Characterizing aging in the human brainstem using quantitative multimodal MRI analysis

Frontiers in Human Neuroscience

Volumn , Issue AUG, 2013, Pages

  Lambert, Christian ^a,b   Chowdhury, Rumana ^b   FitzGerald, Thomas H B ^b   Fleming, Stephen M ^c,d   Lutti, Antoine ^b,e   Hutton, Chloe ^b   Draganski, Bogdan ^e   Frackowiak, Richard ^e   Ashburner, John ^b  

^a ST GEORGE'S UNIVERSITY OF LONDON   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c NEW YORK UNIVERSITY   (United States)

^d UNIVERSITY OF OXFORD   (United Kingdom)

^e LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

Author keywords

Aging; Brainstem; Quantitative MRI; Tensor based morphometry; Voxel based quantification

Indexed keywords

ADULT; AGE; AGED; AGING; ANATOMICAL VARIATION; ARTICLE; BRAIN FUNCTION; BRAIN REGION; BRAIN STEM; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN EXPERIMENT; IMAGE ANALYSIS; IN VIVO STUDY; MAGNETIZATION TRANSFER; MALE; MORPHOMETRICS; NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE IMAGING; OUTCOME ASSESSMENT; PHYSICAL PARAMETERS; PROTON DENSITY; QUANTITATIVE ANALYSIS; SUBSTANTIA NIGRA; SUPERIOR CEREBELLAR PEDUNCLE; TENSOR BASED MORPHOMETRY; VOLUMETRY; VOXEL BASED QUANTIFICATION;

EID: 84884696631     PISSN: 16625161     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnhum.2013.00462     Document Type: Article

References (79)

