Widespread age-related differences in the human brain microstructure revealed by quantitative magnetic resonance imaging

Neurobiology of Aging

Volumn 35, Issue 8, 2014, Pages 1862-1872

  Callaghan, Martina F ^a   Freund, Patrick ^a,b   Draganski, Bogdan ^c   Anderson, Elaine ^a   Cappelletti, Marinella ^d,e   Chowdhury, Rumana ^a   Diedrichsen, Joern ^d   FitzGerald, Thomas H B ^a   Smittenaar, Peter ^a   Helms, Gunther ^f   Lutti, Antoine ^c   Weiskopf, Nikolaus ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^c LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

^e UNIVERSITY OF LONDON   (United Kingdom)

^f UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

3T; Aging; Magnetization transfer; MT; Quantitative; R1; R2*; Relaxation; T1; T2*; VBQ; Water content

Indexed keywords

BIOLOGICAL MARKER; IRON;

ADULT; AGE DISTRIBUTION; AGED; AGING; ARTICLE; BASAL GANGLION; BRAIN CORTEX; BRAIN REGION; COHORT ANALYSIS; CORPUS CALLOSUM; CROSS-SECTIONAL STUDY; DEMYELINATION; FEMALE; HUMAN; HUMAN EXPERIMENT; HUMAN TISSUE; IMAGE ANALYSIS; IN VIVO STUDY; MALE; MYELINATION; NERVE DEGENERATION; NEUROBIOLOGY; NEUROIMAGING; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RED NUCLEUS; SUPERIOR OCCIPITOFRONTAL FASCICLE; VOLUNTEER; VOXEL BASED MORPHOMETRY; WHITE MATTER; BRAIN; IRON METABOLISM DISORDER; METABOLISM; MIDDLE AGED; NEUROAXONAL DYSTROPHY; PATHOLOGY; PROCEDURES; YOUNG ADULT;

ADULT; AGED; AGING; BRAIN; FEMALE; HUMANS; IRON; IRON METABOLISM DISORDERS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; NEUROAXONAL DYSTROPHIES; NEUROIMAGING; YOUNG ADULT;

EID: 84899898647     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2014.02.008     Document Type: Article

References (72)

