Neurobiology of Aging
Volume 29, Issue 3 , Pages 329-340 , March 2008

Accelerated age-related cortical thinning in healthy carriers of apolipoprotein E ɛ4

  • Thomas Espeseth

      Affiliations

    • Department of Psychology, University of Oslo, P.O. Box 1094, Blindern, N-0317 Oslo, Norway
    • Corresponding Author InformationCorresponding author. Tel.: +47 22845135; fax: +47 22845096.
  • ,
  • Lars T. Westlye

      Affiliations

    • Department of Psychology, University of Oslo, P.O. Box 1094, Blindern, N-0317 Oslo, Norway
  • ,
  • Anders M. Fjell

      Affiliations

    • Department of Psychology, University of Oslo, P.O. Box 1094, Blindern, N-0317 Oslo, Norway
  • ,
  • Kristine B. Walhovd

      Affiliations

    • Department of Psychology, University of Oslo, P.O. Box 1094, Blindern, N-0317 Oslo, Norway
  • ,
  • Helge Rootwelt

      Affiliations

    • Department of Medical Biochemistry, Rikshospitalet-Radiumhospitalet Medical Center, Oslo, Norway
  • ,
  • Ivar Reinvang

      Affiliations

    • Department of Psychology, University of Oslo, P.O. Box 1094, Blindern, N-0317 Oslo, Norway

Received 19 May 2006 ,Revised 24 October 2006 ,Accepted 30 October 2006.

