Functional implications of hippocampal degeneration in early Alzheimer's disease: A combined DTI and PET study

European Journal of Nuclear Medicine and Molecular Imaging

Volumn 38, Issue 12, 2011, Pages 2219-2227

  Yakushev, Igor ^a   Schreckenberger, Matthias ^a   Müller, Matthias J ^a   Schermuly, Ingrid ^a   Cumming, Paul ^b   Stoeter, Peter ^a   Gerhard, Alex ^a,c   Fellgiebel, Andreas ^a  

^a UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

^b UNIVERSITY OF MUNICH   (Germany)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Dementia; Diffusion tensor imaging; Episodic memory; Mild cognitive impairment; Positron emission tomography; Posterior cingulate

Indexed keywords

FLUORODEOXYGLUCOSE F 18; GLUCOSE;

ALZHEIMER DISEASE; ARTICLE; BRAIN DEGENERATION; CLINICAL ARTICLE; DIFFUSION TENSOR IMAGING; EPISODIC MEMORY; GLUCOSE METABOLISM; HIPPOCAMPAL DEGENERATION; HUMAN; IMAGE ANALYSIS; IMAGE PROCESSING; MEMORY DISORDER; MINI MENTAL STATE EXAMINATION; NEUROLOGIC EXAMINATION; NEUROPSYCHOLOGICAL TEST; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; POSITRON EMISSION TOMOGRAPHY; VOXEL BASED MORPHOMETRY;

ALZHEIMER DISEASE; BRAIN; DIFFUSION MAGNETIC RESONANCE IMAGING; FEMALE; FLUORODEOXYGLUCOSE F18; FUNCTIONAL NEUROIMAGING; GLUCOSE; HIPPOCAMPUS; HUMANS; MALE; MEMORY DISORDERS; NEURAL PATHWAYS; POSITRON-EMISSION TOMOGRAPHY; RADIOPHARMACEUTICALS; SUBTRACTION TECHNIQUE;

EID: 84856208685     PISSN: 16197070     EISSN: 16197089     Source Type: Journal    
DOI: 10.1007/s00259-011-1882-1     Document Type: Article

References (59)