1. Adinolfi A.M., Yamuy J., Morales F.R., Chase M.H. Segmental demyelination in peripheral nerves of old cats. Neurobiol. Aging 1991, 12:175-179.
2. Ashburner J. Afast diffeomorphic image registration algorithm. Neuroimage 2007, 38:95-113.
3. Ashburner J., Friston K.J. Unified segmentation. Neuroimage 2005, 26:839-851.
4. Aston-Jones G., Rogers J., Shaver R.D., Dinan T.G., Moss D.E. Age-impaired impulse flow from nucleus basalis to cortex. Nature 1985, 318:462-464.
5. Barkhof F., Calabresi P.A., Miller D.H., Reingold S.C. Imaging outcomes for neuroprotection and repair in multiple sclerosis trials. Nat. Rev. Neurol. 2009, 5:256-266.
6. Bartzokis G. Age-related myelin breakdown: a developmental model of cognitive decline and Alzheimer's disease. Neurobiol. Aging 2004, 25:5-18.
7. Bartzokis G. Alzheimer's disease as homeostatic responses to age-related myelin breakdown. Neurobiol. Aging 2011, 32:1341-1371.
8. Bartzokis G., Lu P.H., Heydari P., Couvrette A., Lee G.J., Kalashyan G., Freeman F., Grinstead J.W., Villablanca P., Finn J.P., Mintz J., Alger J.R., Altshuler L.L. Multimodal magnetic resonance imaging assessment of white matter aging trajectories over the lifespan of healthy individuals. Biol Psychiatry 2012, 72:1026-1034.
9. Bartzokis G., Tishler T.A., Lu P.H., Villablanca P., Altshuler L.L., Carter M., Huang D., Edwards N., Mintz J. Brain ferritin iron may influence age- and gender-related risks of neurodegeneration. Neurobiol. Aging 2007, 28:414-423.
10. Beard J.L., Connor J.R., Jones B.C. Iron in the Brain. Nutr. Rev. 2009, 51:157-170.
11. Bender B., Klose U. The invivo influence of white matter fiber orientation towards B(0) on T2** in the human brain. NMR Biomed. 2010, 23:1071-1076.
12. Benedict R.H.B., Zivadinov R. Risk factors for and management of cognitive dysfunction in multiple sclerosis. Nat. Rev. Neurol. 2011, 7:332-342.
13. Connor J.R., Menzies S.L. Relationship of iron to oligodendrocytes and myelination. Glia 1996, 17:83-93.
14. Connor J.R., Menzies S.L., St Martin S.M., Mufson E.J. Cellular distribution of transferrin, ferritin, and iron in normal and aged human brains. J.Neurosci. Res. 1990, 27:595-611.
15. Daugherty A.M., Raz N. Age-related differences in iron content of subcortical nuclei observed invivo: a meta-analysis. Neuroimage 2012, 70:113-121.
16. Deoni S.C.L., Peters T.M., Rutt B.K. High-resolution T1 and T2* mapping of the brain in a clinically acceptable time with DESPOT1 and DESPOT2*. Magn. Reson. Med. 2005, 53:237-241.
17. Dexter D.T., Carayon A., Javoy-Agid F., Agid Y., Wells F.R., Daniel S.E., Lees A.J., Jenner P., Marsden C.D. Alterations in the levels of iron, ferritin and other trace metals in Parkinson's disease and other neurodegenerative diseases affecting the basal ganglia. Brain 1991, 114(Pt 4):1953-1975.
18. Dick F., Tierney A.T., Lutti A., Josephs O., Sereno M.I., Weiskopf N. Invivo functional and myeloarchitectonic mapping of human primary auditory areas. J.Neurosci. 2012, 32:16095-16105.
19. Draganski B., Ashburner J., Hutton C., Kherif F., Frackowiak R.S.J., Helms G., Weiskopf N. Regional specificity of MRI contrast parameter changes in normal ageing revealed by voxel-based quantification (VBQ). Neuroimage 2011, 55:1423-1434.
20. Fjell A.M., Westlye L.T., Grydeland H., Amlien I., Espeseth T., Reinvang I., Raz N., Dale A.M., Walhovd K.B. Accelerating Cortical Thinning: Unique to Dementia or Universal in Aging?. Cereb. Cortex 2014, 24:919-934.
21. Flechsig P. Developmental (myelogenetic) localisation of the cerebral cortex in the human subject. Lancet 1901, 1898:1027-1029.
22. Fotuhi M., Hachinski V., Whitehouse P.J. Changing perspectives regarding late-life dementia. Nat. Rev. Neurol. 2009, 5:649-658.
23. Freund P., Weiskopf N., Ashburner J., Wolf K., Sutter R., Altmann D.R., Friston K.J., Thompson A., Curt A. MRI investigation of the sensorimotor cortex and the corticospinal tract after acute spinal cord injury: a prospective longitudinal study. Lancet Neurol. 2013, 4422:1-9.
24. Freund P., Weiskopf N., Ward N.S., Hutton Chloe, Gall A., Ciccarelli O., Craggs M., Friston K.J., Thompson A.J. Disability, atrophy and cortical reorganization following spinal cord injury. Brain 2011, 134:1610-1622.
