Dynamics of gray matter loss in Alzheimer's disease

Journal of Neuroscience

Volumn 23, Issue 3, 2003, Pages 994-1005

  Thompson, Paul M ^a   Hayashi, Kiralee M ^a   De Zubicaray, Greig ^b   Janke, Andrew L ^b   Rose, Stephen E ^b   Semple, James ^c   Herman, David ^a   Hong, Michael S ^a   Dittmer, Stephanie S ^a   Doddrell, David M ^b   Toga, Arthur W ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF QUEENSLAND   (Australia)

^c ADDENBROOKE S HOSPITAL   (United Kingdom)

Author keywords

Aging; Alzheimer's disease; Brain mapping; Cortex; Dementia; Imaging; Longitudinal; Magnetic resonance imaging

Indexed keywords

AGED; ALZHEIMER DISEASE; ARTICLE; BRAIN ATROPHY; BRAIN MAPPING; BRAIN REGION; CLINICAL ARTICLE; COGNITIVE DEFECT; CONTROLLED STUDY; FEMALE; FRONTAL CORTEX; GRAY MATTER; HUMAN; LEFT HEMISPHERE; LIMBIC CORTEX; MALE; NEUROFIBRILLARY TANGLE; NUCLEAR MAGNETIC RESONANCE IMAGING; OCCIPITAL CORTEX; PRIORITY JOURNAL; RIGHT HEMISPHERE; TEMPORAL CORTEX;

EID: 0037319171     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.23-03-00994.2003     Document Type: Article

References (101)

