Cited by 458Advanced Neuroimaging Techniques and ApplicationsCognitive Abilities and TestingFunctional Brain Connectivity Studies

Assessing the effects of age on long white matter tracts using diffusion tensor tractography

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Davis, Simon W., Dennis, Nancy A., Buchler, Norbou G., White, Leonard E., Madden, David J., Cabeza, Roberto·2009·NeuroImage

Abstract

Aging is associated with significant white matter deterioration and this deterioration is assumed to be at least partly a consequence of myelin degeneration. The present study investigated specific predictions of the myelodegeneration hypothesis using diffusion tensor tractography. This technique has several advantages over other methods of assessing white matter architecture, including the possibility of isolating individual white matter tracts and measuring effects along the whole extent of each tract. The study yielded three main findings. First, age-related white matter deficits increased gradually from posterior to anterior segments within specific fiber tracts traversing frontal and parietal, but not temporal cortex. This pattern inverts the sequence of myelination during childhood and early development observed in previous studies and lends support to a "last-in-first-out" theory of the white matter health across the lifespan. Second, both the effects of aging on white matter and their impact on cognitive performance were stronger for radial diffusivity (RD) than for axial diffusivity (AD). Given that RD has previously been shown to be more sensitive to myelin integrity than AD, this second finding is also consistent with the myelodegeneration hypothesis. Finally, the effects of aging on select white matter tracts were associated with age difference in specific cognitive functions. Specifically, FA in anterior tracts was shown to be primarily associated with executive tasks and FA in posterior tracts mainly associated with visual memory tasks. Furthermore, these correlations were mirrored in RD, but not AD, suggesting that RD is more sensitive to age-related changes in cognition. Taken together, the results help to clarify how age-related white matter decline impairs cognitive performance.

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Crossref · 10.1016/j.neuroimage.2009.01.068

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  • Across brain systems, prefrontal association tracts are the most vulnerable to aging, while cingulum, temporal and parietal-occipital commissural connections are relatively preserved.

    “revealing a typical spatial degeneration pattern across brain systems in which prefrontal association tracts are the most vulnerable to aging, while cingulum, temporal and parietal-occipital commissural connections are relatively preserved.”

    From Quantitative mapping of the brain’s structural connectivity using diffusion MRI tractography: A review (2022) · cites this paper as Davis et al., 2009

    The Discussion (Anterior-Posterior Gradient; page unavailable) ranks age-related FA differences highest in the genu and uncinate fasciculus and lowest in the cingulum bundle and splenium, supporting greater vulnerability of anterior tracts and relative preservation of some connections. But the same section reports appreciable effects in the inferior longitudinal fasciculus, including a stronger effect in its occipito-temporal segment; the Results (Anterior-posterior trend analysis; page unavailable) also find age effects in the cingulum. The claim overstates preservation across the named connections. (LLM, conf=0.88)

    Experimental — accuracy not yet measured
  • Bilingualism is linked to better preservation of white matter structures in normal aging.

    “This evidence suggests that bilingualism is associated with better maintenance of white matter structures in the course of normal aging [113].”

    From Bilingualism: consequences for mind and brain (2012) · cites this paper as [113]

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Research works printed but not linked: 83

