Home LiteratureArticle Details
PMID: 27228371 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Accelerated longitudinal gray/white matter contrast decline in aging in lightly myelinated cortical regions.

Human brain mapping ·Vol. 37 ·No. 10 ·2016-00-00 ·Pages 3669-84

Vidal-Piñeiro D, Walhovd KB, Storsve AB, Grydeland H, Rohani DA, Fjell AM

Abstract

Highly myelinated cortical regions seem to develop early and are more robust to age-related decline. By use of different magnetic resonance imaging (MRI) measures such as contrast between T1- and T2-weighted MRI scans (T1w/T2w) it is now possible to assess correlates of myelin content in vivo. Further, previous studies indicate that gray/white matter contrast (GWC) become blurred as individuals' age, apparently reflecting age-related changes in myelin structure. Here we address whether longitudinal changes in GWC are dependent on initial myelin content within tissue as defined by baseline T1w/T2w contrast, and hypothesize that lightly myelinated regions undergo more decline longitudinally. A sample of 207 healthy adult participants (range: 20-84 years) was scanned twice (interscan interval: 3.6 years). Results showed widespread longitudinal reductions of GWC throughout the cortical surface, especially in the frontal cortices, mainly driven by intensity decay in the white matter. Annual rate of GWC blurring showed acceleration with age in temporal and medial prefrontal regions. Moreover, the anatomical distribution of increased rate of GWC decline with advancing age was strongly related to baseline levels of intracortical myelin. This study provides a first evidence of accelerated regional GWC blurring with advancing age, relates GWC patterns to cortical myeloarchitectonics and supports the hypothesis of increased age-related vulnerability of lightly myelinated areas. Hum Brain Mapp 37:3669-3684, 2016. © 2016 Wiley Periodicals, Inc.

Keywords
T1w/T2w aging gray/white matter contrast lifespan myelin
MeSH Terms
Adult Aged Aged, 80 and over Aging/pathology Cerebral Cortex/diagnostic imaging Female Gray Matter/diagnostic imaging Humans Image Processing, Computer-Assisted Longitudinal Studies Magnetic Resonance Imaging Male Middle Aged Myelin Sheath Organ Size White Matter/diagnostic imaging Young Adult
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Vidal-Piñeiro Didac
Research Group for Lifespan Changes in Brain and Cognition, Department of Psychology, University of Oslo, Oslo, Norway.
Walhovd Kristine B
Research Group for Lifespan Changes in Brain and Cognition, Department of Psychology, University of Oslo, Oslo, Norway.
Storsve Andreas B
Research Group for Lifespan Changes in Brain and Cognition, Department of Psychology, University of Oslo, Oslo, Norway.
Grydeland Håkon
Research Group for Lifespan Changes in Brain and Cognition, Department of Psychology, University of Oslo, Oslo, Norway.
Rohani Darius A
Research Group for Lifespan Changes in Brain and Cognition, Department of Psychology, University of Oslo, Oslo, Norway.
Fjell Anders M
Research Group for Lifespan Changes in Brain and Cognition, Department of Psychology, University of Oslo, Oslo, Norway.
References (87)