1. Braak H, Braak E. Neuropathological stageing of Alzheimerrelated changes. Acta Neuropathol 1991;82:239-59.
2. Gainotti G, Marra C, Villa G, Parlato V, Chiarotti F. Sensitivity and specificity of some neuropsychological markers of Alzheimer dementia. Alzheimer Dis Assoc Disord 1998;12:152-62. (Pubitemid 29154983)
3. de Leon MJ, Mosconi L, Blennow K, DeSanti S, Zinkowski R, Mehta PD, et al. Imaging and CSF studies in the preclinical diagnosis of Alzheimer's disease. Ann N Y Acad Sci 2007;1097:114-45. (Pubitemid 47084889)
4. 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;42:85-94. (Pubitemid 27304784)
5. Kogure D, Matsuda H, Ohnishi T, Asada T, Uno M, Kunihiro T, et al. Longitudinal evaluation of early Alzheimer's disease using brain perfusion SPECT. J Nucl Med 2000;41:1155-62. (Pubitemid 30463997)
6. Chételat G, Desgranges B, Landeau B, Mézenge F, Poline JB, de la Sayette V, et al. Direct voxel-based comparison between grey matter hypometabolism and atrophy in Alzheimer's disease. Brain 2008;131:60-71.
7. Meguro K, Blaizot X, Kondoh Y, Le Mestric C, Baron JC, Chavoix C. Neocortical and hippocampal glucose hypometabolism following neurotoxic lesions of the entorhinal and perirhinal cortices in the non-human primate as shown by PET. Implications for Alzheimer's disease. Brain 1999;122:1519-31. (Pubitemid 29374127)
8. Kobayashi Y, Amaral DG. Macaque monkey retrosplenial cortex: II. Cortical afferents. J Comp Neurol 2003;466:48-79. (Pubitemid 37193686)
9. Schmahmann JD, Pandya DN, Wang R, Dai G, D'Arceuil HE, de Crespigny AJ, et al. Association fibre pathways of the brain: parallel observations from diffusion spectrum imaging and autoradiography. Brain 2007;130:630-53. (Pubitemid 46410733)
10. Mori S, Wakana S, Van Zijl PCM, Nagae-Poetscher LM, editors. MRI atlas of human white matter. Oxford: Elsevier Ltd.; 2005.
11. Machado CJ, Snyder AZ, Cherry SR, Lavenex P, Amaral DG. Effects of neonatal amygdala or hippocampus lesions on resting brain metabolism in the macaque monkey: a microPET imaging study. Neuroimage 2008;39:832-46. (Pubitemid 350117642)
12. Villain N, Desgranges B, Viader F, de la Sayette V, Mézenge F, Landeau B, et al. Relationships between hippocampal atrophy, white matter disruption, and gray matter hypometabolism in Alzheimer's disease. J Neurosci 2008;28:6174-81.
13. Papez J. A proposed mechanism of emotion. Arch Neurol Psychiatry 1937;38:725-43.
14. Guedj E, Barbeau EJ, Didic M, Felician O, de Laforte C, Ranjeva JP, et al. Effects of medial temporal lobe degeneration on brain perfusion in amnestic MCI of AD type: deafferentation and functional compensation? Eur J Nucl Med Mol Imaging 2009;36:1101-12.
15. Petersen RC, Stevens JC, Ganguli M, Tangalos EG, Cummings JL, De Kosky ST. Practice parameter: early detection of dementia: mild cognitive impairment (an evidence-based review). Report of the Quality Standards Subcommittee of the American Academy of Neurology. Neurology 2001;56:1133-42.
16. Basser PJ, Pierpaoli C. Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. J Magn Reson B 1996;111:209-19. (Pubitemid 126758682)
17. Kantarci K, Petersen RC, Boeve BF, Knopman DS, Weigand SD, O'Brien PC. DWI predicts future progression to Alzheimer disease in amnestic mild cognitive impairment. Neurology 2005;64:902-4. (Pubitemid 40316336)
18. Müller MJ, Greverus D, Weibrich C, Dellani PR, Scheurich A, Stoeter P, et al. Diagnostic utility of hippocampal size and mean diffusivity in amnestic MCI. Neurobiol Aging 2007;28:398-403. (Pubitemid 46177388)
19. Zhang Y, Schuff N, Jahng GH, Bayne W, Mori S, Schad L, et al. Diffusion tensor imaging of cingulum fibers in mild cognitive impairment and Alzheimer disease. Neurology 2007;68:13-9. (Pubitemid 46058544)
20. Yakushev I, Müller MJ, Lorscheider M, Schermuly I, Weibrich C, Dellani PR, et al. Increased hippocampal head diffusivity predicts impaired episodic memory performance in early Alzheimer's disease. Neuropsychologia 2010;48:1447-53.
