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PMID: 19955375 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

One-year brain atrophy evident in healthy aging.

Fjell AM, Walhovd KB, Fennema-Notestine C, McEvoy LK, Hagler DJ, Holland D, Brewer JB, Dale AM

Abstract

An accurate description of changes in the brain in healthy aging is needed to understand the basis of age-related changes in cognitive function. Cross-sectional magnetic resonance imaging (MRI) studies suggest thinning of the cerebral cortex, volumetric reductions of most subcortical structures, and ventricular expansion. However, there is a paucity of detailed longitudinal studies to support the cross-sectional findings. In the present study, 142 healthy elderly participants (60-91 years of age) were followed with repeated MRI, and were compared with 122 patients with mild to moderate Alzheimer's disease (AD). Volume changes were measured across the entire cortex and in 48 regions of interest. Cortical reductions in the healthy elderly were extensive after only 1 year, especially evident in temporal and prefrontal cortices, where annual decline was approximately 0.5%. All subcortical and ventricular regions except caudate nucleus and the fourth ventricle changed significantly over 1 year. Some of the atrophy occurred in areas vulnerable to AD, while other changes were observed in areas less characteristic of the disease in early stages. This suggests that the changes are not primarily driven by degenerative processes associated with AD, although it is likely that preclinical changes associated with AD are superposed on changes due to normal aging in some subjects, especially in the temporal lobes. Finally, atrophy was found to accelerate with increasing age, and this was especially prominent in areas vulnerable to AD. Thus, it is possible that the accelerating atrophy with increasing age is due to preclinical AD.

MeSH Terms
Aged Aged, 80 and over Aging/pathology Alzheimer Disease/pathology Atrophy/pathology Brain/pathology Brain Mapping Female Follow-Up Studies Humans Imaging, Three-Dimensional/methods Magnetic Resonance Imaging/methods Male Middle Aged Time Factors
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Fjell Anders M
Center for the Study of Human Cognition, Department of Psychology, University of Oslo, 0317 Oslo, Norway. [email protected]
Walhovd Kristine B
Fennema-Notestine Christine
McEvoy Linda K
Hagler Donald J
Holland Dominic
Brewer James B
Dale Anders M
References (66)
66 references, click to expand
  1. Normal neuroanatomical variation due to age: the major lobes and a parcellation of the temporal region.
    Neurobiol Aging. 2005 Oct;26(9):1245-60; discussion 1279-82 PMID: 16046030
  2. 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 Jul;34(7):939-44 PMID: 6610841
  3. One-year age changes in MRI brain volumes in older adults.
    Cereb Cortex. 2000 May;10(5):464-72 PMID: 10847596
  4. "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician.
    J Psychiatr Res. 1975 Nov;12(3):189-98 PMID: 1202204
  5. Rate of medial temporal lobe atrophy in typical aging and Alzheimer's disease.
    Neurology. 1998 Oct;51(4):993-9 PMID: 9781519
  6. High-dimensional image registration using symmetric priors.
    Neuroimage. 1999 Jun;9(6 Pt 1):619-28 PMID: 10334905
  7. Patterns of age-related shrinkage in cerebellum and brainstem observed in vivo using three-dimensional MRI volumetry.
    Cereb Cortex. 1999 Oct-Nov;9(7):712-21 PMID: 10554994
  8. Spatial patterns of cortical thinning in mild cognitive impairment and Alzheimer's disease.
    Brain. 2006 Nov;129(Pt 11):2885-93 PMID: 17008332
  9. Different regional patterns of cortical thinning in Alzheimer's disease and frontotemporal dementia.
    Brain. 2007 Apr;130(Pt 4):1159-66 PMID: 17353226
  10. Effects of age on volumes of cortex, white matter and subcortical structures.
    Neurobiol Aging. 2005 Oct;26(9):1261-70; discussion 1275-8 PMID: 16005549
  11. Age-associated alterations in cortical gray and white matter signal intensity and gray to white matter contrast.
    Neuroimage. 2009 Oct 15;48(1):21-8 PMID: 19580876
  12. Reliability in multi-site structural MRI studies: effects of gradient non-linearity correction on phantom and human data.
