Neurobiology of Aging
Volume 30, Issue 7 , Pages 1114-1124 , July 2009

Brain structure and function related to cognitive reserve variables in normal aging, mild cognitive impairment and Alzheimer's disease

  • Cristina Solé-Padullés

      Affiliations

    • Departament de Psiquiatria i Psicobiologia Clínica, Universitat de Barcelona, Barcelona, Spain
    • ,
  • David Bartrés-Faz

      Affiliations

    • Departament de Psiquiatria i Psicobiologia Clínica, Universitat de Barcelona, Barcelona, Spain
    • Institut d’Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Barcelona, Spain
    • Corresponding Author InformationCorresponding author at: Departament de Psiquiatria i Psicobiologia Clínica, Facultat de Medicina, Universitat de Barcelona, Casanova 143, 08036 Barcelona, Spain. Tel.: +34 93 4037264; fax: +34 93 4035294.
    • ,
  • Carme Junqué

      Affiliations

    • Departament de Psiquiatria i Psicobiologia Clínica, Universitat de Barcelona, Barcelona, Spain
    • Institut d’Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Barcelona, Spain
    • ,
  • Pere Vendrell

      Affiliations

    • Departament de Psiquiatria i Psicobiologia Clínica, Universitat de Barcelona, Barcelona, Spain
    • Institut d’Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Barcelona, Spain
    • ,
  • Lorena Rami

      Affiliations

    • Alzheimer's Disease and Other Cognitive Disorders Unit, Neurology Service, Hospital Clinic de Barcelona, Barcelona, Spain
    • Institut d’Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Barcelona, Spain
    • ,
  • Imma C. Clemente

      Affiliations

    • Departament de Psiquiatria i Psicobiologia Clínica, Universitat de Barcelona, Barcelona, Spain
    • ,
  • Beatriu Bosch

      Affiliations

    • Alzheimer's Disease and Other Cognitive Disorders Unit, Neurology Service, Hospital Clinic de Barcelona, Barcelona, Spain
    • Institut d’Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Barcelona, Spain
    • ,
  • Amparo Villar

      Affiliations

    • Alzheimer's Disease and Other Cognitive Disorders Unit, Neurology Service, Hospital Clinic de Barcelona, Barcelona, Spain
    • Institut d’Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Barcelona, Spain
    • ,
  • Núria Bargalló

      Affiliations

    • Radiology Service, Hospital Clinic de Barcelona, Spain
    • Institut d’Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Barcelona, Spain
    • ,
  • M. Angeles Jurado

      Affiliations

    • Departament de Psiquiatria i Psicobiologia Clínica, Universitat de Barcelona, Barcelona, Spain
    • ,
  • Maite Barrios

      Affiliations

    • Departament de Metodologia de les Ciències del Comportament, Universitat de Barcelona, Barcelona, Spain
    • ,
  • Jose Luis Molinuevo

      Affiliations

    • Alzheimer's Disease and Other Cognitive Disorders Unit, Neurology Service, Hospital Clinic de Barcelona, Barcelona, Spain
    • Institut d’Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Barcelona, Spain

Received 29 June 2007 ,Revised 7 October 2007 ,Accepted 13 October 2007.

