Cortical hypermetabolism in MCI subjects: a compensatory mechanism?

European Journal of Nuclear Medicine and Molecular Imaging

Volumn 42, Issue 3, 2015, Pages 447-458

  Ashraf, A ^a   Fan, Z ^a   Brooks, D J ^a   Edison, P ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Amyloid negative; Amyloid positive; Compensatory hypermetabolism; MCI; Neuroplasticity

Indexed keywords

AMYLOID; CARBON 11; FLUORINE 18; PITTSBURGH COMPOUND B; BENZOTHIAZOLE DERIVATIVE; GLUCOSE BLOOD LEVEL; N-METHYL-2-(4'-METHYLAMINOPHENYL)-6-HYDROXYBENZOTHIAZOLE; RADIOPHARMACEUTICAL AGENT;

ADULT; AGED; ANTERIOR CINGULATE; ARTICLE; CINGULATE GYRUS; CLINICAL ARTICLE; CONTROLLED STUDY; DEVICE COMPARISON; DOWN REGULATION; FOLLOW UP; FRONTAL CORTEX; GLUCOSE METABOLISM; HUMAN; HYPERMETABOLISM; HYPOMETABOLISM; IN VIVO STUDY; INTERMETHOD COMPARISON; METABOLIC DISORDER; MILD COGNITIVE IMPAIRMENT; NUCLEAR MAGNETIC RESONANCE SCANNER; OCCIPITAL CORTEX; PARIETAL CORTEX; PET SCANNER; POSITRON EMISSION TOMOGRAPHY; POSTERIOR CINGULATE; TEMPORAL CORTEX; UPREGULATION; ALZHEIMER DISEASE; BRAIN CORTEX; FEMALE; GLUCOSE BLOOD LEVEL; MALE; METABOLISM; MIDDLE AGED; SCINTISCANNING;

AGED; ALZHEIMER DISEASE; BENZOTHIAZOLES; BLOOD GLUCOSE; CEREBRAL CORTEX; FEMALE; HUMANS; MALE; MIDDLE AGED; MILD COGNITIVE IMPAIRMENT; POSITRON-EMISSION TOMOGRAPHY; RADIOPHARMACEUTICALS;

EID: 84925512149     PISSN: 16197070     EISSN: 16197089     Source Type: Journal    
DOI: 10.1007/s00259-014-2919-z     Document Type: Article

References (62)

