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Neural Correlates of Brain Reserve: A Neuroimaging Perspective

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Neurobiological and Psychological Aspects of Brain Recovery

Part of the book series: Contemporary Clinical Neuroscience ((CCNE))

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Abstract

Brain (BR) and cognitive reserve (CR) are known to modulate the clinical features of Alzheimer’s disease (AD). This is a critical issue especially in the absence of disease modifying treatments, but with non-pharmacological interventions available which might delay patients’ cognitive disabilities. We reported here a selection of studies investigating the neurobiological substrate of BR and CR in patients with AD at different clinical stages.

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References

  • Anatürk M, Kaufmann T, Cole JH, Suri S, Griffanti L, Zsoldos E, Filippini N, Singh-Manoux A, Kivimäki M, Westlye LT, Ebmeier KP, de Lange AG. Prediction of brain age and cognitive age: quantifying brain and cognitive maintenance in aging. Hum Brain Mapp. 2021;42(6):1626–40.

    PubMed  Google Scholar 

  • Anttila T, Helkala EL, Kivipelto M, Hallikainen M, Alhainen K, Heinonen H, Mannermaa A, Tuomilehto J, Soininen H, Nissinen A. Midlife income, occupation, APOE status, and dementia: a population-based study. Neurology. 2002;59(6):887–93.

    CAS  PubMed  Google Scholar 

  • Arenaza-Urquijo EM, Molinuevo JL, Sala-Llonch R, Solé-Padullés C, Balasa M, Bosch B, Olives J, Antonell A, Lladó A, Sánchez-Valle R, Rami L, Bartrés-Faz D. Cognitive reserve proxies relate to gray matter loss in cognitively healthy elderly with abnormal cerebrospinal fluid amyloid-β levels. J Alzheimers Dis. 2013;35(4):715–26.

    PubMed  Google Scholar 

  • Barulli D, Stern Y. Efficiency, capacity, compensation, maintenance, plasticity: emerging concepts in cognitive reserve. Trends Cogn Sci. 2013;17(10):502–9.

    PubMed  Google Scholar 

  • Belleville S, Mellah S, Cloutier S, Dang-Vu TT, Duchesne S, Maltezos S, Phillips N, Hudon C, CIMA-Q group. Neural correlates of resilience to the effects of hippocampal atrophy on memory. Neuroimage Clin. 2021;29:102526.

    PubMed  Google Scholar 

  • Bozzali M, Dowling C, Serra L, Spanò B, Torso M, Marra C, Castelli D, Dowell NG, Koch G, Caltagirone C, Cercignani M. The impact of cognitive reserve on brain functional connectivity in Alzheimer’s disease. J Alzheimers Dis. 2015;44:243–50.

    PubMed  Google Scholar 

  • Brickman AM, Siedlecki KL, Muraskin J, Manly JJ, Luchsinger JA, Yeung LK, Brown TR, DeCarli C, Stern Y. White matter hyperintensities and cognition: testing the reserve hypothesis. Neurobiol Aging. 2011;32(9):1588–98.

    PubMed  Google Scholar 

  • Coughlan G, Zhukovsky P, Voineskos A, Grady C. A profile of brain reserve in adults at genetic risk of Alzheimer’s disease. Alzheimers Dement (Amst). 2021;13(1):e12208.

    PubMed  Google Scholar 

  • Crowe M, Andel R, Pedersen NL, Johansson B, Gatz M. Does participation in leisure activities lead to reduced risk of Alzheimer’s disease? A prospective study of Swedish twins. J Gerontol B Psychol Sci Soc Sci. 2003;58(5):P249–55.

    PubMed  Google Scholar 

  • Dufouil C, Alpérovitch A, Tzourio C. Influence of education on the relationship between white matter lesions and cognition. Neurology. 2003;60(5):831–6.

    CAS  PubMed  Google Scholar 

  • Elkins JS, Longstreth WT Jr, Manolio TA, Newman AB, Bhadelia RA, Johnston SC. Education and the cognitive decline associated with MRI-defined brain infarct. Neurology. 2006;67(3):435–40.

