Neurobiology of Aging
Volume 30, Issue 11 , Pages 1737-1748 , November 2009

Cerebral perfusion and oxygenation differences in Alzheimer's disease risk

  • Adam S. Fleisher

      Affiliations

    • University of California at San Diego, Department of Neuroscience, United States
    • Corresponding Author InformationCorresponding author at: University of California at San Diego, 9500 Gilman Drive, La Jolla, CA 92037-0949, United Sates. Tel.: +1 858 622 5868; fax: +1 858 452 3058.
  • ,
  • Katherine M. Podraza

      Affiliations

    • University of California at San Diego, Department of Neuroscience, United States
  • ,
  • Katherine J. Bangen

      Affiliations

    • University of California at San Diego, Department of Neuroscience, United States
  • ,
  • Curtis Taylor

      Affiliations

    • University of California at San Diego, Department of Neuroscience, United States
  • ,
  • Ayesha Sherzai

      Affiliations

    • University of California at San Diego, Department of Neuroscience, United States
  • ,
  • Kunal Sidhar

      Affiliations

    • University of California at San Diego, New York Medical College, United States
  • ,
  • Thomas T. Liu

      Affiliations

    • University of California at San Diego, Department of Radiology, United States
  • ,
  • Anders M. Dale

      Affiliations

    • University of California at San Diego, Department of Neuroscience, United States
    • University of California at San Diego, Department of Radiology, United States
  • ,
  • Richard B. Buxton

      Affiliations

    • University of California at San Diego, Department of Radiology, United States

Received 19 October 2007 ,Revised 8 December 2007 ,Accepted 18 January 2008.

