An analysis of diversity in the cognitive performance of elderly community dwellers: individual differences in change scores as a function of age. Psychol. Aging 1999, 14(3):365-379.
Collette F., Van der Linden M., Laureys S., Delfiore G., Degueldre C., Luxen A., Salmon E. Exploring the unity and diversity of the neural substrates of executive functioning. Hum. Brain Mapp. 2005, 25:409-423.
Corbetta M., Shulman G.L. Control of goal-directed and stimulus-driven attention in the brain. Nat. Rev. Neurosci. 2002, 3:201-215.
Cowan N. The focus of attention as observed in visual working memory tasks: making sense of competing claims. Neuropsychologia 2011, 49(6):1401-1406.
Craik F.I.M., Salthouse T.A. The Handbook of Aging and Cognition 2000, Lawrence Erlbaum Associates, Mahwah, NJ.
Damoiseaux J.S., Beckmann C.F., Sanz Arigita E.J., Barkhof F., Scheltens P., Stam C.J., Smith S.M., Rombouts S.A.R.B. Reducted resting-state brain activity in the "default network" in normal aging. Cereb. Cortex 2008, 18:1856-1864.
D'Argembeau A., Jedidi H., Balteau E., Bahri M.A., Phillips C., Salmon E. Valuing one's self: medial prefrontal involvement in epistemic and emotive investments in self-views. Cereb. Cortex 2012, 22(3):659-667.
Davidson P.S.R., Glisky E.L. Neuropsychological correlates of recollection and familiarity in normal aging. Cogn. Affect. Behav. Neurosci. 2002, 2(2):174-186.
Deichmann R., Schwarzbauer C., Turner R. Optimisation of the 3D MDEFT sequence for anatomical brain imaging: technical implications at 1.5 and 3T. NeuroImage 2004, 21:757-767.
Deltour J.J. Echelle de vocabulaire de Mill Hill de J.C. Raven. Adaptation francaise et normes comparées du Mill Hill et du Standard Progressive Matrices (PM 38). Manuel. Braine-le-Château: Editions l'Application des Techniques Modernes 1993.
Desmette D., Hupet M., Van der Linden M. Adaptation en langue francaise du "Reading span test" de Daneman et Carpenter (1980). Annee Psychol. 1995, 95:459-482.
Duarte A., Ranganath C., Trujillo C., Knight R.T. Intact recollection memory in high-performing older adults: ERP and behavioral evidence. J. Cogn. Neurosci. 2006, 18(1):33-47.
Eustache F., Desgranges B., Lalevée C. Clinical evaluation of memory. Rev. Neurol. 1998, 154(Suppl. 2):S18-S32.
Fox M.D., Raichle M.E. Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat. Rev. Neurosci. 2007, 8(9):700-711.
Fox M.D., Snyder A.Z., Vincent J.L., Corbetta M., Van Essen D.C., Raichle M.E. The human brain is instrinsically organized into dynamic, anticorrelated functional networks. Proc. Natl. Acad. Sci. 2005, 102(27):9673-9678.
Fox M.D., Corbetta M., Snyder A.Z., Vincent J.L., Raichle M.E. Spontaneous neuronal activity distinguishes human dorsal and ventral attention systems. Proc. Natl. Acad. Sci. 2006, 103(26):10046-10051.
Glisky E.L., Polster M.R., Routhieaux B.C. Double dissociation between item and source memory. Neuropsychology 1995, 9(2):229-235.
Grady C.L. Cognitive neuroscience of aging. Ann. N. Y. Acad. Sci. 2008, 1124:127-144.
Greicius M.D., Srivastava G., Reiss A.L., Menon V. Default-mode network activity distinguishes Alzheimer's disease from healthy aging: evidence from functional MRI. Proc. Natl. Acad. Sci. 2004, 101(13):4637-4642.
Gutchess A.H., Welsh R.C., Hedden T., Bangert A., Minear M., Liu L.L., Park D.C. Aging and the neural correlates of successful picture encoding: frontal activations compensate for decreased medial-temporal activity. J. Cogn. Neurosci. 2005, 17(1):84-96.
Haier R.J., Siegel B.V., MacLachlan A., Soderling E., Lottenberg S., Buchsbaum M.S. Regional glucose metabolic changes after learning a complex visuospatial/motor task: a positron emission tomographic study. Brain Res. 1992, 570:134-143.
Haier R.J., Siegel B., Tang C., Abel L., Buchsbaum M.S. Intelligence and changes in regional cerebral glucose metabolic rate following learning. Intelligence 1992, 16(3-4):415-426.
Hanyu H., Sato T., Shimizu S., Kanetaka H., Iwamoto T., Koizumi K. The effect of education on rCBF changes in Alzheimer's disease: a longitudinal SPECT study. Eur. J. Nucl. Mol. Imaging 2008, 35:2182-2190.
Hassabis D., Maguire E.A. Deconstructing episodic memory with construction. Trends Cogn. Sci. 2007, 11(7):299-306.