25. Frisoni G.B., Fox N.C., Jack C.R., Scheltens P., Thompson P.M. The clinical use of structural MRI in Alzheimer disease. Nat. Rev. Neurol. 2010, 6:67-77.
26. Gerber M.R., Connor J.R. Do oligodendrocytes mediate iron regulation in the human brain?. Ann. Neurol. 1989, 26:95-98.
27. Gorell J.M., Ordidge R.J., Brown G.G., Deniau J.-C., Buderer N.M., Helpern J.A. Increased iron-related MRI contrast in the substantia nigra in Parkinson's disease. Neurology 1995, 45:1138-1143.
28. Hallgren B., Sourander P. The effect of age on the non-haemin iron in the human brain. J.Neurochem. 1958, 3:41-51.
29. Head D. 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 2004, 14:410-423.
30. Helms G., Dathe H., Dechent P. Quantitative FLASH MRI at 3T using a rational approximation of the Ernst equation. Magn. Reson. Med. 2008, 59:667-672.
31. Helms G., Dathe H., Dechent P. Modeling the influence of TR and excitation flip angle on the magnetization transfer ratio (MTR) in human brain obtained from 3D spoiled gradient echo MRI. Magn. Reson. Med. 2010, 64:177-185.
32. Helms G., Dathe H., Kallenberg K., Dechent P. High-resolution maps of magnetization transfer with inherent correction for RF inhomogeneity and T1 relaxation obtained from 3D FLASH MRI. Magn. Reson. Med. 2008, 60:1396-1407.
33. Helms G., Dechent P. Increased SNR and reduced distortions by averaging multiple gradient echo signals in 3D FLASH imaging of the human brain at 3T. J.Magn. Reson. Imaging 2009, 29:198-204.
34. House M.J., St Pierre T.G., Kowdley K.V., Montine T., Connor J.R., Beard John, Berger J., Siddaiah N., Shankland E., Jin L.-W. Correlation of proton transverse relaxation rates (R2) with iron concentrations in postmortem brain tissue from Alzheimer's disease patients. Magn. Reson. Med. 2007, 57:172-180.
35. Jellinger K., Paulus W. Brain iron and ferritin in Parkinson's and Alzheimer's diseases. J.Neural. Transm. 1990, 2:327-340.
36. Kemper T.L. Neuroanatomical and neuropathological changes during aging and dementia. Clinical Neurology of Aging 1994, 3-67. Oxford University Press, New York. M. Albert, J. Knoefel (Eds.).
37. Khalil M., Langkammer C., Ropele S., Petrovic K., Wallner-Blazek M., Loitfelder M., Jehna M., Bachmaier G., Schmidt R., Enzinger C., Fuchs S., Fazekas F. Determinants of brain iron in multiple sclerosis: a quantitative 3T MRI study. Neurology 2011, 77:1691-1697.
38. Klein A., Andersson J., Ardekani B.A., Ashburner J., Avants B., Chiang M.-C., Christensen G.E., Collins D.L., Gee J., Hellier P., Song J.H., Jenkinson M., Lepage C., Rueckert D., Thompson P., Vercauteren T., Woods R.P., Mann J.J., Parsey R.V. Evaluation of 14 nonlinear deformation algorithms applied to human brain MRI registration. Neuroimage 2009, 46:786-802.
39. Koenig S.H., Brown R.D., Spiller M., Lundbom N. Relaxometry of brain: why white matter appears bright in MRI. Magn. Reson. Med. 1990, 14:482-495.
40. Langkammer C., Krebs N., Goessler W., Scheurer E., Ebner F., Yen K., Fazekas Franz, Ropele Stefan Quantitative MR imaging of brain iron: a postmortem validation study. Radiology 2010, 257:455-462.
41. LeVine S.M., Macklin W.B. Iron-enriched oligodendrocytes: a reexamination of their spatial distribution. J.Neurosci. Res. 1990, 26:508-512.
42. Lutti A., Hutton Chloe, Finsterbusch J., Helms G., Weiskopf N. Optimization and validation of methods for mapping of the radiofrequency transmit field at 3T. Magn. Reson. Med. 2010, 64:229-238.
43. Lutti A., Stadler J., Josephs O., Windischberger C., Speck O., Bernarding J., Hutton Chloe, Weiskopf N. Robust and fast whole brain mapping of the RF transmit field B1 at 7T. PLoS One 2012, 7:e32379.
44. Maldjian J.A., Laurienti P.J., Kraft R.A., Burdette J.H. An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 2003, 19:1233-1239.
45. Marner L., Nyengaard J.R., Tang Y., Pakkenberg B. Marked loss of myelinated nerve fibers in the human brain with age. J.Comp. Neurol. 2003, 462:144-152.
46. McDonald C.R., McEvoy L.K., Gharapetian L., Fennema-Notestine C., Hagler D.J., Holland D., Koyama A., Brewer J.B., Dale A.M. Regional rates of neocortical atrophy from normal aging to early Alzheimer disease. Neurology 2009, 73:457-465.
47. Morris C.M., Candy J.M., Oakley A.E., Bloxham C.A., Edwardson J.A. Histochemical distribution of non-haem iron in the human brain. Acta Anat. (Basel) 1992, 144:235-257.
