The effect of lifelong bilingualism on regional grey and white matter volume

Brain Research

Volumn 1612, Issue , 2015, Pages 128-139

  Olsen, Rosanna K ^a   Pangelinan, Melissa M ^a   Bogulski, Cari ^b   Chakravarty, M Mallar ^a,c,d,e   Luk, Gigi ^f   Grady, Cheryl L ^a,g   Bialystok, Ellen ^a,b  

^a ROTMAN RESEARCH INSTITUTE   (Canada)

^b YORK UNIVERSITY   (Canada)

^c DOUGLAS MENTAL HEALTH UNIVERSITY INSTITUTE   (Canada)

^d MCGILL UNIVERSITY   (Canada)

^e MCGILL UNIVERSITY   (Canada)

^f HARVARD GRADUATE SCHOOL OF EDUCATION   (United States)

^g UNIVERSITY OF TORONTO   (Canada)

Author keywords

Aging; Bilingual; Cognitive reserve; Hippocampus; MRI; Volumetric

Indexed keywords

AGED; AGING; ARTICLE; BILINGUALISM; BRAIN SIZE; CEPHALOMETRY; COGNITIVE RESERVE; CONTROLLED STUDY; CORTICAL THICKNESS (BRAIN); ENTORHINAL CORTEX; EXECUTIVE FUNCTION; FEMALE; FRONTAL LOBE; GRAY MATTER; GREY MATTER VOLUME; HIPPOCAMPUS; HUMAN; HUMAN EXPERIMENT; LANGUAGE ABILITY; LANGUAGE PROCESSING; MALE; MEDIAL TEMPORAL LOBE; MINI MENTAL STATE EXAMINATION; MONOLINGUALISM; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; RESPONSE TIME; STROOP TEST; WHITE MATTER; WHITE MATTER VOLUME; AGE; ANALYSIS OF VARIANCE; ANATOMY AND HISTOLOGY; BRAIN CORTEX; IMAGE PROCESSING; MULTILINGUALISM; NEUROPSYCHOLOGICAL TEST; PHYSIOLOGY; PSYCHOLOGY;

AGE FACTORS; AGED; AGING; ANALYSIS OF VARIANCE; CEREBRAL CORTEX; FEMALE; GRAY MATTER; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MULTILINGUALISM; NEUROPSYCHOLOGICAL TESTS; WHITE MATTER;

EID: 84930044916     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2015.02.034     Document Type: Article

References (92)