Hazlett E.A., Buchsbaum M.S., Mohs R.C., Spiegel-Cohen J., Wei T.-C., Azueta R., Haznedar M.M., Singer M.B., Shihabuddin L., Luu-Hsia C., Harvey P.D. Age-related shift in brain region activity during successful memory performance. Neurobiol. Aging 1998, 19(5):437-445.
Helmstaedter C., Lendt M., Lux S. VLMT Verbaler Lern- und Merkfähigkeitstest 2001, Beltz Test GmbH, Göttingen.
Kemppainen N.M., Aalto S., Karrasch M., Nagren K., Savisto N., Oikonen V., Viitanen M., Parkkola R., Rinne J.O. Cognitive reserve hypothesis: Pittsburgh Compound B and fluorodeoxyglucose positron emission tomography in relation to education in mild Alzheimer's disease. Ann. Neurol. 2008, 63(1):112-118.
Lee D.S., Kang H., Kim H., Park H., Oh J.S., Lee J.S., Lee M.C. Metabolic connectivity by interregional correlation analysis using statistical parametric mapping (SPM) and FDG brain PET; methodological development and patterns of metabolic connectivity in adults. Eur. J. Nucl. Med. Mol. Imaging 2008, 35(9):1681-1691.
Lustig C., Snyder A.Z., Bhakta M., O'Brien K.C., McAvoy M., Raichle M.E., Morris J.C., Buckner R.L. Functional deactivations: change with age and dementia of the Alzheimer type. Proc. Natl. Acad. Sci. 2003, 100(24):14504-14509.
Majerus S., D'Argembeau A., Martinez Perez T., Belayachi S., Van der Linden M., Collette F., Salmon E., Seurinck R., Fias W., Maquet P. The commonality of neural networks for verbal and visual short-term memory. J. Cogn. Neurosci. 2010, 22(11):2570-2593.
Majerus S., Attout L., D'Argembeau A., Degueldre C., Fias W., Maquet P., Van der Linden M., Phillips C., Balteau E. Attention supports verbal short-term memory via competition between dorsal and ventral attention networks. Cereb. Cortex 2012, 22(5):1086-1097.
Manly J.J., Schupf N., Tang M.X., Stern Y. Cognitive decline and literacy among ethnically diverse elders. J. Geriatr. Psychiatry Neurol. 2005, 18(4):213-217.
Mattis S. Dementia Rating Scale 1973, NFER-Nelson, Windsor, England.
Mevel K., Desgranges B., Baron J.C., Landeau B., De La Sayette V., Viader F., Eustache F., Chételat G. Detecting hippocampal hypometabolism in mild cognitive impairment using automatic voxel-based approaches. NeuroImage 2007, 37:18-25.
Murray A.D., Staff R.T., McNeil C.J., Salarirad S., Ahearn T.S., Mustafa N., Whalley L.J. The balance between cognitive reserve and brain imaging biomarkers of cerebrovascular and Alzheimer's diseases. Brain 2011, 134:3687-3696.
Neubauer A.C., Grabner R.H., Fink A., Neuper C. Intelligence and neural efficiency: further evidence of the influence of task content and sex on the brain-IQ relationship. Cogn. Brain Res. 2005, 25:217-225.
Park D., Schwartz N. Cognitive Aging: A Primer 2000, Psychology Press, Hove, UK.
Parks R.W., Loewenstein D.A., Dodrill K.L., Barker W.W., Yoshii F., Chang J.Y., Emran A., Apicella A., Sheramata W.A., Duara R. Cerebral metabolic effects of a verbal fluency test: a PET scan study. J. Clin. Exp. Neuropsychol. 1988, 10(5):565-575.
Perneczky R., Drzezga A., Diehl-Schmid J., Schmid G., Wohlschlager A., Kars S., Grimmer T., Wagenpfeil S., Monsch A., Kurz A. Schooling mediates brain reserve in Alzheimer's disease: findings of fluoro-deoxy-glucose-positron emission tomography. J. Neurol. Neurosurg. Psychiatry 2006, 77(9):1060-1063.
Persson J., Lustig C., Nelson J.K., Reuter-Lorenz P.A. Age differences in deactivation: a link to cognitive control?. J. Cogn. Neurosci. 2007, 19(6):1021-1032.
Raz N. Aging of the brain and its impact on cognitive performance: integration of structural and functional findings. The handbook of aging and cognition 2000, vol. Second:1-90. Lawrence Erlbaum Associates, Mahwah, NJ.
Raz N., Lindenberger U., Rodrigue K.M., Kennedy K.M., Head D., Williamson A., Dahle C., Gerstorf D., Acker J.D. Regional brain changes in aging healthy adults: general trends, individual differences and modifiers. Cereb. Cortex 2005, 15:1676-1689.
Reuter-Lorenz P.A., Park D.C. Human neuroscience and the aging mind: a new look at old problems. J. Gerontol. B Psychol. Sci. Soc. Sci. 2010, 65B(4):405-415.
Rocher A.B., Chapon F., Blaizot X., Baron J.C., Chavoix C. Resting-state brain glucose utilization as measured by PET is directly related to regional synaptophysin levels: a study in baboons. NeuroImage 2003, 20(3):1894-1898.