48. Noseworthy J.H. Progress in determining the causes and treatment of multiple sclerosis. Nature 1999, 399:A40-A47.
49. Ordidge R.J., Gorell J.M., Deniau J.C., Knight R.A., Helpern J.A. Assessment of relative brain iron concentrations using T2*-weighted and T2**-weighted MRI at 3 Tesla. Magn. Reson. Med 1994, 32:335-341.
50. Péran P., Hagberg G., Luccichenti G., Cherubini A., Brainovich V., Celsis P., Caltagirone C., Sabatini U. Voxel-based analysis of R2* maps in the healthy human brain. J.Magn. Reson. Imaging 2007, 26:1413-1420.
51. Peters A. The effects of normal aging on myelin and nerve fibers: a review. J.Neurocytol. 2002, 31:581-593.
52. Preibisch C., Deichmann R. Influence of RF spoiling on the stability and accuracy of T1 mapping based on spoiled FLASH with varying flip angles. Magn. Reson. Med. 2009, 61:125-135.
53. Raz, N., 2000. Aging of the brain and its impact on cognitive performance: integration of structural and functional finding, in: Craik, F.I.M., Salthouse, T.A. (Eds.), Handbook of Aging and Cognition II. pp. 1-90.
54. Rodrigue K.M., Daugherty A.M., Haacke E.M., Raz N. The role of hippocampal iron concentration and hippocampal volume in age-related differences in memory. Cereb. Cortex 2013, 23:1533-1541.
55. Scahill R.I., Fox N.C. Longitudinal imaging in dementia. Br. J. Radiol. 2007, 80(Spec No):S92-S98.
56. Scahill R.I., Schott J.M., Stevens J.M., Rossor M.N., Fox N.C. 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, 99:4703-4707.
57. Schmierer K., Scaravilli F., Altmann D.R., Barker G.J., Miller D.H. Magnetization transfer ratio and myelin in postmortem multiple sclerosis brain. Ann. Neurol. 2004, 56:407-415.
58. Schmierer K., Tozer D.J., Scaravilli F., Altmann D.R., Barker G.J., Tofts P.S., Miller D.H. Quantitative magnetization transfer imaging in postmortem multiple sclerosis brain. J.Magn. Reson. Imaging 2007, 26:41-51.
59. Sereno M.I., Lutti A., Weiskopf N., Dick F. Mapping the human cortical surface by combining quantitative T(1) with retinotopy. Cereb. Cortex 2013, 23:2261-2268.
60. Terao S., Sobue G., Hashizume Y., Shimada N., Mitsuma T. Age-related changes of the myelinated fibers in the human corticospinal tract: a quantitative analysis. Acta Neuropathol. 1994, 88:137-142.
61. Todorich B., Pasquini J.M., Garcia C.I., Paez P.M., Connor J.R. Oligodendrocytes and myelination: the role of iron. Glia 2009, 57:467-478.
62. Tofts P.S. Quantitative MRI of the Brain 2003, John Wiley & Sons, Ltd, Chichester, UK.
63. Tzourio-Mazoyer N., Landeau B., Papathanassiou D., Crivello F., Etard O., Delcroix N., Mazoyer B., Joliot M. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 2002, 15:273-289.
64. Vymazal J., Brooks R.A., Baumgarner C., Tran V., Katz D., Bulte J.W., Bauminger R., Di Chiro G. The relation between brain iron and NMR relaxation times: an invitro study. Magn. Reson. Med. 1996, 35:56-61.
65. Weiskopf N., Lutti A., Helms G., Novak M., Ashburner J., Hutton Chloe Unified segmentation based correction of R1 brain maps for RF transmit field inhomogeneities (UNICORT). Neuroimage 2011, 54:2116-2124.
66. Weiskopf N., Suckling J., Williams G., Correia M.M., Inkster B., Tait R., Ooi C., Bullmore E.T., Lutti A. Quantitative multi-parameter mapping of R1, PD*, MT, and R2* at 3T: a multi-center validation. Front Neurosci. 2013, 7:1-11.
67. Westlye L.T., Walhovd K.B., Dale A.M., Bjørnerud A., Due-Tønnessen P., Engvig A., Grydeland H., Tamnes C.K., Ostby Y., Fjell A.M. Life-span changes of the human brain white matter: diffusion tensor imaging (DTI) and volumetry. Cereb. Cortex 2010, 20:2055-2068.
68. Wharton S., Bowtell R. Fiber orientation-dependent white matter contrast in gradient echo MRI. Proc. Natl. Acad. Sci. U.S.A 2012, 109:18559-18564.
69. Wharton S., Bowtell R. Gradient echo based fiber orientation mapping using R2* and frequency difference measurements. Neuroimage 2013, 83:1011-1023.
70. Wolff S.D., Balaban R.S. Magnetization transfer contrast (MTC) and tissue water proton relaxation invivo. Magn. Reson. Med. 1989, 10:135-144.
71. Zecca L., Youdim M.B.H., Riederer P., Connor J.R., Crichton R.R. Iron, brain ageing and neurodegenerative disorders. Nat. Rev. Neurosci. 2004, 5:863-873.
72. Ziegler G., Dahnke R., Gaser C. Models of the aging brain structure and individual decline. Front. Neuroinform. 2012, 6:3.