1. Aanerud, J., Borghammer, P., Chakravarty, M. M., Vang, K., Rodell, A. B., Jónsdottir, K. Y., et al. (2012). Brain energy metabolism and blood flow differences in healthy aging. J. Cereb. Blood Flow Metab. 32, 1177-1187. doi:10.1038/jcbfm.2012.18
2. Alalade, E., Denny, K., Potter, G., Stef-fens, D., and Wang, L. (2011). Altered cerebellar-cerebral functional connectivity in geriatric depression. PLoS ONE 6:e20035. doi:10.1371/ journal.pone.0020035
3. Alvarez, J. C., Díaz, C., Suárez, C., Fernández, J. A., González del Rey, C., Navarro, A., et al. (2000). Aging and the human vestibular nuclei: morphometric analysis. Mech. Ageing Dev. 114, 149-172. doi:10.1016/S0047-6374(00)00098-1
4. Andersen, B. B., Gundersen, H. J., and Pakkenberg, B. (2003). Aging of the human cerebellum: a stereological study. J. Comp. Neurol. 466,356-365. doi:10.1002/cne.10884
5. Armstrong, C. L., Traipe, E., Hunter, J. V., Haselgrove, J. C., Ledakis, G. E., Tallent, E. M., et al. (2004). Age-related, regional, hemispheric, and medial-lateral differences in myelin integrity in vivo in the normal adult brain. AJNR Am. J. Neuroradiol. 25, 977-984.
6. Ashburner, J., and Friston, K. J. (2000). Voxel-based morphometry - the methods. Neuroimage 11, 805-821. doi:10.1006/nimg.2000.0582
7. Ashburner, J., and Friston, K. J. (2001).Why voxel-based morphom-etry should be used. Neuroimage 14, 1238-1243. doi:10.1006/nimg.2001. 0961
8. Ashburner, J., and Friston, K. J. (2005). Unified segmentation. Neu-roimage 26, 839-851. doi:10.1016/j. neuroimage.2005.02.018
9. Ashburner, J., and Friston, K. J. (2011). Diffeomorphic registration using geodesic shooting and Gauss-Newton optimisation. Neuroim-age 55, 954-967. doi:10.1016/j. neuroimage.2010.12.049
10. Baloh, R. W., Jacobson, K. M., and Socotch, T. M. (1993). The effect of aging on visual-vestibuloocular responses. Exp. Brain Res. 95, 509-516. doi:10.1007/BF00227144
11. Barry, R. L., Martyn Klassen, L., Williams, J. M., and Menon, R. S. (2008). Hybrid two-dimensional navigator correction: a new technique to suppress respiratory-induced physiological noise in multi-shot echo-planar functional MRI. Neuroimage 39, 1142-1150. doi:10.1016/j.neuroimage.2007.09. 060
12. Bilgic, B., Pfefferbaum, A., Rohlfing, T., Sullivan, E. V., and Adalsteinsson, E. (2012). MRI estimates of brain iron concentration in normal aging using quantitative susceptibility mapping. Neuroimage 59, 2625-2635. doi:10. 1016/j.neuroimage.2011.08.077
13. Chiueh, C. C. (2001). Iron overload, oxidative stress, and axonal dystrophy in brain disorders. Pediatr. Neu-rol. 25, 138-147. doi:10.1016/S0887-8994(01)00266-1
14. Chowdhury, R., Guitart-Masip, M., Lambert, C., Dolan, R. J., and Düzel, E. (2013). Structural integrity of the substantia nigraand subthalamic nucleus predicts flexibility of instrumental learning in older-age individuals. Neurobiol. Aging 34, 2261-2270. doi:10.1016/j.neurobiolaging. 2013.03.030
15. Collier, T. J., Lipton, J., Daley, B. F., Palfi, S., Chu, Y., Sortwell, C., et al. (2007). Aging-related changes in the nigros-triatal dopamine system and the response to MPTP in nonhuman primates: diminished compensatory mechanisms as a prelude to parkinsonism. Neurobiol. Dis. 26, 56-65. doi:10.1016/j.nbd.2006.11. 013
16. Dick, F., Tierney, A. T., Lutti, A., Josephs, O., Sereno, M. I., and Weiskopf, N. (2012). In vivo functional and mye-loarchitectonic mapping of human primary auditory areas. J. Neu-rosci. 32, 16095-16105. doi:10.1523/ JNEUROSCI.1712-12.2012