1. American Psychiatric Association (2000) Diagnostic and statistical manual of mental disorders, Ed 4 (DSM-IV). Washington, DC: American Psychiatric Association.
2. Arnold SE, Hyman BT, Flory J, Damasio AR, Van Hoesen GW (1991) The topographical and neuroanatomical distribution of neurofibrillary tangles and neuritic plaques in the cerebral cortex of patients with Alzheimer's disease. Cereb Cortex 1:103-116.
3. Arriagada P, Growdon JH, Hedley-Whyte ET, Hyman BT (1992) Neurofibrillary tangles, but not plaques parallel duration and severity of Alzheimer's disease. Neurology 42:631-639.
4. Ashburner J, Friston KJ (2000) Voxel-based morphometry - the methods. NeuroImage 11:805-821.
5. Ashburner J, Friston KJ (2001) Why voxel-based morphometry should be used. NeuroImage 14:1238-1243.
6. Ashburner J, Csernansky J, Davatzikos C, Fox NC, Frisoni G, Thompson PM (2003) Computational neuroanatomy: towards a computer-assisted diagnosis of degenerative brain diseases based on magnetic resonance imaging. Lancet Neurol, in press.
7. Baron JC, Chetelat G, Desgranges B, Perchey G, Landeau B, de la Sayette V, Eustache F (2001) In vivo mapping of gray matter loss with voxel-based morphometry in mild Alzheimer's disease. NeuroImage 14:298-309.
8. Bookstein FL (2001) Voxel-based morphometry should not be used with imperfectly registered images. NeuroImage 14:1454-1462.
9. Braak H, Braak E (1991) Neuropathological staging of Alzheimer related changes. Acta Neuropathol 82:239-259.
10. Braak H, Braak E (1997) Staging of Alzheimer-related cortical destruction. Int Psychogeriatr 9[Suppl 1]:257-261; discussion 269-272.
11. Brion JP, Octave JN, Couck AM (1994) Distribution of the phosphorylated microtubule-associated protein tau in developing cortical neurons. Neuroscience 63:895-909.
12. Brun A, Englund E (1981) Regional pattern of degeneration in Alzheimer's disease: neuronal loss and histopathologic grading. Histopathology 5:549-564.
13. Bullmore ET, Suckling J, Overmeyer S, Rabe-Hesketh S, Taylor E, Brammer MJ (1999) Global, voxel, and cluster tests, by theory and permutation, for a difference between two groups of structural MR images of the brain. IEEE Trans Med Imaging 18:32-42.
14. Cannon TD, Thompson PM, van Erp T, Toga AW, Poutanen V-P, Huttunen M, Lönnqvist J, Standertskjöld-Nordenstam C-G, Narr KL, Khaledy M, Zoumalan CI, Dail R, Kaprio J (2002) Cortex mapping reveals regionally specific patterns of genetic and disease-specific gray-matter deficits in twins discordant for schizophrenia. Proc Natl Acad Sci USA 99:3228-3233.
15. Clinton J, Blackman SEA, Royston MC, Robert GW (1994) Differential synaptic loss in the cortex in AD: a study using archival material. NeuroReport 5:497-500.
16. Collins DL, Neelin P, Peters T, Evans AC (1994) Automatic 3D intersubject registration of MR volumetric data in standardized Talairach space. J Comput Assist Tomogr 18:192-205.
17. de Brabander JM, Kramers RJ, Uylings HB (1998) Layer-specific dendritic regression of pyramidal cells with aging in the human prefrontal cortex. Eur J Neurosci 10:1261-1269.
18. DeCarli C (2000) Part IV. Neuroimaging in dementing disorders. Dis Mon 46:706-724.
19. Delacourte A, David JP, Sergeant N, Buee L, Wattez A, Vermersch P, Ghozali F, Fallet-Bianco C, Pasquier F, Lebert F, Petit H, Di Menza C (1999) The biochemical pathway of neurofibrillary degeneration in aging and Alzheimer's disease. Neurology 52:1158-1165.
20. de la Torre JC (2002) Alzheimer disease as a vascular disorder: nosological evidence. Stroke 33:1152-1162.
21. Evans AC, Collins DL, Neelin P, MacDonald D, Kamber M, Marrett TS (1994) Three-dimensional correlative imaging: applications in human brain mapping. In: Functional neuroimaging: technical foundations (Thatcher RW, Hallett M, Zeffiro T, John ER, Huerta M, eds), pp 145-162. San Diego: Academic.