References 

  1. Alexander GE, Furey ML, Grady CL, Pietrini P, Brady DR, Mentis MJ, et al. Association of premorbid intellectual function with cerebral metabolism in Alzheimer's disease: implications for the cognitive reserve hypothesis. Am. J. Psychiatry. 1997;154:165–172
  2. Bartres-Faz D, Marti MJ, Junque C, Sole-Padulles C, Ezquerra M, Bralten LB, et al. Increased cerebral activity in Parkinson's disease patients carrying the DRD2 TaqIA A1 allele during a demanding motor task: a compensatory mechanism?. Genes Brain. Behav. 2006;6:588–592
  3. Berg L, McKeel DW, Miller P, Storandt M, Rubin EH, Morris JC, et al. Clinicopathologic studies in cognitively healthy aging and Alzheimer disease. Arch. Neurol. 1998;55:326–335
  4. Cader S, Cifelli A, Abu-Omar Y, Palace J, Matthews PM. Reduced brain functional reserve and altered functional connectivity in patients with multiple sclerosis. Brain. 2006;129:527–537
  5. Chang L, Yakupov R, Cloak C, Ernst T. Marijuana use is associated with a reorganized visual-attention network and cerebellar hypoactivation. Brain. 2006;129:1096–1112
  6. Coffey CE, Saxton JA, Ratcliff G, Bryan RN, Lucke JF. Relation of education to brain size in normal aging: implications for the reserve hypothesis. Neurology. 1999;53:189–196
  7. Colom R, Jung RE, Haier RJ. Distributed brain sites for the g-factor intelligence. Neuroimage. 2006;31:1359–1365
  8. Dickerson BC, Salat DH, Bates JF, Atiya M, Killiany RJ, Greve DN, et al. Medial temporal lobe function and structure in mild cognitive impairment. Ann. Neurol. 2004;56:27–35
  9. Edland SD, Xu Y, Plevak M, O’Brien P, Tangalos EG, Petersen RC, et al. Total intracranial volume: normative values and lack of association with Alzheimer's disease. Neurology. 2002;59:272–274
  10. Ernst T, Chang L, Jovicich J, Ames N, Arnold S. Abnormal brain activation on functional MRI in cognitively asymptomatic HIV patients. Neurology. 2002;59:1343–1349
  11. Gaser C, Schlaug G. Brain structures differ between musicians and non-musicians. J. Neurosci. 2003;23:9240–9245
  12. Golby A, Silverberg G, Race E, Gabrieli S, O'Shea J, Knierim K, et al. Memory encoding in Alzheimer's disease: an fMRI study of explicit and implicit memory. Brain. 2005;128:773–787
  13. Gould RL, Brown RG, Owen AM, Ffytche DH, Howard RJ. fMRi BOLD response to increasing task difficulty during successful paired associates learning. Neuropsychologia. 2003;20:1006–1019
  14. Grady CL. Cognitive reserve in healthy aging and Alzheimer disease: evidence for compensatory reorganization of brain networks. In:  Stern Y editors. Cognitive Reserve. Theory and Applications. New York: Taylor & Francis; 2007;p. 265–283
  15. Habeck C, Hilton HJ, Zarahn E, Flynn J, Moeller J, Stern Y. Relation of cognitive reserve and task performance to expression of regional covariance networks in an event-related fMRI study of nonverbal memory. Neuroimage. 2003;20:1723–1733
  16. Haier RJ, Jung RE, Yeo RA, Head K, Alkire MT. Structural brain variation and general intelligence. Neuroimage. 2004;23:425–433
  17. Haroutunian V, Davies P, Vianna D, Buxbaum JD, Purohit DP. Tau protein abnormalities associated with the progression of Alzheimer disease type dementia. Neurobiol. Aging. 2007;28:1–7
  18. Jenkins R, Fox NC, Rossor AM, Harvey RJ, Rossor MN. Intracranial volume and Alzheimer's disease. Evidence against the cerebral reserve hypothesis. Arch. Neurol. 2000;57:220–224
  19. Jung RE, Haier RJ. The parieto-frontal integration theory (P-FIT) of intelligence: converging neuroimaging evidence. Behav. Brain. Sci. 2007;23:135–154