17. Dousset, V., Grossman, R. I., Ramer, K. N., Schnall, M. D., Young, L. H., Gonzalez-Scarano, F., et al. (1992). Experimental allergic encephalomyelitis and multiple sclerosis: lesion characterization with magnetization transfer imaging. Radiology 182, 483-491.
18. Draganski, B., Ashburner, J., Hutton, C., Kherif, F., Frackowiak, R. S., Helms, G., et al. (2011). Regional specificity of MRI contrast parameter changes in normal ageing revealed by voxel-based quantification (VBQ). Neu-roimage 55,1423-1434. doi:10.1016/ j.neuroimage.2011.01.052
19. FitzGerald, T. H., Friston, K. J., and Dolan, R. J. (2012). Action-specific value signals in reward-related regions of the human brain. J. Neurosci. 32, 16417-16423. doi:10. 1523/JNEUROSCI.3254-12.2012
20. Gelman, N., Ewing, J. R., Gorell, J. M., Spickler, E. M., and Solomon, E. G. (2001). Interregional variation of longitudinal relaxation rates in human brain at 3.0 T: relation to estimated iron and water contents. Magn. Reson. Med. 45, 71-79. doi:10.1002/1522-2594(200101)45: 1<71::AID-MRM1011>3.0.CO;2-2
21. Glover, G. H., Li, T. Q., and Ress, D. (2000). Image-based method for retrospective correction of physiological motion effects in fMRI: RETROICOR. Magn. Reson. Med. 44, 162-167. doi:10.1002/1522-2594(200007)44: 1<162::AID-MRM23>3.3.CO;2-5
22. Graham, S. J., Stanisz, G. J., Kecojevic, A., Bronskill, M. J., and Henkelman, R. M. (1999). Analysis of changes in MR properties of tissues after heat treatment. Magn. Reson. Med. 42, 1061-1071. doi:10.1002/(SICI) 1522-2594(199912)42:6<1061::AID-MRM10>3.0.CO;2-T
23. Griswold, M. A., Jakob, P. M., Hei-demann, R. M., Nittka, M., Jellus, V., Wang, J., et al. (2002). Generalized autocalibrating partially parallel acquisitions (GRAPPA). Magn Reson. Med. 47, 1202-1210. doi:10. 1002/mrm.10171
24. Haacke, E. M., Miao, Y., Liu, M., Habib, C. A., Katkuri, Y., Liu, T. et al. (2010). Correlation of putative iron content as representedby changes in R2*and phase with age in deep gray matter of healthy adults. J. Magn. Reson. Imaging 32, 561-576. doi:10.1002/jmri. 22293
25. Haroian, A. J., Massopust, L. C., and Young, P. A. (1981). Cerebellothal- amic projections in the rat: an autoradiographic and degenera tion study. J. Comp. Neurol. 197, 217-236. doi:10.1002/cne.901970205
26. Hawkes, C. H., Del Tredici, K., and Braak, H. (2010). A timeline for Parkinson's disease. Parkinsonism Relat. Disord. 16, 79-84. doi:10. 1016/j.parkreldis.2009.08.007
27. Helms, G., Dathe, H., and Dechent, P. (2008a). Quantitative FLASH MRI at 3T using a rational approximation of the Ernst equation. Magn. Reson. Med. 59, 667-672. doi:10. 1002/mrm.21542
28. Helms, G., Dathe, H., Kallenberg, K., and Dechent, P. (2008b). High-resolution maps of magnetization transfer with inherent correction for RFinhomogeneity andT1relaxation obtained from 3D FLASH MRI. Magn. Reson. Med. 60, 1396-1407. doi:10.1002/mrm.21732
29. Henkelman, R. M., Huang, X., Xiang, Q. S., Stanisz, G. J., Swanson, S. D., and Bronskill, M. J. (1993). Quantitative interpretation of magnetization transfer. Magn. Reson. Med. 29, 759-766. doi:10.1002/ mrm.1910290607
30. Hu, X., and Kim, S. G. (1994). Reduction of physiological noise in functional MRI using navigator echo. Magn. Reson. Med. 31, 495-503. doi: 10.1002/mrm.1910310505
31. Hut, R. A., and Van der Zee, E. A. (2011). The cholinergic system, cir-cadian rhythmicity, and time memory. Behav. Brain Res. 221, 466-480. doi:10.1016/j.bbr.2010.11.039
32. Hutton, C., Josephs, O., Stadler, J., Feath-erstone, E., Reid, A., Speck, O., et al. (2011). The impact of physiological noise correctiononfMRIat7T. Neu-roimage 57, 101-112. doi:10.1016/j. neuroimage.2011.04.018