87 references, click to expand
  1. Mapping human cortical areas in vivo based on myelin content as revealed by T1- and T2-weighted MRI.
    J Neurosci. 2011 Aug 10;31(32):11597-616 PMID: 21832190
  2. High consistency of regional cortical thinning in aging across multiple samples.
    Cereb Cortex. 2009 Sep;19(9):2001-12 PMID: 19150922
  3. Layer-specific variation of iron content in cerebral cortex as a source of MRI contrast.
    Proc Natl Acad Sci U S A. 2010 Feb 23;107(8):3834-9 PMID: 20133720
  4. Fiber composition of the human corpus callosum.
    Brain Res. 1992 Dec 11;598(1-2):143-53 PMID: 1486477
  5. The basis of anisotropic water diffusion in the nervous system - a technical review.
    NMR Biomed. 2002 Nov-Dec;15(7-8):435-55 PMID: 12489094
  6. In vivo myeloarchitectonic analysis of human striate and extrastriate cortex using magnetic resonance imaging.
    Cereb Cortex. 1992 Sep-Oct;2(5):417-24 PMID: 1422094
  7. Gray matter myelination of 1555 human brains using partial volume corrected MRI images.
    Neuroimage. 2015 Jan 15;105:473-85 PMID: 25449739
  8. Stereological estimation of the total number of myelinated callosal fibers in human subjects.
    J Anat. 2011 Mar;218(3):277-84 PMID: 21250987
  9. The relationship between diffusion tensor imaging and volumetry as measures of white matter properties.
    Neuroimage. 2008 Oct 1;42(4):1654-68 PMID: 18620064
  10. "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
  11. Trends and properties of human cerebral cortex: correlations with cortical myelin content.
    Neuroimage. 2014 Jun;93 Pt 2:165-75 PMID: 23567887
  12. Normal brain development and aging: quantitative analysis at in vivo MR imaging in healthy volunteers.
    Radiology. 2000 Sep;216(3):672-82 PMID: 10966694
  13. Morphometric and histologic substrates of cingulate integrity in elders with exceptional memory capacity.
    J Neurosci. 2015 Jan 28;35(4):1781-91 PMID: 25632151
  14. Ballooning of myelin sheaths in normally aged macaques.
    J Neurocytol. 1998 Aug;27(8):605-14 PMID: 10405027
  15. Decreased Default Mode Network connectivity correlates with age-associated structural and cognitive changes.
    Front Aging Neurosci. 2014 Sep 25;6:256 PMID: 25309433
  16. 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
  17. Alzheimer's disease: maladaptive synaptoplasticity hypothesis.
    Neurodegeneration. 1995 Jun;4(2):217-32 PMID: 7583687
  18. 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
  19. Selective aging of the human cerebral cortex observed in vivo: differential vulnerability of the prefrontal gray matter.
    Cereb Cortex. 1997 Apr-May;7(3):268-82 PMID: 9143446
  20. Heterogeneous age-related breakdown of white matter structural integrity: implications for cortical "disconnection" in aging and Alzheimer's disease.
    Neurobiol Aging. 2004 Aug;25(7):843-51 PMID: 15212838
  21. A nonparametric method for automatic correction of intensity nonuniformity in MRI data.
    IEEE Trans Med Imaging. 1998 Feb;17(1):87-97 PMID: 9617910
  22. The myeloarchitectonic studies on the human cerebral cortex of the Vogt-Vogt school, and their significance for the interpretation of functional neuroimaging data.
    Brain Struct Funct. 2013 Mar;218(2):303-52 PMID: 23076375
  23. Intracortical myelin links with performance variability across the human lifespan: results from T1- and T2-weighted MRI myelin mapping and diffusion tensor imaging.
    J Neurosci. 2013 Nov 20;33(47):18618-30 PMID: 24259583
  24. Prolonged myelination in human neocortical evolution.
    Proc Natl Acad Sci U S A. 2012 Oct 9;109(41):16480-5 PMID: 23012402
  25. Differentiating maturational and aging-related changes of the cerebral cortex by use of thickness and signal intensity.
    Neuroimage. 2010 Aug 1;52(1):172-85 PMID: 20347997
  26. What is normal in normal aging? Effects of aging, amyloid and Alzheimer's disease on the cerebral cortex and the hippocampus.
    Prog Neurobiol. 2014 Jun;117:20-40 PMID: 24548606
  27. Myelination of a key relay zone in the hippocampal formation occurs in the human brain during childhood, adolescence, and adulthood.
    Arch Gen Psychiatry. 1994 Jun;51(6):477-84 PMID: 8192550
  28. Differential aging of the brain: patterns, cognitive correlates and modifiers.
    Neurosci Biobehav Rev. 2006;30(6):730-48 PMID: 16919333
  29. High-resolution intersubject averaging and a coordinate system for the cortical surface.
    Hum Brain Mapp. 1999;8(4):272-84 PMID: 10619420
  30. Retrogenesis: clinical, physiologic, and pathologic mechanisms in brain aging, Alzheimer's and other dementing processes.
    Eur Arch Psychiatry Clin Neurosci. 1999;249 Suppl 3:28-36 PMID: 10654097
  31. Within-subject template estimation for unbiased longitudinal image analysis.
    Neuroimage. 2012 Jul 16;61(4):1402-18 PMID: 22430496
  32. Superficial white matter as a novel substrate of age-related cognitive decline.
    Neurobiol Aging. 2015 Jun;36(6):2094-106 PMID: 25834938
  33. Age-related degeneration of corpus callosum in the 90+ years measured with stereology.
    Neurobiol Aging. 2012 May;33(5):1009.e1-9 PMID: 22118947
  34. Age-related changes in brain T1 are correlated with iron concentration.
    Magn Reson Med. 1998 Nov;40(5):749-53 PMID: 9797159
  35. Hippocampal degeneration is associated with temporal and limbic gray matter/white matter tissue contrast in Alzheimer's disease.