    Neuroimage. 2006 Apr 1;30(2):436-43 PMID: 16300968
  13. Minute effects of sex on the aging brain: a multisample magnetic resonance imaging study of healthy aging and Alzheimer's disease.
    J Neurosci. 2009 Jul 8;29(27):8774-83 PMID: 19587284
  14. A nonparametric method for automatic correction of intensity nonuniformity in MRI data.
    IEEE Trans Med Imaging. 1998 Feb;17(1):87-97 PMID: 9617910
  15. Longitudinal magnetic resonance imaging studies of older adults: a shrinking brain.
    J Neurosci. 2003 Apr 15;23(8):3295-301 PMID: 12716936
  16. Thalamic volume predicts performance on tests of cognitive speed and decreases in healthy aging. A magnetic resonance imaging-based volumetric analysis.
    Brain Res Cogn Brain Res. 2001 Jun;11(3):377-85 PMID: 11339987
  17. Molecular, structural, and functional characterization of Alzheimer's disease: evidence for a relationship between default activity, amyloid, and memory.
    J Neurosci. 2005 Aug 24;25(34):7709-17 PMID: 16120771
  18. Changes in volume with age--consistency and interpretation of observed effects.
    Neurobiol Aging. 2005 Oct;26(9):1271-4; discussion 1275-8 PMID: 16006011
  19. MRI-Based topographic parcellation of human cerebral white matter and nuclei II. Rationale and applications with systematics of cerebral connectivity.
    Neuroimage. 1999 Jan;9(1):18-45 PMID: 9918726
  20. Effects of age and sex on volumes of the thalamus, pons, and cortex.
    Neurobiol Aging. 2004 Feb;25(2):185-92 PMID: 14749136
  21. Mapping the evolution of regional atrophy in Alzheimer's disease: unbiased analysis of fluid-registered serial MRI.
    Proc Natl Acad Sci U S A. 2002 Apr 2;99(7):4703-7 PMID: 11930016
  22. Differential aging of the brain: patterns, cognitive correlates and modifiers.
    Neurosci Biobehav Rev. 2006;30(6):730-48 PMID: 16919333
  23. High-resolution intersubject averaging and a coordinate system for the cortical surface.
    Hum Brain Mapp. 1999;8(4):272-84 PMID: 10619420
  24. A controlled study of cortical gray matter and ventricular changes in alcoholic men over a 5-year interval.
    Arch Gen Psychiatry. 1998 Oct;55(10):905-12 PMID: 9783561
  25. Prefrontal cortex atrophy predicts dementia over a six-year period.
    Neurobiol Aging. 2009 Sep;30(9):1413-9 PMID: 18258339
  26. Effects of age on tissues and regions of the cerebrum and cerebellum.
    Neurobiol Aging. 2001 Jul-Aug;22(4):581-94 PMID: 11445259
  27. Longitudinal progression of Alzheimer's-like patterns of atrophy in normal older adults: the SPARE-AD index.
    Brain. 2009 Aug;132(Pt 8):2026-35 PMID: 19416949
  28. Risk factors for progression of brain atrophy in aging: six-year follow-up of normal subjects.
    Neurology. 2005 May 24;64(10):1704-11 PMID: 15911795
  29. MRI of hippocampal volume loss in early Alzheimer's disease in relation to ApoE genotype and biomarkers.
    Brain. 2009 Apr;132(Pt 4):1067-77 PMID: 19251758
  30. Morphometric changes in the episodic memory network and tau pathologic features correlate with memory performance in patients with mild cognitive impairment.