1. J. Abutalebi, M. Canini, P.A. Della Rosa, L.P. Sheung, D.W. Green, and B.S. Weekes Bilingualism protects anterior temporal lobe integrity in aging Neurobiol. Aging 35 9 2014 2126 2133 10.1016/j.neurobiolaging.2014.03.010
2. J. Abutalebi, P.A. Della Rosa, D.W. Green, M. Hernandez, P. Scifo, R. Keim, and A. Costa Bilingualism tunes the anterior cingulate cortex for conflict monitoring Cereb. Cortex 22 2012 2076 2086 10.1093/cercor/bhr287
3. J. Abutalebi, and D.W. Green Control mechanisms in bilingual language production: neural evidence from language switching studies Lang. Cogn. Process. 23 2008 557 582 10.1080/01690960801920602
4. J.E. Ahlskog, Y.E. Geda, N.R. Graff-Radford, and R.C. Petersen Physical exercise as a preventive or disease-modifying treatment of dementia and brain aging Mayo Clin. Proc. 86 2011 876 884 10.4065/mcp.2011.0252
5. S. Alladi, T.H. Bak, V. Duggirala, B. Surampudi, M. Shailaja, A.K. Shukla, and S. Kaul Bilingualism delays age at onset of dementia, independent of education and immigration status Neurology 81 2013 1938 1944 10.1212/01.wnl.0000436620.33155.a4
6. B.B. Avants, C.L. Epstein, M. Grossman, and J.C. Gee Symmetric diffeomorphic image registration with cross-correlation: evaluating automated labeling of elderly and neurodegenerative brain Med. Image Anal. 12 2008 26 41 10.1016/j.media.2007.06.004
7. E. Bialystok, F.I.M. Craik, M.A. Binns, L. Ossher, and M. Freedman Effects of bilingualism on the age of onset and progression of MCI and AD: evidence from executive function tests Neuropsychology 28 2014 290 304 10.1037/neu0000023
8. E. Bialystok, F.I.M. Craik, and M. Freedman Bilingualism as a protection against the onset of symptoms of dementia Neuropsychologia 45 2007 459 464 10.1016/j.neuropsychologia.2006.10.009
9. E. Bialystok, F.I.M. Craik, D.W. Green, and T.H. Gollan Bilingual minds Psychol. Sci. Public Interest 10 2009 89 129 10.1177/1529100610387084
10. E. Bialystok, F.I.M. Craik, R. Klein, and M. Viswanathan Bilingualism, aging, and cognitive control: evidence from the Simon task Psychol. Aging 19 2004 290 303 10.1037/0882-7974.19.2.290
11. E. Bialystok, F.I.M. Craik, and G. Luk Bilingualism: consequences for mind and brain Trends Cogn. Sci. 16 4 2012 240 250 10.1016/j.tics.2012.03.001
12. E. Bialystok, F.I.M. Craik, and J. Ryan Executive control in a modified antisaccade task: effects of aging and bilingualism J. Exp. Psychol. Learn. Mem. Cogn. 32 2006 1341 1354 10.1037/0278-7393.32.6.1341
13. E. Bialystok, G. Poarch, L. Luo, and F.I.M. Craik Effects of bilingualism and aging on executive function and working memory Psychol. Aging 29 3 2014 696 705
14. M.F. Bonner, and A.R. Price Where is the anterior temporal lobe and what does it do? J. Neurosci. 33 10 2013 4213 4215 10.1523/JNEUROSCI.0041-13.2013
15. A.M. Brickman, M.E. Zimmerman, R.H. Paul, S.M. Grieve, D.F. Tate, R.A. Cohen, and E. Gordon Regional white matter and neuropsychological functioning across the adult lifespan Biol. Psychiatry 60 2006 444 453 10.1016/j.biopsych.2006.01.011
16. V.A. Cardenas, L.L. Chao, C. Studholme, K. Yaffe, B.L. Miller, C. Madison, and M.W. Weiner Brain atrophy associated with baseline and longitudinal measures of cognition Neurobiol. Aging 32 4 2011 572 580 10.1016/j.neurobiolaging.2009.04.011
17. S.J. Colcombe, K.I. Erickson, P.E. Scalf, J.S. Kim, R. Prakash, E. McAuley, and A.F. Kramer Aerobic exercise training increases brain volume in aging humans J. Gerontol. A: Biol. Sci. Med. Sci. 61 2006 1166 1170
18. D.L. Collins, C.J. Holmes, T.M. Peters, and A.C. Evans Automatic 3-D model-based neuroanatomical segmentation Hum. Brain Mapp. 3 1995 190 208 10.1002/hbm.460030304
19. A. Costa, and N. Sebastián-Gallés How does the bilingual experience sculpt the brain? Nat. Rev. Neurosci. 15 2014 336 345 10.1038/nrn3709
20. A.M. Dale, B. Fischl, and M.I. Sereno Cortical surface-based analysis: I. segmentation and surface reconstruction NeuroImage 9 1999 179 194