33. Jernigan, T. L., Archibald, S. L., Fennema-Notestine, C., Gamst, A. C., Stout, J. C., Bonner, J., et al. (2001). Effects of age on tissues and regions of the cerebrum and cerebellum. Neurobiol. Aging 22, 581-594. doi:10.1016/ S0197-4580(01)00217-2
34. Koenig, S. H. (1995). Classes of hydra-tion sites at protein-water interfaces: the source of contrast in magnetic resonance imaging. Biophys. J. 69, 593-603. doi:10.1016/S0006-3495(95)79933-7
35. Kucharczyk, W., Macdonald, P. M., Stanisz, G. J., and Henkelman, R. M. (1994). Relaxivity and magnetization transfer of white matter lipids at MR imaging: importance of cere-brosides and pH. Radiology 192, 521-529.
36. Lambert, C., Lutti, A., Helms, G., Frack-owiak, R., and Ashburner, J. (2013). Multiparametricbrainstem segmentation using a modified multivari-ate mixture of Gaussians. Neuroim-age (Amst.) 2, 684-694. doi:10.1016/ j.nicl.2013.04.017
37. Lambert, C., Zrinzo, L., Nagy, Z., Lutti, A., Hariz, M., Foltynie, T., et al. (2012). Confirmation of functional zones within the human subthal-amic nucleus: patterns of connectivity and sub-parcellation using diffusion weighted imaging. Neu-roimage 60, 83-94. doi:10.1016/j. neuroimage.2011.11.082
38. Lee, N. J., Park, I. S., Koh, I., Jung, T. W., and Rhyu, I. J. (2009). No volume difference of medulla oblongata between young and old Korean people. Brain Res. 1276, 77-82. doi:10. 1016/j.brainres.2009.04.027
39. Lewa, C. J., and Majewska, Z. (1980). Temperature relationships of proton spin-lattice relaxation time T1 in biological tissues. Bull. Cancer 67, 525-530.
40. Liepinsh, E., and Otting, G. (1996). Proton exchange rates from amino acid side chains - implications for image contrast. Magn. Reson. Med. 35, 30-42. doi:10.1002/mrm. 1910350106
41. Luft, A. R., Skalej, M., Schulz, J. B., Welte, D., Kolb, R., Bürk, K., et al. (1999). Patterns of age-related shrinkage in cerebellum and brain-stem observed in vivo using three-dimensional MRI volumetry. Cereb. Cortex 9, 712-721. doi:10.1093/ cercor/9.7.712
42. Lutti, A., Hutton, C., Finsterbusch, J., Helms, G., and Weiskopf, N. (2010). Optimization and validation of methods for mapping of the radiofrequency transmit field at 3T. Magn. Reson. Med. 64, 229-238. doi:10.1002/mrm.22421
43. Lutti, A., Stadler, J., Josephs, O., Windis-chberger, C., Speck, O., Bernard-ing, J., et al. (2012). Robust and fast whole brain mapping of the RF transmit field B1 at 7T. PLoS ONE 7:e32379. doi:10.1371/journal.pone. 0032379
44. McCormack, A. L., Di Monte, D. A., Delfani, K., Irwin, I., DeLanney, L. E., Langston, W. J., et al. (2004). Aging of the nigrostriatal system in the squirrel monkey. J. Comp. Neu-rol. 471, 387-395. doi:10.1002/cne. 20036
45. Mooradian, A. D. (1988). Effect of aging on the blood-brain barrier. Neuro-biol. Aging 9, 31-39. doi:10.1016/ S0197-4580(88)80013-7
46. Naidich, T. P., and Duvernoy, H. M. (2009). Duvernoy's Atlas of the Human Brain Stem and Cerebellum: High-Field MRI: Surface Anatomy, Internal Structure, Vascularization and 3D Sectional Anatomy, Illustrated Ed. Wien,NewYork: Springer.
47. Ozawa, H., Nishida, A., Mito, T., and Takashima, S. (1994). Development of ferritin-containing cells in the pons and cerebellum of the human brain. Brain Dev. 16, 92-95. doi:10. 1016/0387-7604(94)90041-8
48. Papanikolaou, G., and Pantopoulos, K. (2005). Iron metabolism and toxicity. Toxicol. Appl. Pharmacol. 202, 199-211. doi:10.1016/j.taap. 2004.06.021
49. Pfefferbaum, A., Adalsteinsson, E., Rohlfing, T., and Sullivan, E. V. (2009). MRI estimates of brain iron concentration in normal aging: comparison of field-dependent (FDRI) and phase (SWI) methods. Neuroimage 47, 493-500. doi:10.1016/j