22. Fischl B, Sereno MI, Tootell RBH, Dale AM (1999) High-resolution intersubject averaging and a coordinate system for the cortical surface. Hum Brain Mapp 8:272-284.
23. Flood DG, Buell SJ, Horwitz GJ, Coleman PD (1987) Dendritic extent in human dentate gyrus granule cells in normal aging and senile dementia. Brain Res 402:205-216.
24. Folstein MF, Folstein SE, McHugh PR (1975) "Mini mental state": a practical method of grading the cognitive state of patients for the clinician. J Psychiatr Res 12:189-198.
25. Fox NC, Freeborough PA, Rossor MN (1996) Visualisation and quantification of rates of atrophy in AD. Lancet 348:94-97.
26. Fox NC, Scahill RI, Crum WR, Rossor MN (1999) Correlation between rates of brain atrophy and cognitive decline in AD. Neurology 52:1687-1689.
27. Fox NC, Cousens S, Scahill R, Harvey RJ, Rossor MN (2000) Using serial registered brain magnetic resonance imaging to measure disease progression in Alzheimer disease: power calculations and estimates of sample size to detect treatment effects. Arch Neurol 57:339-344.
28. Freeborough PA, Fox NC (1998) Modeling brain deformations in Alzheimer disease by fluid registration of serial 3D MR images. J Comput Assist Tomogr 22:838-843.
29. Friedland RP, Luxenberg J (1988) Neuroimaging and dementia. In: Clinical neuroimaging: frontiers in clinical neuroscience, Vol 4 (Theodore WH, ed), pp 139-163. New York: Allan Liss.
30. Friston KJ, Holmes A, Poline JB, Price CJ, Frith CD 1996 Detecting activations in PET and fMRI: levels of inference and power. NeuroImage 4:223-235.
31. Geschwind N, Levitsky W (1968) Human brain: left-right asymmetries in temporal speech region. Science 161:186-187.
32. Gomez-Isla T, Hollister R, West H, Mui S, Growdon JH, Petersen RC, Parisi JE, Hyman BT (1997) Neuronal loss correlates with but exceeds neurofibrillary tangles in Alzheimer's disease. Ann Neurol 41:17-24.
33. Good CD, Johnsrude IS, Ashburner J, Henson RN, Friston KJ, Frackowiak RSJ (2001) A voxel-based morphometric study of aging in 465 normal adult human brains. NeuroImage 14:21-36.
34. Hampel H, Teipel SJ, Alexander GE, Pogarell O, Rapoport SI, Moller HJ (2002) In vivo imaging of region and cell type specific neocortical neurodegeneration in Alzheimer's disease: perspectives of MRI derived corpus callosum measurement for mapping disease progression and effects of therapy. Evidence from studies with MRI, EEG and PET. J Neural Transm 109:837-855.
35. Hanks SD, Flood DG (1991) Region-specific stability of dendritic extent in normal human aging and regression in Alzheimer's disease. I. CA1 of hippocampus. Brain Res 540:63-82.
36. Hayashi KM, Thompson PM, Mega MS, Zoumalan CI (2002) Medial hemispheric surface gyral pattern delineation in 3D: surface curve protocol. Available at: http://www.loni.ucla.edu/∼khayashi/Public/medial_surface/Medial LinesProtocol.
37. Hof PR, Morrison JH (1994) The cellular basis of cortical disconnection in Alzheimer disease and related dementing conditions. In: Alzheimer disease (Terry RD, Katzman R, Bick KL, eds), pp 197-229. New York: Raven.
38. Holmes AP, Blair RC, Watson JD, Ford I (1996) Nonparametric analysis of statistic images from functional mapping experiments. J Cereb Blood Flow Metab 16:7-22.
39. Hubbard BM, Anderson JM (1981) A quantitative study of cerebral atrophy in old age and senile dementia. J Neurol Sci 50:135-145.
40. (1-42) and tau levels in CSF. Neurology 52:1555-1562.
41. Jack Jr CR, Petersen RC, Xu Y, O'Brien PC, Smith GE, Ivnik RJ, Tangalos EG, Kokmen E (1998) Rate of medial temporal lobe atrophy in typical aging and Alzheimer's disease. Neurology 51:993-999.
42. Jagust WJ, Haan MN, Eberling JL, Wolfe N, Reed BR (1996) Functional imaging predicts cognitive decline in Alzheimer's disease. J Neuroimaging 6:156-160.
