Alzheimer's & Dementia: The Journal of the Alzheimer's Association
Volume 6, Issue 4 , Pages 303-311 , July 2010

Temporal lobe functional activity and connectivity in young adult APOE ɛ4 carriers

  • Nancy A. Dennis

      Affiliations

    • Center for Cognitive Neuroscience, Duke University, Durham, NC, USA
    • Department of Psychology, Pennsylvania State University, University Park, PA, USA
    • ,
  • Jeffrey N. Browndyke

      Affiliations

    • Joseph and Kathleen Bryan Alzheimer's Disease Research Center, Duke University, Durham, NC, USA
    • Division of Medical Psychology, Department of Psychiatry and Behavioral Sciences, Duke University Medical Center, Durham, NC, USA
    • Duke Institute for Brain Sciences, Duke University, Durham, NC, USA
    • Corresponding Author InformationCorresponding author. Tel.: 919-668-1586; Fax: 919-668-0828.
    • ,
  • Jared Stokes

      Affiliations

    • Center for Cognitive Neuroscience, Duke University, Durham, NC, USA
    • ,
  • Anna Need

      Affiliations

    • Institute for Genome Sciences and Policy, Duke University, Durham, NC, USA
    • ,
  • James R. Burke

      Affiliations

    • Joseph and Kathleen Bryan Alzheimer's Disease Research Center, Duke University, Durham, NC, USA
    • Division of Neurology, Department of Medicine, Duke University Medical Center, Durham, NC, USA
    • ,
  • Kathleen A. Welsh-Bohmer

      Affiliations

    • Joseph and Kathleen Bryan Alzheimer's Disease Research Center, Duke University, Durham, NC, USA
    • Division of Medical Psychology, Department of Psychiatry and Behavioral Sciences, Duke University Medical Center, Durham, NC, USA
    • Division of Neurology, Department of Medicine, Duke University Medical Center, Durham, NC, USA
    • ,
  • Roberto Cabeza

      Affiliations

    • Center for Cognitive Neuroscience, Duke University, Durham, NC, USA
    • Duke Institute for Brain Sciences, Duke University, Durham, NC, USA