21. Yakushev I, Bartenstein P, Siessmeier T, Hiemke C, Scheurich A, Lotz J, et al. Cerebrospinal fluid tau protein levels and 18F-fluorodeoxyglucose positron emission tomography in the differential diagnosis of Alzheimer's disease. Dement Geriatr Cogn Disord 2010;30:245-53.
22. Dubois B, Feldman HH, Jacova C, Dekosky ST, Barberger-Gateau P, Cummings J, et al. Research criteria for the diagnosis of Alzheimer's disease: revising the NINCDS-ADRDA criteria. Lancet Neurol 2007;6:734-46. (Pubitemid 47058377)
23. Welsh KA, Butters N, Mohs RC, Beekly D, Edland S, Fillenbaum G, et al. The Consortium to Establish a Registry for Alzheimer's Disease (CERAD). Part V. A normative study of the neuropsychological battery. Neurology 1994;44:609-14. (Pubitemid 24129983)
24. Basser PJ, Mattiello J, Le Bihan D. Estimation of the effective selfdiffusion tensor from the NMR spin echo. J Magn Reson B 1994;103:247-54.
25. Yakushev I, Landvogt C, Buchholz HG, Fellgiebel A, Hammers A, Scheurich A, et al. Choice of reference area in studies of Alzheimer's disease using positron emission tomography with fluorodeoxyglucose-F18. Psychiatry Res 2008;164:143-53.
26. Yakushev I, Hammers A, Fellgiebel A, Schmidtmann I, Scheurich A, Buchholz HG, et al. SPM-based count normalization provides excellent discrimination of mild Alzheimer's disease and amnestic mild cognitive impairment from healthy aging. Neuroimage 2009;44:43-50.
27. Hammers A, Allom R, Koepp MJ, Free SL, Myers R, Lemieux L, et al. Three-dimensional maximum probability atlas of the human brain, with particular reference to the temporal lobe. Hum Brain Mapp 2003;19:224-47. (Pubitemid 36959351)
28. Gousias IS, Rueckert D, Heckemann RA, Dyet LE, Boardman JP, Edwards AD, et al. Automatic segmentation of brain MRIs of 2-yearolds into 83 regions of interest. Neuroimage 2008;40:672-84.
29. 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;68:501-8.
30. Kobayashi Y, Amaral DG. Macaque monkey retrosplenial cortex: III. Cortical efferents. J Comp Neurol 2007;502:810-33. (Pubitemid 46732498)
31. Concha L, Gross DW, Beaulieu C. Diffusion tensor tractography of the limbic system. AJNR Am J Neuroradiol 2005;26:2267-74.
32. Fellgiebel A, Müller MJ, Wille P, Dellani PR, Scheurich A, Schmidt LG, et al. Color-coded diffusion-tensor-imaging of posterior cingulate fiber tracts in mild cognitive impairment. Neurobiol Aging 2005;26:1193-8. (Pubitemid 40726012)
33. Teipel SJ, Born C, Ewers M, Bokde ALW, Reiser MF, Möller HJ, et al. Multivariate deformation-based analysis of brain atrophy to predict Alzheimer's disease in mild cognitive impairment. Neuroimage 2007;38:13-24. (Pubitemid 47429985)
34. Scheltens P, Barkhof F, Leys D, Wolters EC, Ravid R, Kamphorst W. Histopathologic correlates of white matter changes on MRI in Alzheimer's disease and normal aging. Neurology 1995;45:883-8.
35. Huang J, Friedland RP, Auchus AP. Diffusion tensor imaging of normal-appearing white matter in mild cognitive impairment and early Alzheimer disease: preliminary evidence of axonal degeneration in the temporal lobe. AJNR Am J Neuroradiol 2007;28:1943-8. (Pubitemid 350174740)
36. Choo IH, Lee DY, Oh JS, Lee JS, Lee DS, Song IC, et al. Posterior cingulate cortex atrophy and regional cingulum disruption in mild cognitive impairment and Alzheimer's disease. Neurobiol Aging 2010;31:772-9.
37. Salat DH, Tuch DS, van der Kouwe AJW, Greve DN, Pappu V, Lee SY, et al. White matter pathology isolates the hippocampal formation in Alzheimer's disease. Neurobiol Aging 2010;31:244-56.
38. Valenstein E, Bowers D, Verfaellie M, Heilman KM, Day A, Watson RT. Retrosplenial amnesia. Brain 1987;110:1631-46.
39. Maguire EA. The retrosplenial contribution to human navigation: a review of lesion and neuroimaging findings. Scand J Psychol 2001;42:225-38. (Pubitemid 33668475)