43. Janke AL, de Zubicaray GI, Rose SE, Griffin M, Chalk JB, Galloway GJ (2001) 4D deformation modeling of cortical disease progression in Alzheimer's dementia. Magn Reson Med 46:661-666.
44. Jernigan TL, Salmon D, Butters N, Hesselink JR (1991) Cerebral structure on MRI, part II: specific changes in Alzheimer's and Huntington's diseases. Biol Psychiatry 29:68-81.
45. Jobst KA, Smith AD, Szatmari M, Esiri MM, Jaskowski A, Hindley N, McDonald B, Molyneux AJ (1994) Rapidly progressing atrophy of medial temporal lobe in Alzheimer's disease. Lancet 343:829-830.
46. Johnson KA, Jones K, Holman BL, Becker JA, Spiers PA, Satlin A, Albert MS (1998) Preclinical prediction of Alzheimer's disease using SPECT. Neurology 50:1563-1571.
47. Kaye J, Moore M, Kerr D (1999) The rate of brain volume loss accelerates as Alzheimer's disease progresses from a presymptomatic phase to frank dementia. Neurology 52[Suppl]:A569-A570.
48. Kaye JA, Swihart T, Howieson D, Dame A, Moore MM, Karnos T, Camicioli R, Ball M, Oken B, Sexton G (1997) Volume loss of the hippocampus and temporal lobe in healthy elderly persons destined to develop dementia. Neurology 48:1297-1304.
49. Laakso MP, Lehtovirta M, Partanen K, Riekkinen PJ, Soininen H (2000) Hippocampus in AD: a 3-year follow-up MRI study. Biol Psychiatry 47:557-561.
50. Lehtovirta M, Laakso MP, Frisoni GB, Soininen H (2000) How does the apolipoprotein E genotype modulate the brain in aging and in Alzheimer's disease? A review of neuroimaging studies. Neurobiol Aging 21:293-300.
51. Leonard CM (1996) Structural variation in the developing and mature cerebral cortex: noise or signal? In: Developmental neuroimaging: mapping the development of brain and behavior (Thatcher RW, Reid Lyon G, Rumsey J, Krasnegor N, eds), pp. 207-231. New York: Academic.
52. Loewenstein DA, Barker WW, Chang JY, Apicella A, Yoshii F, Kothari P, Levin B, Duara R (1989) Predominant left hemisphere metabolic dysfunction in dementia. Arch Neurol 46:146-152.
53. MacDonald D, Kabani N, Avis D, Evans AC (2000) Automated 3-D extraction of inner and outer surfaces of cerebral cortex from MRI. NeuroImage 12:340-356.
54. Mazziotta JC, Frackowiak RS, Phelps ME (1992) The use of positron emission tomography in the clinical assessment of dementia. Semin Nucl Med 22:233-246.
55. McEwen BS (1997) Possible mechanisms for atrophy of the human hippocampus. Mol Psychiatry 2:255-262.
56. McKhann G, Drachman D, Folstein M, Katzman R, Price D, Stadian EM (1984) Clinical diagnosis of AD: report of the NINCDS-ARDRA Work Group under the auspices of the Health and Human Services Task Force on Alzheimer's Disease. Neurology 34:939-944.
57. Mega MS, Chen S, Thompson PM, Woods RP, Karaca TJ, Tiwari A, Vinters H, Small GW, Toga AW (1997) Mapping pathology to metabolism: coregistration of stained whole brain sections to PET in AD. NeuroImage 5:147-153.
58. Mesulam MM (2000) A plasticity-based theory of the pathogenesis of Alzheimer's disease. Ann NY Acad Sci 924:42-52.
59. Morrison JH, Hof PR (1997) Life and death of neurons in the aging brain. Science 278:412-419.
60. Morrison JH, Hof PR (2002) Selective vulnerability of corticocortical and hippocampal circuits in aging and Alzheimer's disease. Prog Brain Res 136:467-486.
61. Mummery CJ, Patterson K, Price CJ, Ashburner J, Frackowiak RS, Hodges JR (2000) A voxel-based morphometry study of semantic dementia: relationship between temporal lobe atrophy and semantic memory. Ann Neurol 47:36-45.
62. Murphy DGM, DeCarli CD, Daly E, Gillette JA, McIntosh AR, Haxby JV, Teichberg D, Schapiro MB, Rapoport SI, Horwitz B (1993) Volumetric magnetic resonance imaging in men with dementia of the Alzheimer type: correlations with disease severity. Biol Psychiatry 34:612-621.