References 

  1. Bartzokis G, Cummings JL, Sultzer D, Henderson VW, Nuechterlein KH, Mintz J. White matter structural integrity in healthy aging adults and patients with Alzheimer disease: a magnetic resonance imaging study. Arch. Neurol. 2003;60(3):393–398
  2. Bondi MW, Houston WS, Eyler LT, Brown GG. fMRI evidence of compensatory mechanisms in older adults at genetic risk for Alzheimer disease. Neurology. 2005;64(3):501–508
  3. Bookheimer SY, Strojwas MH, Cohen MS, Saunders AM, Pericak-Vance MA, Mazziotta JC, et al. Patterns of brain activation in people at risk for Alzheimer's disease. N. Engl. J. Med. 2000;343(7):450–456
  4. Braak H, Braak E. Diagnostic criteria for neuropathologic assessment of Alzheimer's disease. Neurobiol. Aging. 1997;18:S85–S88
  5. Bretsky P, Guralnik JM, Launer L, Albert M, Seeman TE. The role of APOE-epsilon4 in longitudinal cognitive decline: MacArthur studies of successful aging. Neurology. 2003;60(7):1077–1081
  6. Buckner RL, Head D, Parker J, Fotenos AF, Marcus D, Morris JC, et al. A unified approach for morphometric and functional data analysis in young, old, and demented adults using automated atlas-based head size normalization: reliability and validation against manual measurement of total intracranial volume. NeuroImage. 2004;23:724–738
  7. Cohen RM, Small C, Lalonde F, Friz J, Sunderland T. Effect of apolipoprotein E genotype on hippocampal volume loss in aging healthy women. Neurology. 2001;57:2223–2228
  8. Corder EH, Saunders AM, Strittmatter WJ, Schmechel DE, Gaskell PC, Small GW, et al. Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer's disease in late onset families. Science. 1993;261:921–923
  9. Dale AM, Sereno MI. Improved localization of cortical activity by combining EEG and MEG with MRI cortical surface reconstruction: a linear approach. J. Cogn. Neurosci. 1993;5:162–176
  10. Dale AM, Fischl B, Sereno MI. Cortical surface-based analysis I: segmentation and surface reconstruction. NeuroImage. 1999;9:179–194
  11. Delis DC, Kramer JH, Kaplan E, Ober BA. California Verbal Learning Test. second ed.. San Antonio, TX: The Psychological Corporation; 2000;
  12. Den Heijer T, Oudkerk M, Launer LJ, van Duijn CM, Hofman A, Breteler MM. Hippocampal, amygdalar, and global brain atrophy in different apolipoprotein E genotypes. Neurology. 2002;59:746–748
  13. Dobbs AR, Rule BG. Adult age differences in working memory. Psychol. Aging. 1989;4(4):500–503
  14. Espeseth T, Greenwood PM, Reinvang I, Fjell AM, Walhovd KB, Westlye LT, et al. Interactive effects of APOE and CHRNA4 on attention and white matter volume in healthy middle-aged and older adults. Cogn. Affect. Behav. Neurosci. 2006;6:31–43
  15. Farrer LA, Cupples LA, Haines JL, Hyman B, Kukull WA, Mayeux R, et al. Effects of age, sex, and ethnicity on the association between apolipoprotein E genotype and Alzheimer disease. A meta-analysis. APOE and Alzheimer Disease Meta Analysis Consortium. JAMA. 1997;278:1349–1356
  16. Fazekas F, Strasser-Fuchs S, Kollegger H, Berger T, Kristoferitsch W, Schmidt H, et al. Apolipoprotein E epsilon 4 is associated with rapid progression of multiple sclerosis. Neurology. 2001;57:853–857
  17. Fischl B, Dale AM. Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proc. Natl. Acad. Sci. U.S.A. 2000;97:11050–11055
  18. Fischl B, Sereno MI, Dale AM. Cortical surface-based analysis: II. Inflation, flattening, and a surface-based coordinate system. NeuroImage. 1999;9:195–207
  19. Fischl B, Salat DH, Busa E, Albert M, Dieterich M, Haselgrove C, et al. Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron. 2002;33:341–355
  20. Fjell AM, Walhovd KB, Reinvang I, Lundervold A, Salat D, Quinn BT, et al. Selective increase of cortical thickness in high-performing elderly--structural indices of optimal cognitive aging. NeuroImage. 2006;29(3):984–994
  21. Flory JD, Manuck SB, Ferrell RE, Ryan CM, Muldoon MF. Memory performance and the apolipoprotein E polymorphism in a community sample of middle-aged adults. Am. J. Med. Genet. 2000;96(6):707–711