50. Pfefferbaum, A., Adalsteinsson, E., Rohlfing, T., and Sullivan, E. V. (2010). Diffusion tensor imaging of deep gray matter brain structures: effects of age and iron concentration. Neurobiol. Aging 31, 482-493. doi:10.1016/j.neurobiolaging.2008. 04.013
51. Raz, N. (1996). "Neuroanatomy of the aging brain observed in vivo," in Neuroimaging II: Clinical Applications, ed. E. D. Bigler (New York: Plenum Press), 153-182.
52. Raz, N., Gunning-Dixon, F., Head, D., Williamson, A., and Acker, J. D. (2001). Age and sex differences in the cerebellum and the ventral pons: a prospective MR study of healthy adults. AJNR Am. J. Neuroradiol. 22, 1161-1167.
53. Rooney, W. D., Johnson, G., Li, X., Cohen, E. R., Kim, S. G., Ugur-bil, K., et al. (2007). Magnetic field and tissue dependencies of human brain longitudinal 1H2O relaxation in vivo. Magn. Reson. Med. 57, 308-318. doi:10.1002/mrm.21122
54. Samuels, E. R., and Szabadi, E. (2008). Functional neuroanatomy of the noradrenergic locus coeruleus: its roles in the regulation of arousal and autonomic function part II: physiological and pharmacological manipulations and pathological alterations of locus coeruleus activity in humans. Curr. Neu-ropharmacol. 6, 254. doi:10.2174/ 157015908785777193
55. Sereno, M. I., Lutti, A., Weiskopf, N., and Dick, F. (2013). Mapping the human cortical surface by combining quantitative T1 with retinotopy. Cereb. Cortex 23, 2261-2268. doi:10. 1093/cercor/bhs213
56. Sherwood, C. C., Hof, P. R., Holloway, R. L., Semendeferi, K., Gannon, P. J., Frahm, H. D., et al. (2005). Evolution of the brainstem orofacial motor systeminprimates:acompar-ative study of trigeminal, facial, and hypoglossal nuclei. J. Hum. Evol. 48, 45-84. doi:10.1016/j.jhevol.2004.10. 003
57. Shmueli, K., Dodd, S. J., Li, T. Q., and Duyn, J.H. (2011). The contribution of chemical exchange to MRI frequency shifts in brain tissue. Magn. Reson. Med. 65, 35-43. doi:10.1002/ mrm.22604
58. Simic, G., Stanic, G., Mladinov, M., Jovanov-Milosevic, N., Kostovic, I., and Hof, P. R. (2009). Does Alzheimer's disease begin in the brainstem? Neuropathol. Appl. Neurobiol. 35, 532-554. doi:10. 1111/j.1365-2990.2009.01038.x
59. Stanisz, G. J., Odrobina, E. E., Pun, J., Escaravage, M., Graham, S. J., Bronskill, M. J., et al. (2005). T1, T2 relaxation and magnetization transfer in tissue at 3T. Magn. Reson. Med. 54, 507-512. doi:10. 1002/mrm.20605
60. Sullivan, E. V., Rosenbloom, M., Ser-venti, K. L., and Pfefferbaum, A. (2004). Effects of age and sex on volumes of the thala-mus, pons, and cortex. Neurobiol. Aging 25, 185-192. doi:10.1016/ S0197-4580(03)00044-7
61. Taniwaki, T., Okayama, A., Yoshiura, T., Togao, O., Nakamura, Y., Yamasaki, T., et al. (2007). Age-related alterations of the functional interactions within the basal ganglia and cere-bellar motor loops in vivo. Neu-roimage 36,1263-1276. doi:10.1016/ j.neuroimage.2007.04.027
62. Thambisetty, M., Wan, J., Carass, A., An, Y., Prince, J. L., and Resnick, S. M. (2010). Longitudinal changes in cortical thickness associated with normal aging. Neuroim-age 52, 1215-1223. doi:10.1016/j. neuroimage.2010.04.258
63. Tofts, P. (2003). Quantitative MRI of the Brain: Measuring Changes Caused by Disease. London: John Wiley & Sons Inc.
64. Tsopelas, C., Stewart, R., Savva, G. M., Brayne, C., Ince, P., Thomas, A., et al. (2011). Neuropatholog-ical correlates of late-life depression in older people. Br. J. Psychiatry 198, 109-114. doi:10.1192/bjp. bp.110.078816