  1. Ashburner J Friston KJ 2000 Voxel-based morphometry--the methods Neuroimage 11 805 821 10860804
  2. Bartzokis G 2004 Age-related myelin breakdown: a developmental model of cognitive decline and Alzheimer’s disease Neurobiol Aging 25 5 18 author reply 49–62 14675724
  3. Basser PJ Pajevic S Pierpaoli C Duda J Aldroubi A 2000 In vivo fiber tractography using DT-MRI data Magn Reson Med 44 625 632 11025519
  4. Beaulieu C Allen PS 1994 Determinants of anisotropic water diffusion in nerves Magn Reson Med 31 394 400 8208115
  5. Bhagat YA Beaulieu C 2004 Diffusion anisotropy in subcortical white matter and cortical gray matter: changes with aging and the role of CSF-suppression J Magn Reson Imaging 20 216 227 15269946
  6. Bucur B Madden DJ Spaniol J Provenzale JM Cabeza R White LE Huettel SA 2007 Age-related slowing of memory retrieval: Contributions of perceptual speed and cerebral white matter integrity Neurobiol Aging PMC2396513 17383774
  7. Burgel U Amunts K Hoemke L Mohlberg H Gilsbach JM Zilles K 2006 White matter fiber tracts of the human brain: three-dimensional mapping at microscopic resolution, topography and intersubject variability Neuroimage 29 1092 1105 16236527
  8. Catani M Howard RJ Pajevic S Jones DK 2002 Virtual in vivo interactive dissection of white matter fasciculi in the human brain Neuroimage 17 77 94 12482069
  9. Concha L Gross DW Wheatley BM Beaulieu C 2006 Diffusion tensor imaging of time-dependent axonal and myelin degradation after corpus callosotomy in epilepsy patients Neuroimage 32 1090 1099 16765064
  10. Corouge I Fletcher PT Joshi S Gouttard S Gerig G 2006 Fiber tract-oriented statistics for quantitative diffusion tensor MRI analysis Med Image Anal 10 786 798 16926104
  11. Daselaar SM Browndyke J Cabeza R Cabeza R Kingstone A 2006 Functional neuroimaging of cognitive aging Handbook of Functional Neuroimaging of Cognition 2 MIT Press
  12. Daselaar SM Cabeza R Cabeza R Nyberg L Park DC 2005 Age-related Changes in Hemispheric Organization Cognitive Neuroscience of Aging Oxford Oxford University Press
  13. Dubois J Dehaene-Lambertz G Perrin M Mangin JF Cointepas Y Duchesnay E Le Bihan D Hertz-Pannier L 2008 Asynchrony of the early maturation of white matter bundles in healthy infants: quantitative landmarks revealed noninvasively by diffusion tensor imaging Hum Brain Mapp 29 14 27 17318834 PMC6870818
  14. Duvernoy H 1999 The Human Brain, Surface, Blood Supply, and Three-Dimensional Sectional Anatomy Vienna Springer-Verlag
  15. Ebeling U von Cramon D 1992 Topography of the uncinate fascicle and adjacent temporal fiber tracts Acta Neurochir 115 143 148 1605083
  16. Feldman ML Peters A 1998 Ballooning of myelin sheaths in normally aged macaques J Neurocytol 27 605 614 10405027
  17. Gao W Lin W Chen Y Gerig G Smith JK Jewells V Gilmore JH 2008 Temporal and Spatial Development of Axonal Maturation and Myelination of White Matter in the Developing Brain AJNR Am J Neuroradiol PMC2640448 19001533
  18. Geula C Wu CK Saroff D Lorenzo A Yuan M Yankner BA 1998 Aging renders the brain vulnerable to amyloid beta-protein neurotoxicity Nat Med 4 827 831 9662375
  19. Giedd JN Blumenthal J Jeffries NO Castellanos FX Liu H Zijdenbos A Paus T Evans AC Rapoport JL 1999 Brain development during childhood and adolescence: a longitudinal MRI study Nat Neurosci 2 861 863 10491603
  20. Glenn OA Henry RG Berman JI Chang PC Miller SP Vigneron DB Barkovich AJ 2003 DTI-based three-dimensional tractography detects differences in the pyramidal tracts of infants and children with congenital hemiparesis J Magn Reson Imaging 18 641 648 14635148
  21. Glisky EL Rubin SR Davidson PS 2001 Source memory in older adults: an encoding or retrieval problem? J Exp Psychol Learn Mem Cogn 27 1131 1146 11550742
  22. Goodlett CB Fletcher PT Gilmore JH Gerig G 2008 Group analysis of DTI fiber tract statistics with application to neurodevelopment Neuroimage PMC2727755 19059345