    Neuroimage. 2011 Feb 1;54(3):1795-802 PMID: 20965261
  36. One-year brain atrophy evident in healthy aging.
    J Neurosci. 2009 Dec 2;29(48):15223-31 PMID: 19955375
  37. Distribution of axon diameters in cortical white matter: an electron-microscopic study on three human brains and a macaque.
    Biol Cybern. 2014 Oct;108(5):541-57 PMID: 25142940
  38. The effects of changing water content, relaxation times, and tissue contrast on tissue segmentation and measures of cortical anatomy in MR images.
    Magn Reson Imaging. 2013 Dec;31(10):1709-30 PMID: 24055410
  39. Loss of intracortical myelinated fibers: a distinctive age-related alteration in the human striate area.
    Acta Neuropathol. 1983;61(3-4):178-82 PMID: 6650131
  40. The minimal preprocessing pipelines for the Human Connectome Project.
    Neuroimage. 2013 Oct 15;80:105-24 PMID: 23668970
  41. Memory training impacts short-term changes in aging white matter: a longitudinal diffusion tensor imaging study.
    Hum Brain Mapp. 2012 Oct;33(10):2390-406 PMID: 21823209
  42. Demyelination increases radial diffusivity in corpus callosum of mouse brain.
    Neuroimage. 2005 May 15;26(1):132-40 PMID: 15862213
  43. Genetic and environmental influences of white and gray matter signal contrast: a new phenotype for imaging genetics?
    Neuroimage. 2012 Apr 15;60(3):1686-95 PMID: 22500923
  44. Cortical surface-based analysis. I. Segmentation and surface reconstruction.
    Neuroimage. 1999 Feb;9(2):179-94 PMID: 9931268
  45. In vivo identification of human cortical areas using high-resolution MRI: an approach to cerebral structure-function correlation.
    Proc Natl Acad Sci U S A. 2003 Mar 4;100(5):2981-6 PMID: 12601170
  46. Long-chain omega-3 fatty acids improve brain function and structure in older adults.
    Cereb Cortex. 2014 Nov;24(11):3059-68 PMID: 23796946
  47. Gray & white matter tissue contrast differentiates Mild Cognitive Impairment converters from non-converters.
    Brain Imaging Behav. 2015 Jun;9(2):141-8 PMID: 24493370
  48. Degenerative age changes in white matter connectivity visualized in vivo using magnetic resonance imaging.
    Cereb Cortex. 2002 Jul;12(7):767-71 PMID: 12050088
  49. High-resolution MRI reflects myeloarchitecture and cytoarchitecture of human cerebral cortex.
    Hum Brain Mapp. 2005 Mar;24(3):206-15 PMID: 15543596
  50. Mapping an intrinsic MR property of gray matter in auditory cortex of living humans: a possible marker for primary cortex and hemispheric differences.
    Neuroimage. 2006 Oct 1;32(4):1524-37 PMID: 16806989
  51. Association between white matter microstructure, executive functions, and processing speed in older adults: the impact of vascular health.
    Hum Brain Mapp. 2013 Jan;34(1):77-95 PMID: 21954054
  52. Neuroplasticity failure in Alzheimer's disease: bridging the gap between plaques and tangles.
    Neuron. 1999 Nov;24(3):521-9 PMID: 10595506
  53. Marked loss of myelinated nerve fibers in the human brain with age.
    J Comp Neurol. 2003 Jul 21;462(2):144-52 PMID: 12794739
  54. 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
  55. Smoothing and cluster thresholding for cortical surface-based group analysis of fMRI data.
    Neuroimage. 2006 Dec;33(4):1093-103 PMID: 17011792
  56. Widespread age-related differences in the human brain microstructure revealed by quantitative magnetic resonance imaging.
    Neurobiol Aging. 2014 Aug;35(8):1862-72 PMID: 24656835
  57. Myelination, oligodendrocytes, and serious mental illness.
    Glia. 2014 Nov;62(11):1856-77 PMID: 25056210
  58. 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
  59. T1 and T2 relaxation time estimates in the normal human brain.
    Radiology. 1991 Nov;181(2):537-43 PMID: 1924801
  60. Diameter, length, speed, and conduction delay of callosal axons in macaque monkeys and humans: comparing data from histology and magnetic resonance imaging diffusion tractography.
    J Neurosci. 2013 Sep 4;33(36):14501-11 PMID: 24005301
  61. Validating cluster size inference: random field and permutation methods.
    Neuroimage. 2003 Dec;20(4):2343-56 PMID: 14683734
  62. Automatically parcellating the human cerebral cortex.
    Cereb Cortex. 2004 Jan;14(1):11-22 PMID: 14654453
  63. Regional specificity of MRI contrast parameter changes in normal ageing revealed by voxel-based quantification (VBQ).