    AJNR Am J Neuroradiol. 2008 Jun;29(6):1183-9 PMID: 18544670
  31. The prevalence of cortical gray matter atrophy may be overestimated in the healthy aging brain.
    Neuropsychology. 2009 Sep;23(5):541-50 PMID: 19702408
  32. Early marker for Alzheimer's disease: the atrophic hippocampus.
    Lancet. 1989 Sep 16;2(8664):672-3 PMID: 2570916
  33. Cerebral structure on MRI, Part I: Localization of age-related changes.
    Biol Psychiatry. 1991 Jan 1;29(1):55-67 PMID: 2001446
  34. Cortical surface-based analysis. I. Segmentation and surface reconstruction.
    Neuroimage. 1999 Feb;9(2):179-94 PMID: 9931268
  35. A voxel-based morphometric study of ageing in 465 normal adult human brains.
    Neuroimage. 2001 Jul;14(1 Pt 1):21-36 PMID: 11525331
  36. Mathematical textbook of deformable neuroanatomies.
    Proc Natl Acad Sci U S A. 1993 Dec 15;90(24):11944-8 PMID: 8265653
  37. Differential age-related changes in the regional metencephalic volumes in humans: a 5-year follow-up.
    Neurosci Lett. 2003 Oct 9;349(3):163-6 PMID: 12951194
  38. Aging, gender, and the elderly adult brain: an examination of analytical strategies.
    Neurobiol Aging. 2008 Feb;29(2):290-302 PMID: 17049410
  39. Regional brain changes in aging healthy adults: general trends, individual differences and modifiers.
    Cereb Cortex. 2005 Nov;15(11):1676-89 PMID: 15703252
  40. Atrophy rates of entorhinal cortex in AD and normal aging.
    Neurology. 2003 Feb 11;60(3):481-6 PMID: 12578931
  41. Measuring the thickness of the human cerebral cortex from magnetic resonance images.
    Proc Natl Acad Sci U S A. 2000 Sep 26;97(20):11050-5 PMID: 10984517
  42. Structural MRI biomarkers for preclinical and mild Alzheimer's disease.
    Hum Brain Mapp. 2009 Oct;30(10):3238-53 PMID: 19277975
  43. An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest.
    Neuroimage. 2006 Jul 1;31(3):968-80 PMID: 16530430
  44. Improved Localizadon of Cortical Activity by Combining EEG and MEG with MRI Cortical Surface Reconstruction: A Linear Approach.
    J Cogn Neurosci. 1993 Spring;5(2):162-76 PMID: 23972151
  45. A meta-analysis of hippocampal atrophy rates in Alzheimer's disease.
    Neurobiol Aging. 2009 Nov;30(11):1711-23 PMID: 18346820
  46. Longitudinal pattern of regional brain volume change differentiates normal aging from MCI.
    Neurology. 2009 Jun 2;72(22):1906-13 PMID: 19487648
  47. Regional rates of neocortical atrophy from normal aging to early Alzheimer disease.
    Neurology. 2009 Aug 11;73(6):457-65 PMID: 19667321
  48. Automatically parcellating the human cerebral cortex.
    Cereb Cortex. 2004 Jan;14(1):11-22 PMID: 14654453
  49. High consistency of regional cortical thinning in aging across multiple samples.
    Cereb Cortex. 2009 Sep;19(9):2001-12 PMID: 19150922
  50. Alzheimer disease: quantitative structural neuroimaging for detection and prediction of clinical and structural changes in mild cognitive impairment.
    Radiology. 2009 Apr;251(1):195-205 PMID: 19201945
  51. Prediction of AD with MRI-based hippocampal volume in mild cognitive impairment.
    Neurology. 1999 Apr 22;52(7):1397-403 PMID: 10227624
  52. Aging, sexual dimorphism, and hemispheric asymmetry of the cerebral cortex: replicability of regional differences in volume.
    Neurobiol Aging. 2004 Mar;25(3):377-96 PMID: 15123343
  53. Modeling brain deformations in Alzheimer disease by fluid registration of serial 3D MR images.
    J Comput Assist Tomogr. 1998 Sep-Oct;22(5):838-43 PMID: 9754126
  54. Increased sensitivity to effects of normal aging and Alzheimer's disease on cortical thickness by adjustment for local variability in gray/white contrast: a multi-sample MRI study.