References 

  1. Alsop DC, Detre JA, Grossman M. Assessment of cerebral blood flow in Alzheimer's disease by spin-labeled magnetic resonance imaging. Ann. Neurol. 2000;47(1):93–100
  2. Bassett SS, Yousem DM, Cristinzio C, Kusevic I, Yassa MA, Caffo BS, et al. Familial risk for Alzheimer's disease alters fMRI activation patterns brain activation in offspring of AD cases corresponds to 10q linkage. Brain. 2006;129(Pt 5):1229–1239
  3. Bateman GA, Levi CR, Schofield P, Wang Y, Lovett EC. Quantitative measurement of cerebral haemodynamics in early vascular dementia and Alzheimer's disease. J. Clin. Neurosci. 2006;13(5):563–568Epub March 15, 2006
  4. Benarroch E. Neurovascular unit dysfunction: a vascular component of Alzheimer disease?. Neurology. 2007;68(20):1730–1732
  5. Bondi MW, Houston WS, Eyler LT, Brown GG. Differential BOLD brain response to verbal paired-associate learning by APOE genotype in nondemented older adults: a functional MRI study. Neurobiol. Aging. 2004;25(S2):506
  6. Bondi MW, Houston WS, Eyler LT, Brown GG. FMRI evidence of compensatory mechanisms in older adults at genetic risk for Alzheimer's disease. Neurology. 2005;64:501–508
  7. 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
  8. Brown GG, Eyler Zorrilla LT, Georgy B, Kindermann SS, Wong EC, Buxton RB. BOLD and perfusion response to finger-thumb apposition after acetazolamide administration: differential relationship to global perfusion. J. Cereb. Blood Flow Metab. 2003;23(7):829–837
  9. Buxton RB, Uludag K, Dubowitz DJ, Liu TT. Modeling the hemodynamic response to brain activation. Neuroimage. 2004;23(Suppl. 1):S220–S233
  10. Celone KA, Calhoun VD, Dickerson BC, Atri A, Chua EF, Miller SL, et al. Alterations in memory networks in mild cognitive impairment and Alzheimer's disease: an independent component analysis. J. Neurosci. 2006;26(40):10222–10231
  11. Chalela JA, Alsop DC, Gonzalez-Atavales JB, Maldjian JA, Kasner SE, Detre JA. Magnetic resonance perfusion imaging in acute ischemic stroke using continuous arterial spin labeling. Stroke. 2000;31(3):680–687
  12. Corder EH, Ghebremedhin E, Taylor MG, Thal DR, Ohm TG, Braak H. The biphasic relationship between regional brain senile plaque and neurofibrillary tangle distributions: modification by age, sex, and APOE polymorphism. Ann. NY Acad. Sci. 2004;1019:24–28
  13. Corder EH, Lannfelt L, Bogdanovic N, Fratiglioni L, Mori H. The role of APOE polymorphisms in late-onset dementias. Cell Mol. Life Sci. 1998;54(9):928–934
  14. Cox RW. AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput. Biomed. Res. 1996;29(3):162–173
  15. Cupples LA, Farrer LA, Sadovnick AD, Relkin N, Whitehouse P, Green RC. Estimating risk curves for first-degree relatives of patients with Alzheimer's disease: the REVEAL study. Genet. Med. 2004;6(4):192–196
  16. Davis TL, Kwong KK, Weisskoff RM, Rosen BR. Calibrated functional MRI: mapping the dynamics of oxidative metabolism. Proc. Natl. Acad. Sci. U.S.A. 1998;95(4):1834–1839
  17. Delis DC, Freeland J, Kramer JH, Kaplan E. Integrating clinical assessment with cognitive neuroscience: construct validation of the California Verbal Learning Test. J. Consult. Clin. Psychol. 1988;56(1):123–130
  18. Dickerson BC, Salat DH, Greve DN, Chua EF, Rand-Giovannetti E, Rentz DM, et al. Increased hippocampal activation in mild cognitive impairment compared to normal aging and AD. Neurology. 2005;65(3):404–411
  19. Farkas E, Luiten PG. Cerebral microvascular pathology in aging and Alzheimer's disease. Prog. Neurobiol. 2001;64(6):575–611
  20. 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(3):341–355
  21. Fleisher AS, Houston WS, Eyler LT, Frye S, Jenkins C, Thal LJ, et al. Identification of Alzheimer disease risk by functional magnetic resonance imaging. Arch. Neurol. 2005;62(12):1881–1888
  22. Folin M, Baiguera S, Guidolin D, Di Liddo R, Grandi C, De Carlo E, et al. Apolipoprotein-E modulates the cytotoxic effect of beta-amyloid on rat brain endothelium in an isoform-dependent specific manner. Int. J. Mol. Med. 2006;17(5):821–826
  23. Folstein MF, Folstein SE, McHugh PR. Mini-mental state. A practical method for grading the cognitive state of patients for the clinician. J. Psychiatr. Res. 1975;12(3):189–198