1. Kim J, Basak JM, Holtzman DM. The role of apolipoprotein E in Alzheimer’s disease. Neuron. 2009;63(3):287–303. doi:10.1016/j.neuron.2009.06.026.
2. Klunk WE, Engler H, Nordberg A, Wang Y, Blomqvist G, Holt DP, et al. Imaging brain amyloid in Alzheimer’s disease with Pittsburgh Compound-B. Ann Neurol. 2004;55(3):306–19. doi:10.1002/ana.20009.
3. Shin J, Lee SY, Kim SJ, Kim SH, Cho SJ, Kim YB. Voxel-based analysis of Alzheimer’s disease PET imaging using a triplet of radiotracers: PIB, FDDNP, and FDG. Neuroimage. 2010;52(2):488–96. doi:10.1016/j.neuroimage.2010.04.013.
4. Klunk WE, Wang Y, Huang GF, Debnath ML, Holt DP, Shao L, et al. The binding of 2-(4′-methylaminophenyl)benzothiazole to postmortem brain homogenates is dominated by the amyloid component. J Neurosci. 2003;23(6):2086–92.
5. Jack Jr CR, Lowe VJ, Weigand SD, Wiste HJ, Senjem ML, Knopman DS, et al. Serial PIB and MRI in normal, mild cognitive impairment and Alzheimer’s disease: implications for sequence of pathological events in Alzheimer’s disease. Brain J Neurol. 2009;132(Pt 5):1355–65. doi:10.1093/brain/awp062.
6. Forsberg A, Engler H, Almkvist O, Blomquist G, Hagman G, Wall A, et al. PET imaging of amyloid deposition in patients with mild cognitive impairment. Neurobiol Aging. 2008;29(10):1456–65. doi:10.1016/j.neurobiolaging.2007.03.029.
7. Okello A, Koivunen J, Edison P, Archer HA, Turkheimer FE, Nagren K, et al. Conversion of amyloid positive and negative MCI to AD over 3 years: an 11C-PIB PET study. Neurology. 2009;73(10):754–60. doi:10.1212/WNL.0b013e3181b23564.
8. Weiner MW, Veitch DP, Aisen PS, Beckett LA, Cairns NJ, Green RC, et al. The Alzheimer’s Disease Neuroimaging Initiative: a review of papers published since its inception. Alzheimers Dement. 2013;9(5):e111–94. doi:10.1016/j.jalz.2013.05.1769.
9. Villemagne VL, Pike KE, Chetelat G, Ellis KA, Mulligan RS, Bourgeat P, et al. Longitudinal assessment of Abeta and cognition in aging and Alzheimer disease. Ann Neurol. 2011;69(1):181–92. doi:10.1002/ana.22248.
10. Aizenstein HJ, Nebes RD, Saxton JA, Price JC, Mathis CA, Tsopelas ND, et al. Frequent amyloid deposition without significant cognitive impairment among the elderly. Arch Neurol. 2008;65(11):1509–17. doi:10.1001/archneur.65.11.1509.
11. Mintun MA, Larossa GN, Sheline YI, Dence CS, Lee SY, Mach RH, et al. [11C]PIB in a nondemented population: potential antecedent marker of Alzheimer disease. Neurology. 2006;67(3):446–52.
12. Chetelat G, Villemagne VL, Villain N, Jones G, Ellis KA, Ames D, et al. Accelerated cortical atrophy in cognitively normal elderly with high beta-amyloid deposition. Neurology. 2012;78(7):477–84. doi:10.1212/WNL.0b013e318246d67a.
13. Rodrigue KM, Kennedy KM, Devous Sr MD, Rieck JR, Hebrank AC, Diaz-Arrastia R, et al. beta-Amyloid burden in healthy aging: regional distribution and cognitive consequences. Neurology. 2012;78(6):387–95. doi:10.1212/WNL.0b013e318245d295.
14. Prohovnik I, Perl DP, Davis KL, Libow L, Lesser G, Haroutunian V. Dissociation of neuropathology from severity of dementia in late-onset Alzheimer disease. Neurology. 2006;66(1):49–55.
15. Terry RD, Masliah E, Salmon DP, Butters N, DeTeresa R, Hill R, et al. Physical basis of cognitive alterations in Alzheimer’s disease: synapse loss is the major correlate of cognitive impairment. Ann Neurol. 1991;30(4):572–80. doi:10.1002/ana.410300410.
16. Holmes C, Boche D, Wilkinson D, Yadegarfar G, Hopkins V, Bayer A, et al. Long-term effects of Abeta42 immunisation in Alzheimer’s disease: follow-up of a randomised, placebo-controlled phase I trial. Lancet. 2008;372(9634):216–23. doi:10.1016/S0140-6736(08)61075-2.
17. Benilova I, Karran E, De Strooper B. The toxic Abeta oligomer and Alzheimer’s disease: an emperor in need of clothes. Nat Neurosci. 2012;15(3):349–57. doi:10.1038/nn.3028.
18. Sokoloff L, Reivich M, Kennedy C, Des Rosiers MH, Patlak CS, Pettigrew KD, et al. The [14C]deoxyglucose method for the measurement of local cerebral glucose utilization: theory, procedure, and normal values in the conscious and anesthetized albino rat. J Neurochem. 1977;28(5):897–916.
19. Mosconi L, Mistur R, Switalski R, Tsui WH, Glodzik L, Li Y, et al. FDG-PET changes in brain glucose metabolism from normal cognition to pathologically verified Alzheimer’s disease. Eur J Nucl Med Mol Imaging. 2009;36(5):811–22. doi:10.1007/s00259-008-1039-z.
20. Nordberg A, Rinne JO, Kadir A, Langstrom B. The use of PET in Alzheimer disease. Nat Rev Neurol. 2010;6(2):78–87. doi:10.1038/nrneurol.2009.217.