21. A.M. Dale, and M.I. Sereno Improved localization of cortical activity by combining EEG and MEG with MRI cortical surface reconstruction: a linear approach J. Cogn. Neurosci. 5 2 1993 162 176
22. D.C. Delis, E. Kaplan, and J.H. Kramer Delis-Kaplan Executive Function System (D-KEFS) 2001 Psychological Corporation San Antonio, TX
23. R.S. Desikan, F. Ségonne, B. Fischl, B.T. Quinn, B.C. Dickerson, D. Blacker, and R.J. Killiany An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest NeuroImage 31 3 2006 968 980 10.1016/j.neuroimage.2006.01.021
24. L.R. Dice Measures of the amount of ecologic association between species Ecology 26 1945 297 302
25. A.D. Ekstrom, A.J. Bazih, N.A. Suthana, R. Al-Hakim, K. Ogura, M. Zeineh, and S.Y. Bookheimer Advances in high-resolution imaging and computational unfolding of the human hippocampus NeuroImage 47 1 2009 42 49 10.1016/j.neuroimage.2009.03.017
26. K.I. Erickson, M.W. Voss, R.S. Prakash, C. Basak, A. Szabo, L. Chaddock, and A.F. Kramer Exercise training increases size of hippocampus and improves memory Proc. Natl. Acad. Sci. USA 108 2011 3017 3022 10.1073/pnas.1015950108
27. D. Ferreira, Y. Molina, A. Machado, E. Westman, L.O. Wahlund, A. Nieto, and J. Barroso Cognitive decline is mediated by gray matter changes during middle age Neurobiol. Aging 35 2014 1086 1094 10.1016/j.neurobiolaging.2013.10.095
28. B. Fischl, and A.M. Dale Measuring the thickness of the human cerebral cortex from magnetic resonance images Proc. Natl. Acad. Sci. USA 97 20 2000 11050 11055
29. B. Fischl, A. Liu, and A.M. Dale Automated manifold surgery: constructing geometrically accurate and topologically correct models of the human cerebral cortex IEEE Trans. Med. Imaging 20 1 2001 70 80
30. B. Fischl, D.H. Salat, E. Busa, M. Albert, M. Dieterich, C. Haselgrove, and A.M. Dale Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain Neuron 33 2002 341 355 10.1016/S0896-6273(02)00569-X
31. B. Fischl, D.H. Salat, A.J.W. van der Kouwe, N. Makris, F. Ségonne, B.T. Quinn, and A.M. Dale Sequence-independent segmentation of magnetic resonance images NeuroImage 23 2004 S69 S84 10.1016/j.neuroimage.2004.07.016
32. B. Fischl, M.I. Sereno, and A.M. Dale Cortical surface-based analysis: II: Inflation, flattening, and a surface-based coordinate system NeuroImage 9 2 1999 195 207
33. B. Fischl, M.I. Sereno, R.B.H. Tootell, and A.M. Dale High-resolution intersubject averaging and a coordinate system for the cortical surface Hum. Brain Mapp. 8 4 1999 272 284
34. B. Fischl, A.J.W. van der Kouwe, C. Destrieux, E. Halgren, F. Ségonne, D.H. Salat, and A.M. Dale Automatically parcellating the human cerebral cortex Cereb. Cortex 14 1 2004 11 22 10.1093/cercor/bhg087
35. A.M. Fjell, K.B. Walhovd, C. Fennema-Notestine, L.K. McEvoy, D.J. Hagler, D. Holland, and A.M. Dale One-year brain atrophy evident in healthy aging J. Neurosci. 29 2009 15223 15231 10.1523/JNEUROSCI.3252-09.2009
36. A.M. Fjell, L.T. Westlye, H. Grydeland, I. Amlien, T. Espeseth, I. Reinvang, and K.B. Walhovd Critical ages in the life course of the adult brain: nonlinear subcortical aging Neurobiol. Aging 34 10 2013 2239 2247 10.1016/j.neurobiolaging.2013.04.006
37. M.F. Folstein, S.E. Folstein, and P.R. McHugh "Mini-mental state": a practical method for grading the cognitive state of pateitns for the clinician J. Psychiatr. Res. 12 1975 189 198 10.1016/0022-3956(75)90026-6
38. C. Gaser, and G. Schlaug Brain structures differ between musicians and non-musicians J. Neurosci. 23 2003 9240 9245
39. J.N. Giedd, and J.L. Rapoport Structural MRI of pediatric brain development: what have we learned and where are we going? Neuron 67 5 2010 728 734 10.1016/j.neuron.2010.08.040
40. B.T. Gold, N.F. Johnson, and D.K. Powell Lifelong bilingualism contributes to cognitive reserve against white matter integrity declines in aging Neuropsychologia 51 13 2013 2841 2846 10.1016/j.neuropsychologia.2013.09.037
41. B.T. Gold, C. Kim, N.F. Johnson, R.J. Kryscio, and C.D. Smith Lifelong bilingualism maintains neural efficiency for cognitive control in aging J. Neurosci. 33 2013 387 396 10.1523/JNEUROSCI.3837-12.2013