  24. Fratiglioni L, Ahlbom A, Viitanen M, Winblad B. Risk factors for late-onset Alzheimer's disease: a population-based, case-control study. Ann. Neurol. 1993;33(3):258–266
  25. Ghebremedhin E, Schultz C, Braak E, Braak H. High frequency of apolipoprotein E epsilon4 allele in young individuals with very mild Alzheimer's disease-related neurofibrillary changes. Exp. Neurol. 1998;153(1):152–155
  26. Girouard H, Iadecola C. Neurovascular coupling in the normal brain and in hypertension, stroke, and Alzheimer disease. J. Appl. Physiol. 2006;100(1):328–335
  27. Glover GH, Li TQ, Ress D. Image-based method for retrospective correction of physiological motion effects in fMRI: RETROICOR. Magn. Reson. Med. 2000;44(1):162–167
  28. 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. 2006;
  29. Hardy J, Selkoe DJ. The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science. 2002;297(5580):353–356
  30. Hoge RD, Atkinson J, Gill B, Crelier GR, Marrett S, Pike GB. Investigation of BOLD signal dependence on cerebral blood flow and oxygen consumption: the deoxyhemoglobin dilution model. Magn. Reson. Med. 1999;42(5):849–863
  31. Iadecola C. Neurovascular regulation in the normal brain and in Alzheimer's disease. Nat. Rev. Neurosci. 2004;5(5):347–360
  32. Iannetti GD, Wise RG. BOLD functional MRI in disease and pharmacological studies: room for improvement?. Magn. Reson. Imaging. 2007;25(6):978–988
  33. Ishii K, Sasaki M, Matsui M, Sakamoto S, Yamaji S, Hayashi N, et al. A diagnostic method for suspected Alzheimer's disease using H(2)15O positron emission tomography perfusion Z score. Neuroradiology. 2000;42(11):787–794
  34. Ishiwata A, Sakayori O, Minoshima S, Mizumura S, Kitamura S, Katayama Y. Preclinical evidence of Alzheimer changes in progressive mild cognitive impairment: a qualitative and quantitative SPECT study. Acta. Neurol. Scand. 2006;114(2):91–96
  35. Jinhu Xiong J-HGJLLPTF. Clustered pixels analysis for functional MRI activation studies of the human brain. Hum. Brain Mapp. 1995;3(4):287–301
  36. Johnson KA, Jones K, Holman BL, Becker JA, Spiers PA, Satlin A, et al. Preclinical prediction of Alzheimer's disease using SPECT. Neurology. 1998;50(6):1563–1571
  37. Johnson NA, Jahng GH, Weiner MW, Miller BL, Chui HC, Jagust WJ, et al. Pattern of cerebral hypoperfusion in Alzheimer disease and mild cognitive impairment measured with arterial spin-labeling MR imaging: initial experience. Radiology. 2005;234(3):851–859
  38. Johnson SC, Schmitz TW, Trivedi MA, Ries ML, Torgerson BM, Carlsson CM, et al. The influence of Alzheimer disease family history and apolipoprotein E epsilon4 on mesial temporal lobe activation. J. Neurosci. 2006;26(22):6069–6076
  39. Kaplan EF, Goodglass H, Weintraub S. Boston Naming Test. Philadelphia, PA: Lea & Febiger; 1983;
  40. Liu TT, Wong EC. A signal processing model for arterial spin labeling functional MRI. Neuroimage. 2005;24(1):207–215
  41. Lojkowska W, Ryglewicz D, Jedrzejczak T, Sienkiewicz-Jarosz H, Minc S, Jakubowska T, et al. SPECT as a diagnostic test in the investigation of dementia. J. Neurol. Sci. 2002;203–204:215–219
  42. Luh WM, Wong EC, Bandettini PA, Ward BD, Hyde JS. Comparison of simultaneously measured perfusion and BOLD signal increases during brain activation with T(1)-based tissue identification. Magn. Reson. Med. 2000;44(1):137–143
  43. Marco S, Skaper SD. Amyloid beta-peptide1-42 alters tight junction protein distribution and expression in brain microvessel endothelial cells. Neurosci. Lett. 2006;401(3):219–224
  44. Mohs RC, Knopman D, Petersen RC, Ferris SH, Ernesto C, Grundman M, et al. Development of cognitive instruments for use in clinical trials of antidementia drugs: additions to the Alzheimer's Disease Assessment Scale (ADAS) that broaden its scope. The Alzheimer's Disease Cooperative Study. Alzheimer Dis. Assoc. Dis. 1997;11(Suppl. 2):13S–21S
  45. Monsch AU, Bondi MW, Butters N, Salmon DP, Katzman R, Thal LJ. Comparisons of verbal fluency tasks in the detection of dementia of the Alzheimer type. Arch. Neurol. 1992;49(12):1253–1258
  46. Obata T, Liu TT, Miller KL, Luh WM, Wong EC, Frank LR, et al. Discrepancies between BOLD and flow dynamics in primary and supplementary motor areas: application of the balloon model to the interpretation of BOLD transients. Neuroimage. 2004;21(1):144–153