    Neuroimage. 2009 Oct 1;47(4):1545-57 PMID: 19501655
  55. Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain.
    Neuron. 2002 Jan 31;33(3):341-55 PMID: 11832223
  56. A longitudinal study of brain volume changes in normal aging using serial registered magnetic resonance imaging.
    Arch Neurol. 2003 Jul;60(7):989-94 PMID: 12873856
  57. Consistent neuroanatomical age-related volume differences across multiple samples.
    Neurobiol Aging. 2011 May;32(5):916-32 PMID: 19570593
  58. Age effects on atrophy rates of entorhinal cortex and hippocampus.
    Neurobiol Aging. 2006 May;27(5):733-40 PMID: 15961190
  59. The Clinical Dementia Rating (CDR): current version and scoring rules.
    Neurology. 1993 Nov;43(11):2412-4 PMID: 8232972
  60. Thinning of the cerebral cortex in aging.
    Cereb Cortex. 2004 Jul;14(7):721-30 PMID: 15054051
  61. The cortical signature of Alzheimer's disease: regionally specific cortical thinning relates to symptom severity in very mild to mild AD dementia and is detectable in asymptomatic amyloid-positive individuals.
    Cereb Cortex. 2009 Mar;19(3):497-510 PMID: 18632739
  62. Normative estimates of cross-sectional and longitudinal brain volume decline in aging and AD.
    Neurology. 2005 Mar 22;64(6):1032-9 PMID: 15781822
  63. Deformable templates using large deformation kinematics.
    IEEE Trans Image Process. 1996;5(10):1435-47 PMID: 18290061
  64. Cortical surface-based analysis. II: Inflation, flattening, and a surface-based coordinate system.
    Neuroimage. 1999 Feb;9(2):195-207 PMID: 9931269
  65. Differential aging of the human striatum: a prospective MR imaging study.
    AJNR Am J Neuroradiol. 1998 Sep;19(8):1501-7 PMID: 9763385
  66. Comparisons between global and focal brain atrophy rates in normal aging and Alzheimer disease: Boundary Shift Integral versus tracing of the entorhinal cortex and hippocampus.
    Alzheimer Dis Assoc Disord. 2004 Oct-Dec;18(4):196-201 PMID: 15592130
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
2009-12-02
Pages
15223-31
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC2827793
Subset
IM
Grants
NCRR NIH HHS · U24 RR021382 · United States
NIA NIH HHS · U01 AG024904-01 · United States
NIA NIH HHS · R01 AG031224 · United States
NIA NIH HHS · U01 AG024904-04 · United States
NIA NIH HHS · K01AG029218 · United States
NIA NIH HHS · U01 AG024904-04S1 · United States
NIA NIH HHS · U01 AG024904-05S4 · United States
NIA NIH HHS · U01 AG024904-03 · United States
NIA NIH HHS · U01 AG024904-05S2 · United States
NIA NIH HHS · R01 AG031244 · United States
NIA NIH HHS · U01 AG024904-02 · United States
NIA NIH HHS · U01 AG024904-05S1 · United States
NIA NIH HHS · U01 AG024904-01S2 · United States
NIA NIH HHS · U01 AG024904-05S6 · United States
NIA NIH HHS · U01 AG024904 · United States
NIA NIH HHS · U19 AG010483 · United States
NIA NIH HHS · U01 AG024904-01S1 · United States
NIA NIH HHS · U01 AG024904-05S5 · United States
NIA NIH HHS · U01 AG024904-03S1A1 · United States
NIA NIH HHS · U01 AG024904-05 · United States
NIA NIH HHS · U01 AG024904-03S4 · United States
NIA NIH HHS · U01 AG024904-04S2 · United States
NIA NIH HHS · R01 AG031224-01A1 · United States
NIA NIH HHS · U01 AG024904-05S3 · United States
NIA NIH HHS · K01 AG029218 · United States
NIA NIH HHS · U01 AG024904-03S5 · United States
NIA NIH HHS · U01 AG024904-03S3 · United States
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