65. Vaillancourt, D. E., Spraker, M. B., Pro-doehl, J., Zhou, X. J., and Little, D. M. (2012). Effects of aging on the ventral and dorsal substantia nigra using diffusion tensor imaging. Neu-robiol. Aging 33, 35-42. doi:10.1016/ j.neurobiolaging.2010.02.006
66. Van Gelderen, P., De Zwart, J. A., Starewicz, P., Hinks, R. S., and Duyn, J. H. (2007). Real-time shimming to compensate for respiration-induced B0 fluctuations. Magn. Reson. Med. 57, 362-368. doi:10. 1002/mrm.21136
67. van Zijl, P. C., Zhou, J., Mori, N., Payen, J. F., Wilson, D., and Mori, S. (2003). Mechanism of magnetization transfer during on-resonance water saturation. A new approach to detect mobile proteins, peptides, and lipids. Magn. Reson. Med. 49, 440-449. doi: 10.1002/mrm.10398
68. Vita, G., Princi, P., Calabro, R., Toscano, A., Manna, L., and Messina, C. (1986). Cardiovascular reflex tests: assessment of age-adjusted normal range. J. Neurol. Sci. 75, 263-274. doi:10.1016/0022-510X(86)90074-2
69. Vul, E., Harris, C., Winkielman, P., and Pashler, H. (2009). Puzzlingly high correlations in fMRI studies of emotion, personality, and social cognition. Perspect. Psychol. Sci. 4, 274-290. doi:10.1111/j.1745-6924.2009.01132.x
70. Walhovd, K. B., Fjell, A. M., Rein-vang, I., Lundervold, A., Dale, A. M., Eilertsen, D. E., et al. (2005). Effects of age on volumes of cortex, white matter and subcortical structures. Neurobiol. Aging 26, 1261-1270. doi:10.1016/j. neurobiolaging.2005.05.020
71. Walhovd, K. B., Westlye, L. T., Amlien, I., Espeseth, T., Reinvang, I., Raz, N., et al. (2011). Consistent neuroanatom-ical age-related volume differences across multiple samples. Neurobiol. Aging 32, 916-932. doi:10.1016/j. neurobiolaging.2009.05.013
72. Weiskopf, N., Lutti, A., Helms, G., Novak, M., Ashburner, J., and Hut-ton, C. (2011). Unified segmentation based correction of R1 brain maps for RF transmit field inho-mogeneities (UNICORT). Neuroim-age 54, 2116-2124. doi:10.1016/j. neuroimage.2010.10.023
73. Wharton, S., and Bowtell, R. (2012). Fiber orientation-dependent white matter contrast in gradient echo MRI. Proc. Natl. Acad. Sci. U.S.A. 109, doi:10.1073/pnas.1211075109
74. Woodruff-Pak, D. S., Foy, M. R., Akopian, G. G., Lee, K. H., Zach, J., Nguyen, K. P., et al. (2010). Differential effects and rates of normal aging in cerebellum and hippocampus. Proc. Natl. Acad. Sci. U.S.A. 107, 1624-1629. doi:10.1073/pnas. 0914207107
75. Yao, B., Li, T.Q., Gelderen, P.V., Shmueli, K., de Zwart, J. A., and Duyn, J. H. (2009). Susceptibility contrast in high field MRI of human brain as a function of tissue iron content. Neu-roimage 44,1259-1266. doi:10.1016/ j.neuroimage.2008.10.029
76. Zaitsev, M., Dold, C., Sakas, G., Hennig, J., and Speck, O. (2006). Magnetic resonance imaging of freely moving objects: prospective real-time motion correction using an external optical motion tracking system. Neuroimage 31, 1038-1050. doi:10. 1016/j.neuroimage.2006.01.039
77. Zauner, A., and Muizelaar, J. P. (1997). "Chapter 5: brain metabolism and cerebral blood flow," in Head Injury: Pathophysiology and Management of Severe Closed Injury,eds P. Reilly and R. Bullock (London: Chapman and Hall), 89-99.
78. Zecca, L., Gallorini, M., Schünemann, V., Trautwein, A. X., Gerlach, M., Riederer, P., et al. (2001). Iron, neuromelanin and ferritin content in the substantia nigra of normal subjects at different ages: consequences for iron storage and neurodegenerative processes. J. Neu-rochem. 76, 1766-1773. doi:10.1046/ j.1471-4159.2001.00186.x
79. Zecca, L., Youdim, M. B., Riederer, P., Connor, J. R., and Crichton, R. R. (2004). Iron, brain ageing and neu-rodegenerative disorders. Nat. Rev. Neurosci. 5, 863-873. doi:10.1038/ nrn1537