  20. Katzman R, Terry R, DeTeresa R, Brown T, Davies P, Fuld P, et al. Clinical, pathological, and neurochemical changes in dementia: a subgroup with preserved mental status and numerous neocortical plaques. Ann. Neurol. 1988;23:138–144
  21. Kidron D, Black SE, Stanchev P, Buck B, Szalai JP, Parker J, et al. Quantitative MR volumetry in Alzheimer's disease. Topographic markers and the effects of sex and education. Neurology. 1997;49:1504–1512
  22. Lezak D, Howieson DB, Loring DW, Hannay HJ, Fischer JS. Neuropsychological Assessment. New York: Oxford University Press; 2004;pp. 91–97
  23. Logothetis NK, Pauls J, Augath M, Trinath T, Oeltermann A. Neurophysiological investigation of the basis of the fMRI signal. Nature. 2001;12:150–157
  24. Lopez O, Jagust WJ, Dekosky ST, Becker JT, Fitzpatrick A, Dulberg C, et al. Prevalence and classification of mild cognitive impairment in the cardiovascular health study cognition. Arch. Neurol. 2003;60:1385–1389
  25. Markesbery WR, Shcmitt FA, Kryscio RJ, Davis DG, Smith CD, Wekstein DR. Neuropathologic substrate of mild cognitive impairment. Arch. Neurol. 2006;63:38–46
  26. Morris JC, Storandt M, Miller JP, McKeel DW, Price JL, Rubin EH, et al. Mild cognitive impairment represents early-stage Alzheimer disease. Arch. Neurol. 2001;58:397–405
  27. Mortimer JA, Snowdon DA, Markesbery WR. Head circumference, education and risk of dementia: findings from the nun study. J. Clin. Exp. Neuropsychol. 2003;25:671–679
  28. Pena-Casanova J, Guardia J, Bertran-Serra I, Manero RM, Jarne A. Shortened version of the Barcelona test (I): subtests and normal profiles. Neurologia. 1997;12:99–111
  29. Perneczky R, Drzezga A, Diehl-Schmid J, Schmid G, Wohlschlager A, Kars S, et al. Schooling mediates brain reserve in Alzheimer's disease: findings of fluoro-deoxy-glucose-positron emission tomography. J. Neurol. Neurosurg. Psychiatry. 2006;77:1060–1063
  30. Petersen RC, Doody R, Kurz A, Mohs RC, Morris JC, Rabins PV, et al. Current concepts in mild cognitive impairment. Arch. Neurol. 2001;58:1985–1992
  31. Rami L, Gomez-Anson B, Sanchez-Valle R, Bosch B, Monte GC, Llado A, et al. Longitudinal study of amnesic patients at high risk for Alzheimer's disease: clinical, neuropsychological and magnetic resonance spectroscopy features. Dement. Geriatr. Cogn. Disord. 2007;24:274–279
  32. Satz P. Brain reserve capacity on symptom onset after brain injury: a formulation and review of evidence for threshold theory. Neuropsychology. 1993;7:273–295
  33. Scarmeas N. Lifestyle patterns and cognitive reserve. In:  Stern Y editors. Cognitive Reserve. Theory and Applications. New York: Taylor & Francis; 2007;p. 187–206
  34. Scarmeas N, Zarahn E, Anderson KE, Habeck CGT, Hilton J, Flynn J, et al. Association of life activities with cerebral blood flow in Alzheimer disease. Arch. Neurol. 2003;60:359–365
  35. Scarmeas N, Zarahn E, Anderson KE, Hilton J, Flynn J, Van Heertum RL, et al. Cognitive reserve modulates functional brain responses during memory tasks: a PET study in healthy young and elderly subjects. Neuroimage. 2003;19:1215–1227
  36. Scarmeas N, Zarahn E, Anderson KE, Honing LS, Park A, Hilton J, et al. Cognitive reserve-mediated modulation of positron emission tomographic activations during memory tasks in Alzheimer disease. Arch. Neurol. 2004;61:73–78
  37. Scarmeas N, Albert SM, Manly JJ, Stern Y. Education and rates of cognitive decline in incident Alzheimer's disease. J. Neurol. Neurosurg. Psychiatry. 2006;77:308–316