References 

  1. Saunders AM, Strittmatter WJ, Schmechel D, George-Hyslop PH, Pericak-Vance MA, Joo SH, et al. Association of apolipoprotein E allele epsilon 4 with late-onset familial and sporadic Alzheimer's disease. Neurology. 1993;43:1467–1472
  2. Tervo S, Kivipelto M, Hanninen T, Vanhanen M, Hallikainen M, Mannermaa A, et al. Incidence and risk factors for mild cognitive impairment: a population-based three-year follow-up study of cognitively healthy elderly subjects. Dement Geriatr Cogn Disord. 2004;17:196–203
  3. Tschanz JT, Welsh-Bohmer KA, Lyketsos CG, Corcoran C, Green RC, Hayden K, et al. Conversion to dementia from mild cognitive disorder: the Cache County Study. Neurology. 2006;67:229–234
  4. Petersen RC, Waring SC, Smith GE, Tangalos EG, Thibodeau SN. Predictive value of APOE genotyping in incipient Alzheimer's disease. Ann N Y Acad Sci. 1996;802:58–69
  5. 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;343:450–456
  6. Bondi MW, Houston WS, Eyler LT, Brown GG. fMRI evidence of compensatory mechanisms in older adults at genetic risk for Alzheimer disease. Neurology. 2005;64:501–508
  7. Dickerson BC, Goncharova I, Sullivan MP, Forchetti C, Wilson RS, Bennett DA, et al. MRI-derived entorhinal and hippocampal atrophy in incipient and very mild Alzheimer's disease. Neurobiology of Aging. 2001;22:747–754
  8. Trivedi MA, Schmitz TW, Ries ML, Torgerson BM, Sager MA, Hermann BP, et al. Reduced hippocampal activation during episodic encoding in middle-aged individuals at genetic risk of Alzheimer's disease: a cross-sectional study. BMC medicine. 2006;4:1
  9. Kircher TT, Weis S, Freymann K, Erb M, Jessen F, Grodd W, et al. Hippocampal activation in patients with mild cognitive impairment is necessary for successful memory encoding. J Neurol Neurosurg Psychiatry. 2007;78:812–818
  10. Machulda MM, Ward HA, Borowski B, Gunter JL, Cha RH, O'Brien PC, et al. Comparison of memory fMRI response among normal, MCI, and Alzheimer's patients. Neurology. 2003;61:500–506
  11. Williams GC. Pleiotropy, natural selection, and the evolution of senescence. Evolution. 1957;11:398–411
  12. Han SD, Bondi MW. Revision of the apolipoprotein E compensatory mechanism recruitment hypothesis. Alzheimers Dement. 2008;4:251–254
  13. Han SD, Drake AI, Cessante LM, Jak AJ, Houston WS, Delis DC, et al. Apolipoprotein E and traumatic brain injury in a military population: evidence of a neuropsychological compensatory mechanism?. J Neurol Neurosurg Psychiatry. 2007;78:1103–1108
  14. Shaw P, Lerch JP, Pruessner JC, Taylor KN, Rose AB, Greenstein D, et al. Cortical morphology in children and adolescents with different apolipoprotein E gene polymorphisms: an observational study. Lancet Neurol. 2007;6:494–500
  15. Qiu S, Korwek KM, Weeber EJ. A fresh look at an ancient receptor family: emerging roles for low density lipoprotein receptors in synaptic plasticity and memory formation. Neurobiol Learn Mem. 2006;85:16–29
  16. Herz J, Chen Y. Reelin, lipoprotein receptors and synaptic plasticity. Nat Rev Neurosci. 2006;7:850–859
  17. Filbey FM, Slack KJ, Sunderland TP, Cohen RM. Functional magnetic resonance imaging and magnetoencephalography differences associated with APOEepsilon4 in young healthy adults. Neuroreport. 2006;17:1585–1590
  18. Scarmeas N, Habeck CG, Hilton J, Anderson KE, Flynn J, Park A, et al. APOE related alterations in cerebral activation even at college age. J Neurol Neurosurg Psychiatry. 2005;76:1440–1444
  19. Mondadori CR, de Quervain DJ, Buchmann A, Mustovic H, Wollmer MA, Schmidt CF, et al. Better memory and neural efficiency in young apolipoprotein E epsilon4 carriers. Cereb Cortex. 2007;17:1934–1947
  20. Filippini N, Macintosh BJ, Hough MG, Goodwin GM, Frisoni GB, Smith SM, et al. Distinct patterns of brain activity in young carriers of the APOE-{varepsilon}4 allele. Proc Natl Acad Sci U S A. 2009;106:7209–7214
  21. Paller KA, Wagner AD. Observing the transformation of experience into memory. Trends in Cognitive Sciences. 2002;6:93–102
  22. Braak H, Braak E, Bohl J. Staging of Alzheimer-related cortical destruction. Eur Neurol. 1993;33:403–408
  23. Braak H, Braak E. Evolution of neuronal changes in the course of Alzheimer's disease. J Neural Transm Suppl. 1998;53:127–140
  24. Jack CR, Petersen RC, Xu YC, Waring SC, O'Brien PC, Tangalos EG, et al. Medial temporal atrophy on MRI in normal aging and very mild Alzheimer's disease. Neurology. 1997;49:786–794
  25. Mori E, Yoneda Y, Yamashita H, Hirono N, Ikeda M, Yamadori A. Medial temporal structures relate to memory impairment in Alzheimer's disease: an MRI volumetric study. J Neurol Neurosurg Psychiatry. 1997;63:214–221
  26. Stout JC, Bondi MW, Jernigan TL, Archibald SL, Delis DC, Salmon DP. Regional cerebral volume loss associated with verbal learning and memory in dementia of the Alzheimer type. Neuropsychology. 1999;13:188–197