  23. Gould RL Brown RG Owen AM ffytche DH Howard RJ 2003 fMRI BOLD response to increasing task difficulty during successful paired associates learning Neuroimage 20 1006 1019 14568470
  24. Grady CL McIntosh AR Horwitz B Maisog JM Ungerleider LG Mentis MJ Pietrini P Schapiro MB Haxby JV 1995 Age-related reductions in human recognition memory due to impaired encoding Science 269 218 221 7618082
  25. Grieve SM Williams LM Paul RH Clark CR Gordon E 2007 Cognitive aging, executive function, and fractional anisotropy: a diffusion tensor MR imaging study AJNR Am J Neuroradiol 28 226 235 17296985 PMC7977408
  26. Gutchess AH Welsh RC Hedden T Bangert A Minear M Liu LL Park DC 2005 Aging and the neural correlates of successful picture encoding: frontal activations compensate for decreased medial-temporal activity J Cogn Neurosci 17 84 96 15701241
  27. Hayakawa K Konishi Y Kuriyama M Konishi K Matsuda T 1991 Normal brain maturation in MRI Eur J Radiol 12 208 215 1855514
  28. Head D Buckner RL Shimony JS Williams LE Akbudak E Conturo TE McAvoy M Morris JC Snyder AZ 2004 Differential vulnerability of anterior white matter in nondemented aging with minimal acceleration in dementia of the Alzheimer type: evidence from diffusion tensor imaging Cereb Cortex 14 410 423 15028645
  29. Husain J Juurlink BH 1995 Oligodendroglial precursor cell susceptibility to hypoxia is related to poor ability to cope with reactive oxygen species Brain Res 698 86 94 8581507
  30. Jensen JH Helpern JA Ramani A Lu H Kaczynski K 2005 Diffusional kurtosis imaging: the quantification of non-gaussian water diffusion by means of magnetic resonance imaging Magn Reson Med 53 1432 1440 15906300
  31. Kennedy KM Erickson KI Rodrigue KM Voss MW Colcombe SJ Kramer AF Acker JD Raz N 2008 Age-related differences in regional brain volumes: A comparison of optimized voxel-based morphometry to manual volumetry Neurobiol Aging PMC2756236 18276037
  32. Kier EL Staib LH Davis LM Bronen RA 2004 MR imaging of the temporal stem: anatomic dissection tractography of the uncinate fasciculus, inferior occipitofrontal fasciculus, and Meyer’s loop of the optic radiation AJNR Am J Neuroradiol 25 677 691 15140705 PMC7974480
  33. Kinney HC Brody BA Kloman AS Gilles FH 1988 Sequence of central nervous system myelination in human infancy. II. Patterns of myelination in autopsied infants J Neuropathol Exp Neurol 47 217 234 3367155
  34. Lamantia AS Rakic P 1990 Cytological and quantitative characteristics of four cerebral commissures in the rhesus monkey J Comp Neurol 291 520 537 2329189
  35. Madden DJ Spaniol J Bucur B Whiting WL 2007 Age-related increase in top-down activation of visual features Q J Exp Psychol (Colchester) 60 644 651 17455072 PMC1857303
  36. Madden DJ Spaniol J Costello MC Bucur B White LE Cabeza R Davis SW Dennis NA Provenzale JM Huettel SA in press Cerebral White Matter Integrity Mediates Adult Age Differences in Cognitive Performance J Cogn Neurosci PMC2676336 18564054
  37. Madden DJ Spaniol J Whiting WL Bucur B Provenzale JM Cabeza R White LE Huettel SA 2006 Adult age differences in the functional neuroanatomy of visual attention: A combined fMRI and DTI study Neurobiol Aging PMC1995072 16500004
  38. Madden DJ Turkington TG Provenzale JM Denny LL Langley LK Hawk TC Coleman RE 2002 Aging and attentional guidance during visual search: functional neuroanatomy by positron emission tomography Psychol Aging 17 24 43 11931285 PMC1831840
  39. Madden DJ Whiting WL Huettel SA White LE MacFall JR Provenzale JM 2004 Diffusion tensor imaging of adult age differences in cerebral white matter: relation to response time Neuroimage 21 1174 1181 15006684
  40. Markowitsch HJ 1995 Which brain regions are critically involved in the retrieval of old episodic memory? Brain Res Brain Res Rev 21 117 127 8866670
  41. Meier-Ruge W Ulrich J Bruhlmann M Meier E 1992 Age-related white matter atrophy in the human brain Ann N Y Acad Sci 673 260 269 1485724
  42. Mori S van Zijl PC 2002 Fiber tracking: principles and strategies - a technical review NMR Biomed 15 468 480 12489096