    CAS  PubMed  Google Scholar 

  • Evans DA, Hebert LE, Beckett LA, Scherr PA, Albert MS, Chown MJ, Pilgrim DM, Taylor JO. Education and other measures of socioeconomic status and risk of incident Alzheimer disease in a defined population of older persons. Arch Neurol. 1997;54(11):1399–405.

    CAS  PubMed  Google Scholar 

  • Ewers M, Insel PS, Stern Y, Weiner MW. Alzheimer’s Disease Neuroimaging Initiative (ADNI). Cognitive reserve associated with FDG-PET in preclinical Alzheimer disease. Neurology. 2013;80(13):1194–201.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Facal D, Burgo C, Spuch C, Gaspar P, Campos-Magdaleno M. Cognitive frailty: an update. Front Psychol. 2021;12:813398.

    PubMed  PubMed Central  Google Scholar 

  • Farinpour R, Miller EN, Satz P, Selnes OA, Cohen BA, Becker JT, Skolasky RL Jr, Visscher BR. Psychosocial risk factors of HIV morbidity and mortality: findings from the Multicenter AIDS Cohort Study (MACS). J Clin Exp Neuropsychol. 2003;25(5):654–70.

    PubMed  Google Scholar 

  • Friedland RP. Epidemiology, education, and the ecology of Alzheimer’s disease. Neurology. 1993;43(2):246–9.

    CAS  PubMed  Google Scholar 

  • Friedland RP, Fritsch T, Smyth KA, Koss E, Lerner AJ, Chen CH, Petot GJ, Debanne SM. Patients with Alzheimer’s disease have reduced activities in midlife compared with healthy control-group members. Proc Natl Acad Sci U S A. 2001;98(6):3440–5.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gallo F, Kalpouzos G, Laukka EJ, Wang R, Qiu C, Bäckman L, Marseglia A, Fratiglioni L, Dekhtyar S. Cognitive trajectories and dementia risk: a comparison of two cognitive reserve measures. Front Aging Neurosci. 2021;13:737736.

    PubMed  PubMed Central  Google Scholar 

  • Garibotto V, Borroni B, Kalbe E, Herholz K, Salmon E, Holtoff V, Sorbi S, Cappa SF, Padovani A, Fazio F, Perani D. Education and occupation as proxies for reserve in aMCI converters and AD: FDG-PET evidence. Neurology. 2008;71(17):1342–9.

    CAS  PubMed  Google Scholar 

  • Garibotto V, Borroni B, Sorbi S, Cappa SF, Padovani A, Perani D. Education and occupation provide reserve in both ApoE ε4 carrier and noncarrier patients with probable Alzheimer’s disease. Neurol Sci. 2012;33(5):1037–42.

    CAS  PubMed  Google Scholar 

  • Garibotto V, Tettamanti M, Marcone A, Florea I, Panzacchi A, Moresco R, Virta JR, Rinne J, Cappa SF, Perani D. Cholinergic activity correlates with reserve proxies in Alzheimer’s disease. Neurobiol Aging. 2013;34(11):2694.

    Google Scholar 

  • Gilleard CJ. Edication and Alzheimer’s disease: a review of recent international epidemiological studies. Aging Ment Health. 1997;1(1):33–46.

    Google Scholar 

  • Glatt SL, Hubble JP, Lyons K, Paolo A, Tröster AI, Hassanein RE, Koller WC. Risk factors for dementia in Parkinson’s disease: effect of education. Neuroepidemiology. 1996;15(1):20–5.

    CAS  PubMed  Google Scholar 

  • Jack CR Jr, Knopman DS, Jagust WJ, Petersen RC, Weiner MW, Aisen PS, Shaw LM, Vemuri P, Wiste HJ, Weigand SD, Lesnick TG, Pankratz VS, Donohue MC, Trojanowski JQ. Tracking pathophysiological processes in Alzheimer’s disease: an updated hypothetical model of dynamic biomarkers. Lancet Neurol. 2013;12(2):207–16.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Katzman R. Education and the prevalence of dementia and Alzheimer’s disease. Neurology. 1993;43(1):13–20.