40. McDonald CR, Crosson B, Valenstein E, Bowers D. Verbal encoding deficits in a patient with a left retrosplenial lesion. Neurocase 2001;7:407-17. (Pubitemid 34056015)
41. Wagner AD, Shannon BJ, Kahn I, Buckner RL. Parietal lobe contributions to episodic memory retrieval. Trends Cogn Sci 2005;9:445-53. (Pubitemid 41208254)
42. Desgranges B, Baron JC, Lalevée C, Giffard B, Viader F, de La Sayette V, et al. The neural substrates of episodic memory impairment in Alzheimer's disease as revealed by FDG-PET: relationship to degree of deterioration. Brain 2002;125:1116-24. (Pubitemid 34464622)
43. Witter MP. The perforant path: projections from the entorhinal cortex to the dentate gyrus. Prog Brain Res 2007;163:43-61. (Pubitemid 47321428)
44. Yakushev I, Fellgiebel A. Horizontal versus longitudinal axis of the hippocampus: metabolic differentiation as measured with high-resolution PET/MRI. J Nucl Med 2011;52:329.
45. Hyman BT, Van Hoesen GW, Damasio AR, Barnes CL. Alzheimer's disease: cell-specific pathology isolates the hippocampal formation. Science 1984;225:1168-70. (Pubitemid 14029099)
46. Kirkby DL, Higgins GA. Characterization of perforant path lesions in rodent models of memory and attention. Eur J Neurosci 1998;10:823-38. (Pubitemid 28375608)
47. Rolls ET. An attractor network in the hippocampus: theory and neurophysiology. Learn Mem 2007;14:714-31. (Pubitemid 350172771)
48. Hyman BT, Van Hoesen GW, Kromer LJ, Damasio AR. Perforant pathway changes and the memory impairment of Alzheimer's disease. Ann Neurol 1986;20:472-81. (Pubitemid 16005665)
49. Shukla C, Bridges LR. Tau, beta-amyloid and beta-amyloid precursor protein distribution in the entorhinal-hippocampal alvear and perforant pathways in the Alzheimer's brain. Neurosci Lett 2001;303:193-7. (Pubitemid 32373288)
50. García-Sierra F, Hauw JJ, Duyckaerts C, Wischik CM, Luna-Muñoz J, Mena R. The extent of neurofibrillary pathology in perforant pathway neurons is the key determinant of dementia in the very old. Acta Neuropathol 2000;100:29-35. (Pubitemid 30352865)
51. Kalus P, Slotboom J, Gallinat J, Mahlberg R, Cattapan-Ludewig K, Wiest R, et al. Examining the gateway to the limbic system with diffusion tensor imaging: the perforant pathway in dementia. Neuroimage 2006;30:713-20.
52. Stoub TR, de Toledo-Morrell L, Stebbins GT, Leurgans S, Bennett DA, Shah RC. Hippocampal disconnection contributes to memory dysfunction in individuals at risk for Alzheimer's disease. Proc Natl Acad Sci U S A 2006;103:10041-5. (Pubitemid 43993619)
53. Deller T, Haas CA, Freiman TM, Phinney A, Jucker M, Frotscher M. Lesion-induced axonal sprouting in the central nervous system. Adv Exp Med Biol 2006;557:101-21.
54. 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;29:1456-65.
55. Mosconi L, Pupi A, De Leon MJ. Brain glucose hypometabolism and oxidative stress in preclinical Alzheimer's disease. Ann N Y Acad Sci 2008;1147:180-95.
56. Small GW, Kepe V, Ercoli LM, Siddarth P, Bookheimer SY, Miller KJ, et al. PET of brain amyloid and tau in mild cognitive impairment. N Engl J Med 2006;355:2652-63. (Pubitemid 44969124)
57. Drzezga A, Becker JA, Van Dijk KR, Sreenivasan A, Talukdar T, Sullivan C, et al. Neuronal dysfunction and disconnection of cortical hubs in non-demented subjects with elevated amyloid burden. Brain 2011;134:1635-46. doi:10.1093/brain/awr066.
58. Raji CA, Becker JT, Tsopelas ND, Price JC, Mathis CA, Saxton JA, et al. Characterizing regional correlation, laterality and symmetry of amyloid deposition in mild cognitive impairment and Alzheimer's disease with Pittsburgh Compound B. J Neurosci Methods 2008;172:277-82.
59. Pengas G, Hodges JR, Watson P, Nestor PJ. Focal posterior cingulate atrophy in incipient Alzheimer's disease. Neurobiol Aging 2010;31:25-33.