  43. O’Donnell L Westin CF 2006 High-dimensional white matter atlas generation and group analysis Med Image Comput Comput Assist Interv Int Conf Med Image Comput Comput Assist Interv 9 243 251 17354778
  44. O’Sullivan M Jones DK Summers PE Morris RG Williams SC Markus HS 2001 Evidence for cortical “disconnection” as a mechanism of age-related cognitive decline Neurology 57 632 638 11524471
  45. Owen AM Morris RG Sahakian BJ Polkey CE Robbins TW 1996 Double dissociations of memory and executive functions in working memory tasks following frontal lobe excisions, temporal lobe excisions or amygdalo-hippocampectomy in man Brain 119 Pt 5 1597 1615 8931583
  46. Persson J Nyberg L Lind J Larsson A Nilsson LG Ingvar M Buckner RL 2006 Structure-function correlates of cognitive decline in aging Cereb Cortex 16 907 915 16162855
  47. Peters A Moss MB Sethares C 2000 Effects of aging on myelinated nerve fibers in monkey primary visual cortex J Comp Neurol 419 364 376 10723011
  48. Peters A Sethares C 2002 Aging and the myelinated fibers in prefrontal cortex and corpus callosum of the monkey J Comp Neurol 442 277 291 11774342
  49. Pfefferbaum A Adalsteinsson E Sullivan EV 2005 Frontal circuitry degradation marks healthy adult aging: Evidence from diffusion tensor imaging Neuroimage 26 891 899 15955499
  50. Price G Cercignani M Parker GJ Altmann DR Barnes TR Barker GJ Joyce EM Ron MA 2008 White matter tracts in first-episode psychosis: a DTI tractography study of the uncinate fasciculus Neuroimage 39 949 955 17988894 PMC2387199
  51. Rabbitt P Lowe C 2000 Patterns of cognitive ageing Psychol Res 63 308 316 11004884
  52. Raz N Cabeza R Nyberg L Park DC 2005 The Aging Brain Observed in Vivo: Differential Changes and Their Modifiers Cognitive Neuroscience of Aging 19 57 Oxford University Press
  53. Raz N Gunning FM Head D Dupuis JH McQuain J Briggs SD Loken WJ Thornton AE Acker JD 1997 Selective aging of the human cerebral cortex observed in vivo: differential vulnerability of the prefrontal gray matter Cereb Cortex 7 268 282 9143446
  54. Raz N Lindenberger U Rodrigue KM Kennedy KM Head D Williamson A Dahle C Gerstorf D Acker JD 2005 Regional brain changes in aging healthy adults: general trends, individual differences and modifiers Cereb Cortex 15 1676 1689 15703252
  55. Robbins TW James M Owen AM Sahakian BJ Lawrence AD McInnes L Rabbitt PM 1998 A study of performance on tests from the CANTAB battery sensitive to frontal lobe dysfunction in a large sample of normal volunteers: implications for theories of executive functioning and cognitive aging. Cambridge Neuropsychological Test Automated Battery J Int Neuropsychol Soc 4 474 490 9745237
  56. Ronen I Ugurbil K Kim D 2005 How Does DWI Correlate With White Matter Structures? MAGNETIC RESONANCE IN MEDICINE 54 317 16032693
  57. Sakuma H Nomura Y Takeda K Tagami T Nakagawa T Tamagawa Y Ishii Y Tsukamoto T 1991 Adult and neonatal human brain: diffusional anisotropy and myelination with diffusion-weighted MR imaging Radiology 180 229 233 2052700
  58. Salat DH Kaye JA Janowsky JS 1999 Prefrontal gray and white matter volumes in healthy aging and Alzheimer disease Arch Neurol 56 338 344 10190825
  59. Salat DH Tuch DS Hevelone ND Fischl B Corkin S Rosas HD Dale AM 2005 Age-related changes in prefrontal white matter measured by diffusion tensor imaging Ann N Y Acad Sci 1064 37 49 16394146
  60. Scahill RI Frost C Jenkins R Whitwell JL Rossor MN Fox NC 2003 A longitudinal study of brain volume changes in normal aging using serial registered magnetic resonance imaging Arch Neurol 60 989 994 12873856
  61. Schmierer K Scaravilli F Altmann DR Barker GJ Miller DH 2004 Magnetization transfer ratio and myelin in postmortem multiple sclerosis brain Ann Neurol 56 407 415 15349868
  62. Smith SM Jenkinson M Johansen-Berg H Rueckert D Nichols TE Mackay CE Watkins KE Ciccarelli O Cader MZ Matthews PM Behrens TE 2006 Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data Neuroimage 31 1487 1505 16624579