Ruff C.C., Knauff M., Fangmeier T., Spreer J. Reasoning and working memory: common and distinct neuronal processes. Neuropsychologia 2003, 41(9):1241-1253.
Rypma B., Berger J.S., Prabhakaran V., Bly B.M., Kimberg D.Y., Biswal B.B., D'Esposito M. Neural correlates of cognitive efficiency. NeuroImage 2006, 33:969-979.
Saxe R., Kanwisher N. People thinking about thinking people: the role of the temporo-parietal junction in "theory of mind". NeuroImage 2003, 19:1835-1842.
Scarmeas N., Zarahn E., Anderson K.E., Habeck C.G., Hilton J., Flynn J., Marder K.S., Bell K.L., Sackeim H.A., Van Heertum R.L., Moeller J.R., Stern Y. Association of life activities with cerebral blood flow in Alzheimer disease: implications for the cognitive reserve hypothesis. Arch. Neurol. 2003, 60(3):359-365.
Scarmeas N., Zarahn E., Anderson K.E., Hilton J., Flynn J., Van Heertum R.L., Sackeim H.A., Stern Y. Cognitive reserve modulates functional brain responses during memory tasks: a PET study in healthy young and elderly subjects. NeuroImage 2003, 19(3):1215-1227.
Schacter D.L., Addis D.R., Buckner R.L. Remembering the past to imaging the future: the prospective brain. Nat. Rev. Neurosci. 2007, 8:657-661.
Schmidt K.-H., Metzler P. Wortschatztest. WST. Testmappe 1992, Beltz, Germany, Weinheim.
Siedlecki K.L., Stern Y., Reuben A., Sacco R.L., Elkind M.S., Wright C.B. Construct validity of cognitive reserve in a multiethnic cohort: the Northern Manhattan Study. J. Int. Neuropsychol. Soc. 2009, 15(4):558-569.
Solé-Padullés C., Bartrés-Faz D., Junqué C., Vendrell P., Rami L., Clemente I.C., Bosch B., Villar A., Bargallo N., Jurado M.A., Barrios M., Molinuevo J.L. Brain structure and function related to cognitive reserve variables in normal aging, mild cognitive impairment and Alzheimer's disease. Neurobiol. Aging 2009, 30(7):1114-1124.
Springer M.V., McIntosh A.R., Winocur G., Grady C.L. The relation between brain activity during memory tasks and years of education in young and older adults. Neuropsychology 2005, 19(2):181-192.
Steffener J., Stern Y. Exploring the neural basis of cognitive reserve in aging. Biochim. Biophys. Acta 2012, 1822(3):467-473.
Steffener J., Reuben A., Rakitin B.C., Stern Y. Supporting performance in the face of age-related neural changes: testing mechanistic roles of cognitive reserve. Brain Imaging Behav. 2011, 5(3):212-221.
Stern Y. What is cognitive reserve? Theory and research application of the reserve concept. J. Int. Neuropsychol. Soc. 2002, 8(3):448-460.
Stern Y. Cognitive reserve and Alzheimer disease. Alzheimer Dis. Assoc. Disord. 2006, 20(3 Suppl. 2):S69-S74.
Stern Y. Cognitive reserve. Neuropsychologia 2009, 47(10):2015-2028.
Stern Y., Habeck C., Moeller J., Scarmeas N., Anderson K.E., Hilton H.J., Flynn J., Sackeim H., van Heertum R. Brain networks associated with cognitive reserve in healthy young and old adults. Cereb. Cortex 2005, 15(4):394-402.
Stern Y., Zarahn E., Habeck C., Holtzer R., Rakitin B.C., Kumar A., Flynn J., Steffener J., Brown T. A common neural network for cognitive reserve in verbal and object working memory in young but not old. Cereb. Cortex 2008, 18(4):959-967.
Tucker A.M., Stern Y. Cognitive reserve in aging. Curr. Alzheimer Res. 2011, 8(4):354-360.
Vanhaudenhuyse A., Demertzi A., Schabus M., Noirhomme Q., Brédart S., Boly M., Phillips C., Soddu A., Luxen A., Moonen G., Laureys S. Two distinct neuronal networks mediate the awareness of environment and of self. J. Cogn. Neurosci. 2011, 23(3):570-578.
Vitouch O., Bauer H., Gittler G., Leodolter M., Leodolter U. Cortical activity of good and poor spatial test performers during spatial verbal processing studied with slow potential topography. Int. J. Psychophysiol. 1997, 27:183-199.
Vogt F., Klimesch W., Doppermayr M. High-frequency components in the alpha band and memory performance. J. Clin. Neurophysiol. 1998, 15:167-172.
Wu J.-T., Wu H.Z., Yan C.-G., Chen W.-X., Zhang H.-Y., He Y., Yang H.-S. Aging-related changes in the default mode network and its anti-correlated networks: a resting-state fMRI study. Neurosci. Lett. 2011, 504:62-67.