21. Minoshima S, Giordani B, Berent S, Frey KA, Foster NL, Kuhl DE. Metabolic reduction in the posterior cingulate cortex in very early Alzheimer’s disease. Ann Neurol. 1997;42(1):85–94. doi:10.1002/ana.410420114.
22. Mosconi L, Tsui WH, De Santi S, Li J, Rusinek H, Convit A, et al. Reduced hippocampal metabolism in MCI and AD: automated FDG-PET image analysis. Neurology. 2005;64(11):1860–7.
23. Mosconi L, De Santi S, Li Y, Li J, Zhan J, Tsui WH, et al. Visual rating of medial temporal lobe metabolism in mild cognitive impairment and Alzheimer’s disease using FDG-PET. Eur J Nucl Med Mol Imaging. 2006;33(2):210–21.
24. Anchisi D, Borroni B, Franceschi M, Kerrouche N, Kalbe E, Beuthien-Beumann B, et al. Heterogeneity of brain glucose metabolism in mild cognitive impairment and clinical progression to Alzheimer disease. Arch Neurol. 2005;62(11):1728–33. doi:10.1001/archneur.62.11.1728.
25. Stern Y. Cognitive reserve and Alzheimer disease. Alzheimer Dis Assoc Disord. 2006;20(2):112–7. doi:10.1097/01.wad.0000213815.20177.19.
26. Sattler C, Toro P, Schonknecht P, Schroder 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. doi:10.1016/j.psychres.2011.11.012.
27. Okello A, Edison P, Archer HA, Turkheimer FE, Kennedy J, Bullock R, et al. Microglial activation and amyloid deposition in mild cognitive impairment: a PET study. Neurology. 2009;72(1):56–62. doi:10.1212/01.wnl.0000338622.27876.0d.
28. Edison P, Archer HA, Hinz R, Hammers A, Pavese N, Tai YF, et al. Amyloid, hypometabolism, and cognition in Alzheimer disease: an [11C]PIB and [18F]FDG PET study. Neurology. 2007;68(7):501–8. doi:10.1212/01.wnl.0000244749.20056.d4.
29. McKhann G, Drachman D, Folstein M, Katzman R, Price D, Stadlan EM. Clinical diagnosis of Alzheimer’s disease: report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer’s Disease. Neurology. 1984;34(7):939–44.
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(12):1985–92.
31. Ewers M, Insel P, Jagust WJ, Shaw L, Trojanowski JQ, Aisen P, et al. CSF biomarker and PIB-PET-derived beta-amyloid signature predicts metabolic, gray matter, and cognitive changes in nondemented subjects. Cereb Cortex. 2012;22(9):1993–2004. doi:10.1093/cercor/bhr271.
32. Jagust WJ, Landau SM, Shaw LM, Trojanowski JQ, Koeppe RA, Reiman EM, et al. Relationships between biomarkers in aging and dementia. Neurology. 2009;73(15):1193–9. doi:10.1212/Wnl.0b013e3181bc010c.
33. Busche MA, Chen X, Henning HA, Reichwald J, Staufenbiel M, Sakmann B, et al. Critical role of soluble amyloid-beta for early hippocampal hyperactivity in a mouse model of Alzheimer’s disease. Proc Natl Acad Sci U S A. 2012;109(22):8740–5. doi:10.1073/pnas.1206171109.
34. Balducci C, Beeg M, Stravalaci M, Bastone A, Sclip A, Biasini E, et al. Synthetic amyloid-beta oligomers impair long-term memory independently of cellular prion protein. Proc Natl Acad Sci U S A. 2010;107(5):2295–300. doi:10.1073/pnas.0911829107.
35. Lesne S, Kotilinek L, Ashe KH. Plaque-bearing mice with reduced levels of oligomeric amyloid-beta assemblies have intact memory function. Neuroscience. 2008;151(3):745–9. doi:10.1016/j.neuroscience.2007.10.054.
36. Cleary JP, Walsh DM, Hofmeister JJ, Shankar GM, Kuskowski MA, Selkoe DJ, et al. Natural oligomers of the amyloid-beta protein specifically disrupt cognitive function. Nat Neurosci. 2005;8(1):79–84. doi:10.1038/nn1372.
37. Jana A, Pahan K. Fibrillar amyloid-beta-activated human astroglia kill primary human neurons via neutral sphingomyelinase: implications for Alzheimer’s disease. J Neurosci. 2010;30(38):12676–89. doi:10.1523/JNEUROSCI.1243-10.2010.
38. Stern Y. Cognitive reserve in ageing and Alzheimer’s disease. Lancet Neurol. 2012;11(11):1006–12. doi:10.1016/S1474-4422(12)70191-6.
39. Jagust WJ, Mormino EC. Lifespan brain activity, beta-amyloid, and Alzheimer’s disease. Trends Cogn Sci. 2011;15(11):520–6. doi:10.1016/j.tics.2011.09.004.
40. Ossenkoppele R, Madison C, Oh H, Wirth M, van Berckel BN, Jagust WJ. Is verbal episodic memory in elderly with amyloid deposits preserved through altered neuronal function? Cereb Cortex. 2014;24(8):2210–8. doi:10.1093/cercor/bht076.
41. Morbelli S, Perneczky R, Drzezga A, Frisoni GB, Caroli A, van Berckel BN, et al. Metabolic networks underlying cognitive reserve in prodromal Alzheimer disease: a European Alzheimer disease consortium project. J Nucl Med. 2013;54(6):894–902. doi:10.2967/jnumed.112.113928.