    CAS  PubMed  Google Scholar 

  • Katzman R, Terry R, DeTeresa R, Brown T, Davies P, Fuld P, Renbing X, Peck A. Clinical, pathological, and neurochemical changes in dementia: a subgroup with preserved mental status and numerous neocortical plaques. Ann Neurol. 1988;23(2):138–44.

    CAS  PubMed  Google Scholar 

  • Kesler SR, Adams HF, Blasey CM, Bigler ED. Premorbid intellectual functioning, education, and brain size in traumatic brain injury: an investigation of the cognitive reserve hypothesis. Appl Neuropsychol. 2003;10(3):153–62.

    PubMed  Google Scholar 

  • Li X, Zhou S, Zhu W, Li X, Gao Z, Li M, Luo S, Wu X, Tian Y, Yu Y. Sex difference in network topology and education correlated with sex difference in cognition during the disease process of Alzheimer. Front Aging Neurosci. 2021;13:639529.

    PubMed  PubMed Central  Google Scholar 

  • Lin Y, Zeng Q, Hu M, Peng G, Luo B, Alzheimer’s Disease Neuroimaging Initiative. Temporal dynamic changes of intrinsic brain activity associated with cognitive reserve in prodromal Alzheimer’s disease. J Alzheimers Dis. 2021;81(3):1285–94.

    PubMed  Google Scholar 

  • Marioni RE, van den Hout A, Valenzuela MJ, Brayne C, Matthews FE. MRC cognitive function and ageing study. Active cognitive lifestyle associates with cognitive recovery and a reduced risk of cognitive decline. J Alzheimers Dis. 2012;28(1):223–30.

    PubMed  Google Scholar 

  • Morbelli S, Perneczky R, Drzezga A, Frisoni GB, Caroli A, van Berckel BN, Ossenkoppele R, Guedj E, Didic M, Brugnolo A, Naseri M, Sambuceti G, Pagani M, Nobili F. Metabolic networks underlying cognitive reserve in prodromal Alzheimer disease: a European Alzheimer disease consortium project. J Nucl Med. 2013;54(6):894–902.

    CAS  PubMed  Google Scholar 

  • Mortimer JA, Borenstein AR, Gosche KM, Snowdon DA. Very early detection of Alzheimer neuropathology and the role of brain reserve in modifying its clinical expression. J Geriatr Psychiatry Neurol. 2005;18(4):218–23.

    PubMed  PubMed Central  Google Scholar 

  • Murray AD, Staff RT, McNeil CJ, Salarirad S, Ahearn TS, Mustafa N, Whalley LJ. The balance between cognitive reserve and brain imaging biomarkers of cerebrovascular and Alzheimer’s diseases. Brain. 2011;134(Pt 12):3687–96.

    PubMed  Google Scholar 

  • Nyberg L, Magnussen F, Lundquist A, Baaré W, Bartrés-Faz D, Bertram L, Boraxbekk CJ, Brandmaier AM, Drevon CA, Ebmeier K, Ghisletta P, Henson RN, Junqué C, Kievit R, Kleemeyer M, Knights E, Kühn S, Lindenberger U, Penninx BWJH, Pudas S, Sørensen Ø, Vaqué-Alcázar L, Walhovd KB, Fjell AM. Educational attainment does not influence brain aging. Proc Natl Acad Sci U S A. 2021;118(18):e2101644118.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Perry BL, Roth AR, Peng S, Risacher SL, Saykin AJ, Apostolova LG. Social networks and cognitive reserve: network structure moderates the association between amygdalar volume and cognitive outcomes. J Gerontol B Psychol Sci Soc Sci. 2021:gbab192.