  22. Gerdes LU, Jeune B, Ranberg KA, Nybo H, Vaupel JW. Estimation of apolipoprotein E genotype-specific relative mortality risks from the distribution of genotypes in centenarians and middle-aged men: apolipoprotein E gene is a “frailty gene,” not a “longevity gene”. Genet. Epidemiol. 2000;19(3):202–210
  23. Greenwood P, Parasuraman R. Normal genetic variation, cognition, and aging. Behav. Cogn. Neurosci. Rev. 2003;2:278–306
  24. Greenwood PM, Lambert C, Sunderland T, Parasuraman R. Effects of apolipoprotein E genotype on spatial attention, working memory, and their interaction in healthy, middle-aged adults: results From the National Institute of Mental Health's BIOCARD study. Neuropsychology. 2005;19(2):199–211
  25. Greenwood PM, Sunderland T, Friz J, Parasuraman R. Genetics and visual attention: Selective deficits in healthy adult carriers of the E4 allele of the apolipoprotein E gene. Proc. Natl. Acad. Sci. U.S.A. 2000;97:11661–11666
  26. Greenwood PM, Sunderland T, Putnam K, Levy J, Parasuraman R. Scaling of visuospatial attention undergoes differential longitudinal change as a function of APOE genotype prior to old age: results from the NIMH BIOCARD study. Neuropsychology. 2005;19(6):830–840
  27. Huang Y, Weisgraber KH, Mucke L, Mahley RW. Apolipoprotein E: diversity of cellular origins, structural and biophysical properties, and effects in Alzheimer's disease. J. Mol. Neurosci. 2004;23:189–204
  28. Ji Z-S, Müllendorff K, Cheng IH, Miranda RD, Huang Y, Mahley RW. Reactivity of apolipoprotein E4 and amyloid beta peptide: lysosomal stability and neurodegeneration. J. Biol. Chem. 2006;281:2683–2692
  29. Kuperberg GR, Broome MR, McGuire PK, David AS, Eddy M, Ozawa F, et al. Regionally localized thinning of the cerebral cortex in schizophrenia. Arch. Gen. Psychiatry. 2003;60:878–888
  30. Lemaître H, Crivello F, Dufouil C, Grassiot B, Tzourio C, Alperovitch A, et al. No epsilon4 gene dose effect on hippocampal atrophy in a large MRI database of healthy elderly subjects. NeuroImage. 2005;24(4):1205–1213
  31. Lerch JP, Pruessner JC, Zijdenbos A, Hampel H, Teipel SJ, Evans AC. Focal decline of cortical thickness in Alzheimer's disease identified by computational neuroanatomy. Cereb. Cortex. 2005;15(7):995–1001
  32. Lind J, Persson J, Ingvar M, Larsson A, Cruts M, Van Broeckhoven C, et al. Reduced functional brain activity response in cognitively intact apolipoprotein E epsilon4 carriers. Brain. 2006;129:1240–1248
  33. Lippa CF, Smith TW, Saunders AM, Hulette C, Pulaski-Salo D, Roses AD. Apolipoprotein E-epsilon 2 and Alzheimer's disease: genotype influences pathologic phenotype. Neurology. 1997;48(2):515–519
  34. Luo L, O’Leary DD. Axon retraction and degeneration in development and disease. Annu. Rev. Neurosci. 2005;28:127–156
  35. Mahley RW, Weisgraber KH, Huang Y. Apolipoprotein E4: a causative factor and therapeutic target in neuropathology, including Alzheimer's disease. Proc. Natl. Acad. Sci. U.S.A. 2006;103:5644–5651
  36. Mauch DH, Nägler K, Schumacher S, Göritz C, Müller E-C, Otto A, et al. CNS synaptogenesis promoted by glia-derived cholesterol. Science. 2001;294:1354–1357
  37. Moffat SD, Szekely CA, Zonderman AB, Kabani NJ, Resnick SM. Longitudinal change in hippocampal volume as a function of apolipoprotein E genotype. Neurology. 2000;55:134–136
  38. Pfefferbaum A, Sullivan EV, Carmelli D. Genetic regulation of regional microstructure of the corpus callosum in late life. Neuroreport. 2001;12(8):1677–1681
  39. Pfefferbaum A, Sullivan EV, Swan GE, Carmelli D. Brain structure in men remains highly heritable in the seventh and eighth decades of life. Neurobiol. Aging. 2000;21:63–74
  40. Plassman BL, Welsh-Bohmer KA, Bigler ED, Johnson SC, Anderson CV, Helms MJ, et al. Apolipoprotein E epsilon 4 allele and hippocampal volume in twins with normal cognition. Neurology. 1997;48:985–989