63. Nakamura S, Akiguchi I, Kameyama M, Kudo M, Mizuno N (1984) Senile changes in the basal dendrites of the pyramidal cells in the human motor cortex: a quantitative Golgi study. Rinsho Shinkeigaku 24:85-95.
64. Nichols TE, Holmes AP (2002) Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum Brain Mapp 15:1-25.
65. O'Brien JT, Paling S, Barber R, Williams ED, Ballard C, McKeith IG, Gholkar A, Crum WR, Rossor MN, Fox NC (2001) Progressive brain atrophy on serial MRI in dementia with Lewy bodies, AD, and vascular dementia. Neurology 56:1386-1388.
66. Ono M, Kubik S, Abernathey CD (1990) Atlas of the cerebral sulci. Stuttgart, Germany: Thieme.
67. Pearson RCA, Esiri MM, Hiorns RW, Wilcock GK, Powell TPS (1985) Anatomical correlates of the distribution of the pathological changes in the neocortex in Alzheimer's disease. Proc Natl Acad Sci USA 82:4531-4534.
68. Price JL, Morris JC (1999) Tangles and plaques in nondemented aging and "preclinical" Alzheimer's disease. Ann Neurol 45:358-368.
69. Reiman EM, Caselli RJ, Chen K, Alexander GE, Bandy D, Frost J (2001) Declining brain activity in cognitively normal apolipoprotein E epsilon 4 heterozygotes: a foundation for using positron emission tomography to efficiently test treatments to prevent Alzheimer's disease. Proc Natl Acad Sci USA 98:3334-3339.
70. Rombouts SA, Barkhof F, Witter MP, Scheltens P (2000) Unbiased whole-brain analysis of gray matter loss in Alzheimer's disease. Neurosci Lett 285:231-233.
71. Scahill RI, Schott JM, Stevens JM, Rossor MN, Fox NC (2002) Mapping the evolution of regional atrophy in Alzheimer's disease: unbiased analysis of fluid-registered serial MRI. Proc Natl Acad Sci USA 99:4703-4707.
72. Shimada A (1999) Age-dependent cerebral atrophy and cognitive dysfunction in SAMP10 mice. Neurobiol Aging 20:125-136.
73. Simic G, Kostovic I, Winblad B, Bogdanovic N (1997) Volume and number of neurons of the human hippocampal formation in normal aging and Alzheimer's disease. J Comp Neurol 379:482-494.
74. Sled JG, Zijdenbos AP, Evans AC (1998) A non-parametric method for automatic correction of intensity non-uniformity in MRI data. IEEE Trans Med Imaging 17:87-97.
75. Small GW, Ercoli LM, Silverman DH, Huang SC, Komo S, Bookheimer SY, Lavretsky H, Miller K, Siddarth P, Rasgon NL, Mazziotta JC, Saxena S, Wu HM, Mega MS, Cummings JL, Saunders AM, Pericak-Vance MA, Roses AD, Barrio JR, Phelps ME (2000) Cerebral metabolic and cognitive decline in persons at genetic risk for Alzheimer's disease. Proc Natl Acad Sci USA 97:6037-6042.
76. Sowell ER, Thompson PM, Holmes CJ, Jernigan TL, Toga AW (1999) Progression of structural changes in the human brain during the first three decades of life: in vivo evidence for post-adolescent frontal and striatal maturation. Nat Neurosci 2:859-861.
77. Sowell ER, Thompson PM, Mega MS, Zoumalan CI, Lindshield C, Rex DE (2000) Gyral pattern delineation in 3D: surface curve protocol. Available at: http://www.loni.ucla.edu/∼esowell/new_sulcvar.html.
78. Sowell ER, Thompson PM, Tessner KD, Toga AW (2001) Accelerated brain growth and cortical gray matter thinning are inversely related during post-adolescent frontal lobe maturation. J Neurosci 21:8819-8829.
79. Steinmetz H, Furst G, Freund H-J (1990) Variation ofperisylvian and calcarine anatomic landmarks within stereotaxic proportional coordinates. Am J Neuroradiol 11:1123-1130.
80. Studholme C, Cardenas V, Schuff N, Rosen H, Miller B, Weiner MW (2001) Detecting spatially consistent structural differences in Alzheimer's and frontotemporal dementia using deformation morphometry. Proceedings of the Third International Conference on Medical Image Computing and Computer Assisted Intervention (MICCAI). Berlin: Springer.
81. Subsol G, Roberts N, Doran M, Thirion JP, Whitehouse GH (1997) Automatic analysis of cerebral atrophy. Magn Reson Imaging 15:917-927.