  38. Schofield PW, Mosesson RE, Stern Y, Mayeux R. The age at onset of Alzheimer's disease and intracranial area measurement: a relationship. Arch. Neurol. 1995;52:95–98
  39. 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;49:30–37
  40. Serra-Grabulosa JM, Salgado-Pineda P, Junqué C, Solé-Padullés C, Moral P, López-Alomar A, et al. Apolipoproteins E and C1 and brain morphology in memory impaired elders. Neurogenetics. 2003;4:141–146
  41. Snowdon D. Healthy aging and dementia: findings from the Nun Study. Ann. Intern. Med. 2003;139:450–454
  42. Shmuel A, Augath M, Oeltermann A, Logothetis N. Negative functional MRI response correlates with decreases in neuronal activity in monkey visual area V1. Nat. Neurosci. 2006;9:569–577
  43. Springer MV, McIntosh AR, Wincour G, Grady CL. The relation between brain activity during memory tasks and years of education in young and older adults. Neuropsychology. 2005;19:181–192
  44. Staff R, Murray AD, Deary IJ, Whalley LJ. What provides cerebral reserve. Brain. 2004;127:1191–1199
  45. Starr JM, Loeffler B, Abousleiman Y, Simonotto E, Marxhall I, Goddard N, et al. Episodic and semantic memory tasks activate different brain regions in Alzheimer disease. Neurology. 2005;65:266–269
  46. Stern Y. What is cognitive reserve? Theory and research application of the reserve concept. J. Int. Neuropsychol. Soc. 2002;8:448–460
  47. Stern Y. Imaging cognitive reserve. In:  Stern Y editors. Cognitive Reserve. Theory and Applications. New York: Taylor & Francis; 2007;p. 251–263
  48. Stern CE, Corkin S, González RG, Guimaraes AR, Baker JR, Jennings PJ, et al. The ippocampal formation participates in novel picture encoding: evidence from functional magnetic resonance imaging. Proc. Natl. Acad. Sci. U.S.A. 1996;93:8660–8665
  49. Stern Y, Albert S, Tang MX, Tsai WY. Rate of memory decline in AD is related to education and occupation: cognitive reserve?. Neurology. 1999;53:1942–1947
  50. Stern Y, Zarahn E, Hilton HJ, Flynn J, DeLaPaz R, Rakitin B. Exploring the neural basis of cognitive reserve. J. Clin. Exp. Neuropsychol. 2003;25:691–701
  51. Stern Y, Habeck C, Moeller J, Scarmeas N, Anderson KE, Hilton HJ, et al. Brain networks associated with cognitive reserve in healthy young and old adults. Cereb. Cortex. 2005;15:394–402
  52. Taki Y, Kinomura S, Sato K, Goto R, Okada K, Ono S, et al. Both global gray matter volume and regional gray matter volume negatively correlate with lifetime alcohol intake in non-alcohol-dependent Japanese men: a volumetric analysis and a voxel-based morphometry. Alcohol. Clin. Exp. Res. 2006;30:1045–1050
  53. Tisserand DJ, Bosma H, Van Boxtel PJ, Jolles J. Head size and cognitive ability in non-demented older adults are related. Neurology. 2001;56:969–971
  54. Valenzuela MJ, Sachdev P. Brain reserve and dementia: a systematic review. Psychol. Med. 2005;35:1–14
  55. Wilson RS, Bennett DA, Gilley DW, Beckett LA, Barnes LL, Evans DA. Premorbid reading activity and patterns of cognitive decline in Alzheimer disease. Arch. Neurol. 2000;57:1718–1723
  56. Wolf H, Julin P, Gertz HJ, Winblad B, Wahlund LO. Intracranial volume in mild cognitive impairment, Alzheimer's disease and vascular dementia: evidence for brain reserve?. Int. J. Geriatr. Psychiatry. 2004;19:995–1007
  57. Wright CI, Feczko E, Dickerson B, Williams D. Neuroanatomical correlates of personality in the elderly. Neuroimage. 2007;35:263–272

PII: S0197-4580(07)00408-3

doi: 10.1016/j.neurobiolaging.2007.10.008

Neurobiology of Aging
Volume 30, Issue 7 , Pages 1114-1124 , July 2009

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