    Google Scholar 

  • Qiu C, Karp A, von Strauss E, Winblad B, Fratiglioni L, Bellander T. Lifetime principal occupation and risk of Alzheimer’s disease in the Kungsholmen project. Am J Ind Med. 2003;43(2):204–11.

    PubMed  Google Scholar 

  • Querbes O, Aubry F, Pariente J, Lotterie JA, Démonet JF, Duret V, Puel M, Berry I, Fort JC, Celsis P. Alzheimer’s disease neuroimaging initiative. Early diagnosis of Alzheimer’s disease using cortical thickness: impact of cognitive reserve. Brain. 2009;132(Pt 8):2036–47.

    PubMed  PubMed Central  Google Scholar 

  • Rentz DM, Locascio JJ, Becker JA, Moran EK, Eng E, Buckner RL, Sperling RA, Johnson KA. Cognition, reserve, and amyloid deposition in normal aging. Ann Neurol. 2010;67(3):353–64.

    PubMed  Google Scholar 

  • Rydwik E, Welmer AK, Angleman S, Fratiglioni L, Wang HX. Is midlife occupational physical activity related to disability in old age? The SNAC-Kungsholmen study. PLoS One. 2013;8(7):e70471.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sadiq MU, Langella S, Giovanello KS, Mucha PJ, Dayan E. Accrual of functional redundancy along the lifespan and its effects on cognition. NeuroImage. 2021;229:117737.

    PubMed  Google Scholar 

  • Sato T, Hanyu H, Koyama Y, Horita H, Aoki T, Hirao K, Kanetaka H, Shimizu S. Discrepancy between the degree of cognitive impairment and brain imaging abnormalities in Alzheimer’s disease patients is associated with cognitive reserve. J Alzheimers Dis. 2021;84(1):273–81.

    CAS  PubMed  Google Scholar 

  • Sattler C, Toro P, Schönknecht P, Schröder J. Cognitive activity, education and socioeconomic status as preventive factors for mild cognitive impairment and Alzheimer’s disease. Psychiatry Res. 2012;196(1):90–5.

    PubMed  Google Scholar 

  • Schofield PW, Logroscino G, Andrews HF, Albert S, Stern Y. An association between head circumference and Alzheimer’s disease in a population-based study of aging and dementia. Neurology. 1997;49(1):30–7.

    CAS  PubMed  Google Scholar 

  • Serra L, Cercignani M, Petrosini L, Basile B, Perri R, Fadda L, Spanò B, Marra C, Giubilei F, Carlesimo GA, Caltagirone C, Bozzali M. Neuroanatomical correlates of cognitive reserve in Alzheimer disease. Rejuvenation Res. 2011;14(2):143–51.

    PubMed  Google Scholar 

  • Serra L, Musicco M, Cercignani M, Torso M, Spanò B, Mastropasqua C, Giulietti G, Marra C, Bruno G, Koch G, Caltagirone C, Bozzali M. Cognitive reserve and the risk for Alzheimer’s disease: a longitudinal study. Neurobiol Aging. 2015;36(2):592–600.

    PubMed  Google Scholar 

  • Serra L, Mancini M, Cercignani M, Di Domenico C, Spanò B, Giulietti G, Koch G, Marra C, Bozzali M. Network-based substrate of cognitive reserve in Alzheimer’s disease. J Alzheimers Dis. 2017;55(1):421–30.

    CAS  PubMed  Google Scholar 

  • Serra L, Petrosini L, Salaris A, Pica L, Bruschini M, Di Domenico C, Caltagirone C, Marra C, Bozzali M. Testing for the myth of cognitive reserve: are the static and dynamic cognitive reserve indexes a representation of different reserve warehouses? J Alzheimers Dis. 2019;72(1):111–26.

    PubMed  Google Scholar 

  • Smart EL, Gow AJ, Deary IJ. Occupational complexity and lifetime cognitive abilities. Neurology. 2014;83(24):2285–91.