  63. Smith SM Zhang Y Jenkinson M Chen J Matthews PM Federico A De Stefano N 2002 Accurate, robust, and automated longitudinal and cross-sectional brain change analysis Neuroimage 17 479 489 12482100
  64. Snook L Paulson LA Roy D Phillips L Beaulieu C 2005 Diffusion tensor imaging of neurodevelopment in children and young adults Neuroimage 26 1164 1173 15961051
  65. Song SK Sun SW Ju WK Lin SJ Cross AH Neufeld AH 2003 Diffusion tensor imaging detects and differentiates axon and myelin degeneration in mouse optic nerve after retinal ischemia Neuroimage 20 1714 1722 14642481
  66. Song SK Yoshino J Le TQ Lin SJ Sun SW Cross AH Armstrong RC 2005 Demyelination increases radial diffusivity in corpus callosum of mouse brain Neuroimage 26 132 140 15862213
  67. Sowell ER Thompson PM Leonard CM Welcome SE Kan E Toga AW 2004 Longitudinal mapping of cortical thickness and brain growth in normal children J Neurosci 24 8223 8231 15385605 PMC6729679
  68. Sowell ER Trauner DA Gamst A Jernigan TL 2002 Development of cortical and subcortical brain structures in childhood and adolescence: a structural MRI study Dev Med Child Neurol 44 4 16 11811649
  69. Sullivan EV Adalsteinsson E Hedehus M Ju C Moseley M Lim KO Pfefferbaum A 2001 Equivalent disruption of regional white matter microstructure in ageing healthy men and women Neuroreport 12 99 104 11201100
  70. Sullivan EV Adalsteinsson E Pfefferbaum A 2006 Selective age-related degradation of anterior callosal fiber bundles quantified in vivo with fiber tracking Cereb Cortex 16 1030 1039 16207932
  71. Sullivan EV Pfefferbaum A 2006 Diffusion tensor imaging and aging Neurosci Biobehav Rev 30 749 761 16887187
  72. Sullivan EV Rohlfing T Pfefferbaum A 2008 Quantitative fiber tracking of lateral and interhemispheric white matter systems in normal aging: Relations to timed performance Neurobiol Aging PMC2815144 18495300
  73. Sun SW Liang HF Schmidt RE Cross AH Song SK 2007 Selective vulnerability of cerebral white matter in a murine model of multiple sclerosis detected using diffusion tensor imaging Neurobiol Dis 28 30 38 17683944 PMC2905808
  74. Tang Y Nyengaard JR 1997 A stereological method for estimating the total length and size of myelin fibers in human brain white matter J Neurosci Methods 73 193 200 9196291
  75. Trip SA Wheeler-Kingshott C Jones SJ Li WY Barker GJ Thompson AJ Plant GT Miller DH 2006 Optic nerve diffusion tensor imaging in optic neuritis Neuroimage 30 498 505 16242968
  76. Vernooij MW de Groot M van der Lugt A Ikram MA Krestin GP Hofman A Niessen WJ Breteler MM 2008 White matter atrophy and lesion formation explain the loss of structural integrity of white matter in aging Neuroimage 43 470 477 18755279
  77. Vogt BA Finch DM Olson CR 1992 Functional heterogeneity in cingulate cortex: the anterior executive and posterior evaluative regions Cereb Cortex 2 435 443 1477524
  78. Wakana S Caprihan A Panzenboeck MM Fallon JH Perry M Gollub RL Hua K Zhang J Jiang H Dubey P Blitz A van Zijl P Mori S 2007 Reproducibility of quantitative tractography methods applied to cerebral white matter Neuroimage 36 630 644 17481925 PMC2350213
  79. Wakana S Jiang H Nagae-Poetscher LM van Zijl PC Mori S 2004 Fiber tract-based atlas of human white matter anatomy Radiology 230 77 87 14645885
  80. West RL 1996 An application of prefrontal cortex function theory to cognitive aging Psychol Bull 120 272 292 8831298
  81. Wozniak JR Lim KO 2006 Advances in white matter imaging: a review of in vivo magnetic resonance methodologies and their applicability to the study of development and aging Neurosci Biobehav Rev 30 762 774 16890990 PMC2895765
  82. Xu D Mori S Solaiyappan M van Zijl PC Davatzikos C 2002 A framework for callosal fiber distribution analysis Neuroimage 17 1131 1143 12414255
  83. Yasmin H Nakata Y Aoki S Abe O Sato N Nemoto K Arima K Furuta N Uno M Hirai S Masutani Y Ohtomo K 2008 Diffusion abnormalities of the uncinate fasciculus in Alzheimer’s disease: diffusion tensor tract-specific analysis using a new method to measure the core of the tract Neuroradiology 18246334