  27. Remy F, Mirrashed F, Campbell B, Richter W. Verbal episodic memory impairment in Alzheimer's disease: a combined structural and functional MRI study. Neuroimage. 2005;25:253–266
  28. Braak H, Braak E. Evolution of the neuropathology of Alzheimer's disease. Acta Neurol Scand Suppl. 1996;165:3–12
  29. Dobbins IG, Davachi L. Functional Neuroimaging of Episodic Memory. In:  Cabeza R,  Kingstone A editor. Handbook of Functional Neuroimaging of Cognition. Vol 2nd edition. Cambridge, MA: MIT Press; 2006;p. 229–268
  30. Koch W, Ehrenhaft A, Griesser K, Pfeufer A, Muller J, Schomig A, et al. TaqMan systems for genotyping of disease-related polymorphisms present in the gene encoding apolipoprotein E. Clin Chem Lab Med. 2002;40:1123–1131
  31. Snodgrass JG, Vanderwart M. A standardized set of 260 pictures: norms for name agreement, image agreement, familiarity, and visual complexity. J Exp Psychol [Hum Learn]. 1980;6:174–215
  32. Woodruff CC, Uncapher MR, Rugg MD. Neural correlates of differential retrieval orientation: Sustained and item-related components. Neuropsychologia. 2006;44:3000–3010
  33. Sperling R, Chua E, Cocchiarella A, Rand-Giovannetti E, Poldrack R, Schacter DL, et al. Putting names to faces: successful encoding of associative memories activates the anterior hippocampal formation. Neuroimage. 2003;20:1400–1410
  34. Dennis NA, Hayes SM, Prince SE, Huettel SA, Madden DJ, Cabeza R. Effects of aging on the neural correlates of successful item and source memory encoding. Journal of Experimental Psychology: Learning, Memory and Cognition. 2008;34:791–808
  35. Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, et al. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage. 2002;15:273–289
  36. Fisher RA. Statistical methods for Research Workers. London: Oliver and Boyd; 1950;
  37. Lazar NA, Luna B, Sweeney JA, Eddy WF. Combining brains: a survey of methods for statistical pooling of information. Neuroimage. 2002;16:538–550
  38. Forman SD, Cohen JD, Fitzgerald M, Eddy WF, Mintun MA, Noll DC. Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): use of a cluster-size threshold. Magnetic Resonance in Medicine. 1995;33:636–647
  39. Rissman J, Gazzaley A, D'Esposito M. Measuring functional connectivity during distinct stages of a cognitive task. Neuroimage. 2004;23:752–763
  40. Daselaar SM, Fleck MS, Dobbins IG, Madden DJ, Cabeza R. Effects of healthy aging on hippocampal and rhinal memory functions: an event-related fMRI study. Cerebral Cortex. 2006;16:1771–1782
  41. Good CD, Johnsrude IS, Ashburner J, Henson RN, Friston KJ, Frackowiak RS. A voxel-based morphometric study of ageing in 465 normal adult human brains. Neuroimage. 2001;14:21–36
  42. Ashburner J, Friston KJ. Voxel-based morphometry–the methods. Neuroimage. 2000;11:805–821
  43. Reiman EM, Chen K, Alexander GE, Caselli RJ, Bandy D, Osborne D, et al. Correlations between apolipoprotein E epsilon4 gene dose and brain-imaging measurements of regional hypometabolism. Proc Natl Acad Sci U S A. 2005;102:8299–8302
  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. PNAS. 2004;101:284–289
  45. Chen K, Reiman EM, Alexander GE, Caselli RJ, Gerkin R, Bandy D, et al. Correlations between apolipoprotein E epsilon4 gene dose and whole brain atrophy rates. Am J Psychiatry. 2007;164:916–921
  46. Wishart HA, Saykin AJ, Rabin LA, Santulli RB, Flashman LA, Guerin SJ, et al. Increased brain activation during working memory in cognitively intact adults with the APOE epsilon4 allele. Am J Psychiatry. 2006;163:1603–1610
  47. 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
  48. Han SD, Houston WS, Jak AJ, Eyler LT, Nagel BJ, Fleisher AS, et al. Verbal paired-associate learning by APOE genotype in non-demented older adults: fMRI evidence of a right hemispheric compensatory response. Neurobiol Aging. 2007;28:238–247
  49. Selkoe DJ. Alzheimer's Disease Is a Synaptic Failure. Science. 2002;298:789–791
  50. Morishima-Kawashima M, Oshima N, Ogata H, Yamaguchi H, Yoshimura M, Sugihara S, et al. Effect of apolipoprotein E allele epsilon4 on the initial phase of amyloid beta-protein accumulation in the human brain. Am J Pathol. 2000;157:2093–2099
  51. Petrella JR, Prince SE, Wang L, Hellegers C, Doraiswamy PM. Prognostic value of posteromedial cortex deactivation in mild cognitive impairment. PLoS ONE. 2007;2:e1104
  52. Lustig C, Snyder AZ, Bhakta M, O'Brien KC, McAvoy M, Raichle ME, et al. Functional deactivations: Change with age and dementia of the Alzheimer type. PNAS. 2003;100:14504–14509
  53. Prince SE, Woo S, Doraiswamy PM, Petrella JR. Functional MRI in the early diagnosis of Alzheimer's disease: is it time to refocus?. Expert review of neurotherapeutics. 2008;8:169–175

 N.A.D. and J.N.B. contributed equally to this work.

PII: S1552-5260(09)02093-7

doi: 10.1016/j.jalz.2009.07.003

Alzheimer's & Dementia: The Journal of the Alzheimer's Association
Volume 6, Issue 4 , Pages 303-311 , July 2010

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