  41. Raz N. The aging brain observed in vivo: differential changes and their modifiers. In:  Cabeza R,  Nyberg L,  Park DC editor. The Cognitive Neuroscience of Aging. New York: Oxford University Press; 2005;p. 19–58
  42. Raz N, Lindenberger U, Rodriue KM, Kennedy KM, Head D, Williamson A, et al. Regional brain changes in aging healthy adults: general trends, individual differences and modifiers. Cereb. Cortex. 2005;15(11):1676–1689
  43. Reiman EM, Caselli RJ, Yun LS, Chen K, Bandy D, Minoshima S, et al. Preclinical evidence of Alzheimer's disease in persons homozygous for the epsilon 4 allele for apolipoprotein E. N. Engl. J. Med. 1996;334(12):752–758
  44. Reiman EM, Chen K, Alexander GE, Caselli RJ, Bandy D, Osborne D, et al. Functional brain abnormalities in young adults at genetic risk for late-onset Alzheimer's dementia. Proc. Natl. Acad. Sci. U.S.A. 2004;101(1):284–289
  45. Reiman EM, Uecker A, Caselli RJ, Lewis S, Bandy D, de Leon MJ, et al. Hippocampal volumes in cognitively normal persons at genetic risk for Alzheimer's disease. Ann. Neurol. 1998;44(2):288–291
  46. Resnick SM, Pham DL, Kraut MA, Zonderman AB, Davatzikos C. Longitudinal magnetic resonance imaging studies of older adults: a shrinking brain. J. Neurosci. 2003;23(8):3295–3301
  47. Rosas HD, Liu AK, Hersch S, Glessner M, Ferrante RJ, Salat DH, et al. Regional and progressive thinning of the cortical ribbon in Huntington's disease. Neurology. 2002;58:695–701
  48. Rosen VM, Bergeson JL, Putnam K, Harwell A, Sunderland T. Working memory and apolipoprotein E: what's the connection?. Neuropsychologia. 2002;40(13):2226–2233
  49. Salat DH, Buckner RL, Snyder AZ, Greve DN, Desikan RSR, Busa E, et al. Thinning of the cerebral cortex in aging. Cereb. Cortex. 2004;14:721–730
  50. Salthouse TA. The processing-speed theory of adult age differences in cognition. Psychol. Rev. 1996;103(3):403–428
  51. Scoville WB, Milner B. Loss of recent memory after bilateral hippocampal lesions. J. Neurol. Neurosurg. Psychiatry. 1957;20:1–21
  52. Small BJ, Rosnick CB, Fratiglioni L, Bäckman L. Apolipoprotein E and cognitive performance: a meta-analysis. Psychol. Aging. 2004;19:592–600
  53. Soininen H, Partanen K, Pitkanen A, Hallikainen M, Hanninen T, Helisalmi S, et al. Decreased hippocampal volume asymmetry on MRIs in nondemented elderly subjects carrying the apolipoprotein E epsilon 4 allele. Neurology. 1995;45(2):391–392
  54. Spreen O, Strauss E. A Compendium of Neuropsychological Tests: Adminstration, Norms and Commentary. second ed.. New York: Oxford University Press; 1998;
  55. Sullivan EV, Pfefferbaum A, Swan GE, Carmelli D. Heritability of hippocampal size in elderly twin men: equivalent influence from genes and environment. Hippocampus. 2001;11(6):754–762
  56. Sundstrom A, Marklund P, Nilsson LG, Cruts M, Adolfsson R, Van Broeckhoven C, et al. Neurology. 2004;62(11):1963–1966
  57. Teter B, Xu PT, Gilbert JR, Roses AD, Galasko D, Cole GM. Defective neuronal sprouting by human apolipoprotein E4 is a gain-of-negative function. J. Neurosci. Res. 2002;68:331–336
  58. Toga AW, Thompson PM. Genetics of brain structure and intelligence. Annu. Rev. Neurosci. 2005;28:1–23
  59. Wechsler D. Wechsler Abbreviated Scale of Intelligence. San Antonio, TX: The Psychological Corporation; 1999;
  60. Wilson RS, Schneider JA, Barnes LL, Beckett LA, Aggarwal NT, Cochran EJ, et al. The apolipoprotein E epsilon 4 allele and decline in different cognitive systems during a 6-year period. Arch. Neurol. 2002;59:1154–1160
  61. Ye S, Huang Y, Mullendorff K, Dong L, Giedt G, Meng EC, et al. Apolipoprotein (apo) E4 enhances amyloid beta peptide production in cultured neuronal cells: apoE structure as a potential therapeutic target. Proc. Natl. Acad. Sci. U.S.A. 2005;102:18700–18705

PII: S0197-4580(06)00403-9

doi: 10.1016/j.neurobiolaging.2006.10.030

Neurobiology of Aging
Volume 29, Issue 3 , Pages 329-340 , March 2008