42. Cohen AD, Price JC, Weissfeld LA, James J, Rosario BL, Bi W, et al. Basal cerebral metabolism may modulate the cognitive effects of Abeta in mild cognitive impairment: an example of brain reserve. J Neurosci. 2009;29(47):14770–8. doi:10.1523/JNEUROSCI.3669-09.2009.
43. Borghammer P, Cumming P, Aanerud J, Gjedde A. Artefactual subcortical hyperperfusion in PET studies normalized to global mean: lessons from Parkinson’s disease. Neuroimage. 2009;45(2):249–57. doi:10.1016/j.neuroimage.2008.07.042.
44. Borghammer P, Chakravarty M, Jonsdottir KY, Sato N, Matsuda H, Ito K, et al. Cortical hypometabolism and hypoperfusion in Parkinson’s disease is extensive: probably even at early disease stages. Brain Struct Funct. 2010;214(4):303–17. doi:10.1007/s00429-010-0246-0.
45. Jack Jr CR, Knopman DS, Jagust WJ, Petersen RC, Weiner MW, Aisen PS, et al. Tracking pathophysiological processes in Alzheimer’s disease: an updated hypothetical model of dynamic biomarkers. Lancet Neurol. 2013;12(2):207–16. doi:10.1016/S1474-4422(12)70291-0.
46. Knight EM, Verkhratsky A, Luckman SM, Allan SM, Lawrence CB. Hypermetabolism in a triple-transgenic mouse model of Alzheimer’s disease. Neurobiol Aging. 2012;33(1):187–93. doi:10.1016/j.neurobiolaging.2010.02.003.
47. Busche MA, Eichhoff G, Adelsberger H, Abramowski D, Wiederhold KH, Haass C, et al. Clusters of hyperactive neurons near amyloid plaques in a mouse model of Alzheimer’s disease. Science. 2008;321(5896):1686–9. doi:10.1126/science.1162844.
48. Calero MD, Navarro E. Relationship between plasticity, mild cognitive impairment and cognitive decline. Arch Clin Neuropsychol. 2004;19(5):653–60.
49. Mesulam MM. A plasticity-based theory of the pathogenesis of Alzheimer’s disease. Ann N Y Acad Sci. 2000;924:42–52.
50. Kantarci K, Senjem ML, Lowe VJ, Wiste HJ, Weigand SD, Kemp BJ, et al. Effects of age on the glucose metabolic changes in mild cognitive impairment. AJNR Am J Neuroradiol. 2010;31(7):1247–53. doi:10.3174/ajnr.A2070.
51. Iacono D, Resnick SM, O’Brien R, Zonderman AB, An Y, Pletnikova O, et al. Mild cognitive impairment and asymptomatic Alzheimer disease subjects: equivalent beta-amyloid and tau loads with divergent cognitive outcomes. J Neuropathol Exp Neurol. 2014;73(4):295–304. doi:10.1097/NEN.0000000000000052.
52. Bell KF, Bennett DA, Cuello AC. Paradoxical upregulation of glutamatergic presynaptic boutons during mild cognitive impairment. J Neurosci. 2007;27(40):10810–7. doi:10.1523/JNEUROSCI.3269-07.2007.
53. Riudavets MA, Iacono D, Resnick SM, O’Brien R, Zonderman AB, Martin LJ, et al. Resistance to Alzheimer’s pathology is associated with nuclear hypertrophy in neurons. Neurobiol Aging. 2007;28(10):1484–92. doi:10.1016/j.neurobiolaging.2007.05.005.
54. Sultana R, Butterfield DA. Regional expression of key cell cycle proteins in brain from subjects with amnestic mild cognitive impairment. Neurochem Res. 2007;32(4–5):655–62. doi:10.1007/s11064-006-9123-x.
55. Braak H, Braak E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol. 1991;82(4):239–59.
56. 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):404–11.
57. O’Brien JL, O’Keefe KM, LaViolette PS, DeLuca AN, Blacker D, Dickerson BC, et al. Longitudinal fMRI in elderly reveals loss of hippocampal activation with clinical decline. Neurology. 2010;74(24):1969–76. doi:10.1212/WNL.0b013e3181e3966e.
58. Andres P, Parmentier FB, Escera C. The effect of age on involuntary capture of attention by irrelevant sounds: a test of the frontal hypothesis of aging. Neuropsychologia. 2006;44(12):2564–8. doi:10.1016/j.neuropsychologia.2006.05.005.
59. Sperling RA, Laviolette PS, O’Keefe K, O’Brien J, Rentz DM, Pihlajamaki M, et al. Amyloid deposition is associated with impaired default network function in older persons without dementia. Neuron. 2009;63(2):178–88. doi:10.1016/j.neuron.2009.07.003.
60. Bakker A, Krauss GL, Albert MS, Speck CL, Jones LR, Stark CE, et al. Reduction of hippocampal hyperactivity improves cognition in amnestic mild cognitive impairment. Neuron. 2012;74(3):467–74. doi:10.1016/j.neuron.2012.03.023.
61. Risberg J, Passant U, Warkentin S, Gustafson L. Regional cerebral blood flow in frontal lobe dementia of non-Alzheimer type. Dementia. 1993;4(3-4):186–7.
62. Rohrer JD, Warren JD, Omar R, Mead S, Beck J, Revesz T, et al. Parietal lobe deficits in frontotemporal lobar degeneration caused by a mutation in the progranulin gene. Arch Neurol. 2008;65(4):506–13. doi:10.1001/archneur.65.4.506.