82. Terry RD, DeTeresa R, Hansen LA (1987) Neocortical cell counts in normal human adult aging. Ann Neurol 21:530-539.
83. Thompson PM, Mega MS, Narr KL, Sowell ER, Blanton RE, Toga AW (2000) Brain image analysis and atlas construction. In: Handbook on medical image analysis (Fitzpatrick M, Sonka M, eds). Bellingham, WA: SPIE.
84. Thompson PM, Toga AW (1997) Detection, visualization and animation of abnormal anatomic structure with a deformable probabilistic brain atlas based on random vector field transformations. Med Image Anal 1:271-294.
85. Thompson PM, Toga AW (2002) A framework for computational anatomy. Comput Vis Sci 5:1-12.
86. Thompson PM, MacDonald D, Mega MS, Holmes CJ, Evans AC, Toga AW (1997) Detection and mapping of abnormal brain structure with a probabilistic atlas of cortical surfaces. J Comp Assist Tomogr 21:567-581.
87. Thompson PM, Moussai J, Khan AA, Zohoori S, Goldkorn A, Mega MS, Small GW, Cummings JL, Toga AW (1998) Cortical variability and asymmetry in normal aging and Alzheimer's disease. Cereb Cortex 8:492-509.
88. Thompson PM, Giedd JN, Woods RP, MacDonald D, Evans A, Toga AW (2000a) Growth patterns in the developing brain detected by using continuum-mechanical tensor maps. Nature 404:190-193.
89. Thompson PM, Woods RP, Mega MS, Toga AW (2000b) Mathematical/computational challenges in creating deformable and probabilistic atlases of the human brain. Hum Brain Mapp 9:81-92.
90. Thompson PM, Cannon TD, Narr KL, van Erp T, Khaledy M, Poutanen V-P, Huttunen M, Lönnqvist J, Standertskjöld-Nordenstam C-G, Kaprio J, Dail R, Zoumalan CI, Toga AW (2001a) Genetic influences on brain structure. Nat Neurosci 4:1253-1258.
91. Thompson PM, Mega RS, Woods RP, Zoumalan CI, Lindshield CJ, Blanton RE, Moussai J, Holmes CJ, Cummings JL, Toga AW (2001b) Cortical change in Alzheimer's disease detected with a disease-specific population-based brain atlas. Cereb Cortex 11:1-16.
92. Thompson PM, Mega MS, Vidal C, Rapoport JL, Toga AW (2001c) Detecting disease-specific patterns of brain structure using cortical pattern matching and a population-based probabilistic brain atlas. IEEE Conference on Information Processing in Medical Imaging, Davis, CA. In: Lecture notes in computer science 2082 (Insana M, Leahy R, eds), pp 488-501. New York: Springer.
93. Thompson PM, Vidal CN, Giedd JN, Gochman P, Blumenthal J, Nicolson R, Toga AW, Rapoport JL (2001d) Mapping adolescent brain change reveals dynamic wave of accelerated gray matter loss in very early-onset schizophrenia. Proc Natl Acad Sci USA 98:11650-11655.
94. Thompson PM, Cannon TD, Toga AW (2003) Mapping genetic influences on human brain structure. Ann Med, in press.
95. Uylings HB, de Brabander JM (2002) Neuronal changes in normal human aging and Alzheimer's disease. Brain Cogn 49:268-276.
96. Wang D, Chalk JB, Rose SE, de Zubicaray GI, Cowin G, Galloway GJ, Barnes D, Spooner D, Doddrell DM, Semple J (2002) MR image-based measurement of rates of change in volumes of brain structures. Part II: application to a study of Alzheimer's disease and normal aging. Magn Reson Imaging 20:41-48.
97. Weinberger DR, McClure RK (2002) Neurotoxicity, neuroplasticity, and magnetic resonance imaging morphometry: what is happening in the schizophrenic brain? Arch Gen Psychiatry 59:553-558.
98. Woods RP, Mazziotta JC, Cherry SR (1993) MRI-PET registration with automated algorithm. J Comput Assist Tomogr 17:536-546.
99. Wright IC, McGuire PK, Poline JB, Travere JM, Murray RM, Frith CD, Frackowiak RS, Friston KJ (1995) A voxel-based method for the statistical analysis of gray and white matter density applied to schizophrenia. NeuroImage 2:244-252.
100. Yesavage JA (1988) Geriatric depression scale. Psychopharmacol Bull 24:709-711.
101. Zijdenbos AP, Dawant BM (1994) Brain segmentation and white matter lesion detection in MR images. Crit Rev Biomed Eng 22:401-465.