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Authors
Davis, S. W., Dennis, N. A., Buchler, N. G., White, L. E., Madden, D. J., & Cabeza, R.
Affiliations
  • Duke University (US)
  • Duke Medical Center (US)
Corresponding author
Davis, Simon W.
Venue
NeuroImage
Publisher
Elsevier BV
Published
2009-06
Volume
46
Issue
2
Pages
530-541
ISSN
1053-8119 (ISSN-L)
OpenAlex
W1977845408
Cited by
458
References
13
Citations by year
2026: 5 · 2025: 15 · 2024: 20 · 2023: 28 · 2022: 25 · 2021: 38 · 2020: 22 · 2019: 35 · 2018: 33 · 2017: 27 · 2016: 29 · 2015: 27 · 2014: 24 · 2013: 30 · 2012: 25
FWCI
25.19
Type
journal article
Language
en
Open access
Locations
  • NeuroImage (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • National Institutes of Health (AG011622, AG19731)
  • National Institute on Aging (T32 AG000029)
Topics
  • Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced Neuroimaging Techniques and Applications
  • Social Sciences › Psychology › Experimental and Cognitive Psychology › Cognitive Abilities and Testing
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
Keywords
brain aging, myelin integrity, radial diffusivity, axial diffusivity, fractional anisotropy, cognitive aging, executive function, visual memory, myelination, diffusion tensor tractography
MeSH terms
Adult, Aged, Aging, Brain, Female, Humans, Male, Middle Aged, Nerve Fibers, Myelinated, Diffusion Magnetic Resonance Imaging

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