    Neuroimage. 2011 Apr 15;55(4):1423-34 PMID: 21277375
  64. Associations between regional cortical thickness and attentional networks as measured by the attention network test.
    Cereb Cortex. 2011 Feb;21(2):345-56 PMID: 20525771
  65. Accurate and robust brain image alignment using boundary-based registration.
    Neuroimage. 2009 Oct 15;48(1):63-72 PMID: 19573611
  66. The effects of normal aging on myelin and nerve fibers: a review.
    J Neurocytol. 2002 Sep-Nov;31(8-9):581-93 PMID: 14501200
  67. The effects of normal aging on myelinated nerve fibers in monkey central nervous system.
    Front Neuroanat. 2009 Jul 06;3:11 PMID: 19636385
  68. Establishing norms for age-related changes in proton T1 of human brain tissue in vivo.
    Magn Reson Imaging. 1997;15(10):1133-43 PMID: 9408134
  69. 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
  70. A web-portal for interactive data exploration, visualization, and hypothesis testing.
    Front Neuroinform. 2014 Mar 26;8:25 PMID: 24723882
  71. Accelerating cortical thinning: unique to dementia or universal in aging?
    Cereb Cortex. 2014 Apr;24(4):919-34 PMID: 23236213
  72. Cholesterol of myelin is the determinant of gray-white contrast in MRI of brain.
    Magn Reson Med. 1991 Aug;20(2):285-91 PMID: 1775053
  73. Calculating and reporting effect sizes to facilitate cumulative science: a practical primer for t-tests and ANOVAs.
    Front Psychol. 2013 Nov 26;4:863 PMID: 24324449
  74. Mapping the human cortical surface by combining quantitative T(1) with retinotopy.
    Cereb Cortex. 2013 Sep;23(9):2261-8 PMID: 22826609
  75. Brain changes in older adults at very low risk for Alzheimer's disease.
    J Neurosci. 2013 May 8;33(19):8237-42 PMID: 23658162
  76. Age-related changes in frontal and temporal lobe volumes in men: a magnetic resonance imaging study.
    Arch Gen Psychiatry. 2001 May;58(5):461-5 PMID: 11343525
  77. Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain.
    Neuron. 2002 Jan 31;33(3):341-55 PMID: 11832223
  78. Differential longitudinal changes in cortical thickness, surface area and volume across the adult life span: regions of accelerating and decelerating change.
    J Neurosci. 2014 Jun 18;34(25):8488-98 PMID: 24948804
  79. Association of change in brain structure to objectively measured physical activity and sedentary behavior in older adults: Age, Gene/Environment Susceptibility-Reykjavik Study.
    Behav Brain Res. 2016 Jan 1;296:118-124 PMID: 26363425
  80. Superficial white matter: effects of age, sex, and hemisphere.
    Brain Connect. 2013;3(2):146-59 PMID: 23461767
  81. Disrupted myelin and axon loss in the anterior commissure of the aged rhesus monkey.
    J Comp Neurol. 2003 Nov 3;466(1):14-30 PMID: 14515238
  82. Que PASA? The posterior-anterior shift in aging.
    Cereb Cortex. 2008 May;18(5):1201-9 PMID: 17925295
  83. Sequence-independent segmentation of magnetic resonance images.
    Neuroimage. 2004;23 Suppl 1:S69-84 PMID: 15501102
  84. Structural maturation of neural pathways in children and adolescents: in vivo study.
    Science. 1999 Mar 19;283(5409):1908-11 PMID: 10082463
  85. Improved prediction of Alzheimer's disease with longitudinal white matter/gray matter contrast changes.
    Hum Brain Mapp. 2013 Nov;34(11):2775-85 PMID: 22674625
  86. Disruption of large-scale brain systems in advanced aging.
    Neuron. 2007 Dec 6;56(5):924-35 PMID: 18054866
  87. Cortical surface-based analysis. II: Inflation, flattening, and a surface-based coordinate system.
    Neuroimage. 1999 Feb;9(2):195-207 PMID: 9931269
Article Info
Journal
Human brain mapping
Abbr.
Hum Brain Mapp
ISSN
1097-0193
DOI
10.1002/hbm.23267
Published
2016-00-00
Epub
2016-00-26
Pages
3669-84
Language
English
Region
United States
NLM ID
9419065
PMCID
PMC6867532
Subset
IM
External Links
PubMed source DOI: 10.1002/hbm.23267 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2