  47. Reiman EM, Caselli RJ, Chen K, Alexander GE, Bandy D, Frost J. Declining brain activity in cognitively normal apolipoprotein E varepsilon 4 heterozygotes: a foundation for using positron emission tomography to efficiently test treatments to prevent Alzheimer's disease. Proc. Natl. Acad. Sci. U.S.A. 2001;98(6):3334–3339
  48. 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
  49. 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):284–289Epub December 19, 2003
  50. Reitan RM. Validity of the trail making test as an indicator of organic brain damage. Percept. Mot. Skills. 1958;8:271–276
  51. Restom K, Bangen KJ, Bondi MW, Perthen JE, Liu TT. Cerebral blood flow and BOLD responses to a memory encoding task: a comparison between healthy young and elderly adults. Neuroimage. 2007;37(2):430–439Epub May 25, 2007
  52. Restom K, Behzadi Y, Liu TT. Physiological noise reduction for arterial spin labeling functional MRI. Neuroimage. 2006;31(3):1104–1115Epub March 13, 2006
  53. 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(8):1467–1472
  54. 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(10):1440–1444
  55. Smith A. Symbol Digit Modalities Test Manual—Revised. Los Angeles: Western Psychological Services; 1982;
  56. Smith CD, Andersen AH, Kryscio RJ, Schmitt FA, Kindy MS, Blonder LX, et al. Altered brain activation in cognitively intact individuals at high risk for Alzheimer's disease. Neurology. 1999;53(7):1391–1396
  57. Smith CD, Andersen AH, Kryscio RJ, Schmitt FA, Kindy MS, Blonder LX, et al. Women at risk for AD show increased parietal activation during a fluency task. Neurology. 2002;58(8):1197–1202
  58. Sperling RA, 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(2):1400–1410
  59. Sperling RA, Dickerson B, Bates JF, Chua EF, Cocchiarella AJ, Rentz DM, et al. fMRI studies of associative encoding in young and elderly controls and mild Alzheimer's disease. J. Neurol. Neurosurg. Psychiatry. 2003;74(1):44–50
  60. Sperling RA, Bates JF, Cocchiarella AJ, Schacter DL, Rosen BR, Albert MS. Encoding novel face-name associations: a functional MRI study. Hum. Brain Mapp. 2001;14(3):129–139
  61. Stefanovic B, Warnking JM, Rylander KM, Pike GB. The effect of global cerebral vasodilation on focal activation hemodynamics. Neuroimage. 2006;30(3):726–734Epub December 5, 2005
  62. 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 Med. 2006;4:1
  63. Uludag K, Dubowitz DJ, Yoder EJ, Restom K, Liu TT, Buxton RB. Coupling of cerebral blood flow and oxygen consumption during physiological activation and deactivation measured with fMRI. Neuroimage. 2004;23(1):148–155
  64. Varma AR, Adams W, Lloyd JJ, Carson KJ, Snowden JS, Testa HJ, et al. Diagnostic patterns of regional atrophy on MRI and regional cerebral blood flow change on SPECT in young onset patients with Alzheimer's disease, frontotemporal dementia and vascular dementia. Acta Neurol. Scand. 2002;105(4):261–269
  65. Wechsler D. Manual for the Wechsler Adult Intelligence Scale (rev. ed.). New York: The Pscyhological Corporation, Harcourt Brace Janvanovich Inc.; 1981;
  66. Wechsler D. WMS-R Wechsler Memory Scale—Revised Manual. New York: The Psychological Corporation, Harcourt Brace Jovanovich Inc.; 1987;
  67. 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(9):1603–1610
  68. Wong EC, Buxton RB, Frank LR. Quantitative imaging of perfusion using a single subtraction (QUIPSS and QUIPSS II). Magn. Reson. Med. 1998;39(5):702–708
  69. Xu G, Antuono PG, Jones J, Xu Y, Wu G, Ward D, et al. Perfusion fMRI detects deficits in regional CBF during memory-encoding tasks in MCI subjects. Neurology. 2007;69(17):1650–1656
  70. Yesavage JA, Brink TL, Rose TL, Lum O, Huang V, Adey M, et al. Development and validation of a geriatric depression screening scale: a preliminary report. J. Psychiatr. Res. 1982;17(1):37–49
  71. Zlokovic BV. Neurovascular mechanisms of Alzheimer's neurodegeneration. Trends Neurosci. 2005;28(4):202–208
  72. Zlokovic BV, Deane R, Sallstrom J, Chow N, Miano JM. Neurovascular pathways and Alzheimer amyloid beta-peptide. Brain Pathol. 2005;15(1):78–83

PII: S0197-4580(08)00028-6

doi: 10.1016/j.neurobiolaging.2008.01.012

Neurobiology of Aging
Volume 30, Issue 11 , Pages 1737-1748 , November 2009