    PubMed  PubMed Central  Google Scholar 

  • Soldan A, Pettigrew C, Li S, Wang MC, Moghekar A, Selnes OA, Albert M, O’Brien R, BIOCARD Research Team. Relationship of cognitive reserve and cerebrospinal fluid biomarkers to the emergence of clinical symptoms in preclinical Alzheimer’s disease. Neurobiol Aging. 2013;34(12):2827–34.

    CAS  PubMed  Google Scholar 

  • Steffener J. Education and age-related differences in cortical thickness and volume across the lifespan. Neurobiol Aging. 2021;102:102–10.

    PubMed  Google Scholar 

  • Stern Y. What is cognitive reserve? Theory and research application of the reserve concept. J Int Neuropsychol Soc. 2002;8(3):448–60.

    PubMed  Google Scholar 

  • Stern Y. Cognitive reserve. Neuropsychologia. 2009;47(10):2015–28.

    PubMed  PubMed Central  Google Scholar 

  • Stern Y. Cognitive reserve in ageing and Alzheimer’s disease. Lancet Neurol. 2012;11(11):1006–12.

    PubMed  PubMed Central  Google Scholar 

  • Stern Y, Alexander GE, Prohovnik I, Mayeux R. Inverse relationship between education and parietotemporal perfusion deficit in Alzheimer’s disease. Ann Neurol. 1992;32(3):371–5.

    CAS  PubMed  Google Scholar 

  • Stern Y, Gurland B, Tatemichi TK, Tang MX, Wilder D, Mayeux R. Influence of education and occupation on the incidence of Alzheimer’s disease. JAMA. 1994;271(13):1004–10.

    CAS  PubMed  Google Scholar 

  • Stern Y, Varangis E, Habeck C. A framework for identification of a resting-bold connectome associated with cognitive reserve. NeuroImage. 2021;232:117875.

    PubMed  Google Scholar 

  • Sumowski JF, Leavitt VM. Cognitive reserve in multiple sclerosis. Mult Scler. 2013;19(9):1122–7.

    PubMed  Google Scholar 

  • Valenzuela M, Brayne C, Sachdev P, Wilcock G, Matthews F. Medical research council cognitive function and ageing study. Cognitive lifestyle and long-term risk of dementia and survival after diagnosis in a multicenter population-based cohort. Am J Epidemiol. 2011;173(9):1004–12.

    PubMed  Google Scholar 

  • Vance DE, Crowe M. A proposed model of neuroplasticity and cognitive reserve in older adults. Act Adapt Aging. 2006;30(3):61–79.

    Google Scholar 

  • Vemuri P, Weigand SD, Przybelski SA, Knopman DS, Smith GE, Trojanowski JQ, Shaw LM, Decarli CS, Carmichael O, Bernstein MA, Aisen PS, Weiner M, Petersen RC, Jack CR Jr. Alzheimer’s disease neuroimaging initiative. Cognitive reserve and Alzheimer’s disease biomarkers are independent determinants of cognition. Brain. 2011;134(Pt 5):1479–92.

    PubMed  PubMed Central  Google Scholar 

  • Verghese J, Lipton RB, Katz MJ, Hall CB, Derby CA, Kuslansky G, Ambrose AF, Sliwinski M, Buschke H. Leisure activities and the risk of dementia in the elderly. N Engl J Med. 2003;348(25):2508–16.

    PubMed  Google Scholar 

  • Wilson RS, Bennett DA, Bienias JL, Aggarwal NT, Mendes De Leon CF, Morris MC, Schneider JA, Evans DA. Cognitive activity and incident AD in a population-based sample of older persons. Neurology. 2002;59(12):1910–4.

    CAS  PubMed  Google Scholar 

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Serra, L., Bozzali, M. (2023). Neural Correlates of Brain Reserve: A Neuroimaging Perspective. In: Petrosini, L. (eds) Neurobiological and Psychological Aspects of Brain Recovery. Contemporary Clinical Neuroscience. Springer, Cham. https://doi.org/10.1007/978-3-031-24930-3_6

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