42. C.L. Grady, G. Luk, F.I.M. Craik, and E. Bialystok Brain network activity in monolingual and bilingual older adults Neuropsychologia 66 2015 170 181 10.1016/j.neuropsychologia.2014.10.042
43. X. Han, J. Jovicich, D. Salat, A.J.W. van der Kouwe, B. Quinn, S. Czanner, and B. Fischl Reliability of MRI-derived measurements of human cerebral cortical thickness: the effects of field strength, scanner upgrade and manufacturer NeuroImage 32 1 2006 180 194 10.1016/j.neuroimage.2006.02.051
44. B. Hanna-Pladdy, and A. MacKay The relation between instrumental musical activity and cognitive aging Neuropsychology 25 3 2011 378 386 10.1037/a0021895
45. C.N. Harada, M.C. Natelson Love, and K.L. Triebel Normal cognitive aging Clin. Geriatr. Med. 29 4 2013 737 752 10.1016/j.cger.2013.07.002
46. D. Head, R.L. Buckner, J.S. Shimony, L.E. Williams, E. Akbudak, T.E. Conturo, and A.Z. Snyder 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 2004 410 423 10.1093/cercor/bhh003
47. C.R. Jack, R.C. Petersen, Y. Xu, P.C. O'Brien, G.E. Smith, R.J. Ivnik, and E. Kokmen Rate of medial temporal lobe atrophy in typical aging and Alzheimer's disease Neurology 51 1998 993 999
48. D.K. Jones, T.R. Knösche, and R. Turner White matter integrity, fiber count, and other fallacies: the do's and don'ts of diffusion MRI NeuroImage 73 2013 239 254 10.1016/j.neuroimage.2012.06.081
49. J. Jovicich, S. Czanner, D. Greve, E. Haley, A.J.W. van der Kouwe, R. Gollub, and A.M. Dale Reliability in multi-site structural MRI studies: effects of gradient non-linearity correction on phantom and human data NeuroImage 30 2 2006 436 443 10.1016/j.neuroimage.2005.09.046
50. K.M. Kennedy, and N. Raz Aging white matter and cognition: differential effects of regional variations in diffusion properties on memory, executive functions, and speed Neuropsychologia 47 2009 916 927 10.1016/j.neuropsychologia.2009.01.001
51. A.F. Kramer, and K.I. Erickson Capitalizing on cortical plasticity: influence of physical activity on cognition and brain function Trends Cogn. Sci. 11 2007 342 348 10.1016/j.tics.2007.06.009
52. J.F. Kroll, and E. Bialystok Understanding the consequences of bilingualism for language processing and cognition J. Cogn. Psychol. 25 2013 497 514 10.1080/20445911.2013.799170 Understanding
53. R.K. Lenroot, N. Gogtay, D.K. Greenstein, E.M. Wells, G.L. Wallace, L.S. Clasen, and J.N. Giedd Sexual dimorphism of brain developmental trajectories during childhood and adolescence NeuroImage 36 4 2007 1065 1073 10.1016/j.neuroimage.2007.03.053
54. R.K. Lenroot, J.E. Schmitt, S.J. Ordaz, G.L. Wallace, M.C. Neale, J.P. Lerch, and J.N. Giedd Differences in genetic and environmental influences on the human cerebral cortex associated with development during childhood and adolescence Hum. Brain Mapp. 30 1 2009 163 174 10.1002/hbm.20494
55. J.P. Lerch, K. Worsley, W.P. Shaw, D.K. Greenstein, R.K. Lenroot, J. Giedd, and A.C. Evans Mapping anatomical correlations across cerebral cortex (MACACC) using cortical thickness from MRI NeuroImage 31 2006 993 1003
56. G. Luk, E. Bialystok, F.I.M. Craik, and C.L. Grady Lifelong bilingualism maintains white matter integrity in older adults J. Neurosci. 31 2011 16808 16813 10.1523/JNEUROSCI.4563-11.2011
57. G. Luk, D.W. Green, J. Abutalebi, and C. Grady Cognitive control for language switching in bilinguals: a quantitative meta-analysis of functional neuroimaging studies Lang. Cogn. Process. 27 2012 1479 1488 10.1080/01690965.2011.613209
58. J. Mårtensson, J. Eriksson, N.C. Bodammer, M. Lindgren, M. Johansson, L. Nyberg, and M. Lövdén Growth of language-related brain areas after foreign language learning NeuroImage 63 1 2012 240 244 10.1016/j.neuroimage.2012.06.043
59. A. Mechelli, J.T. Crinion, U. Noppeney, J. O'Doherty, J. Ashburner, R.S. Frackowiak, and C.J. Price Structural plasticity in the bilingual brain Nature 431 2004 757 10.1038/nature03016
60. E.A. Mueller, M.M. Moore, D.C.R. Kerr, G. Sexton, R.M. Camicioli, D.B. Howieson, and J.A. Kaye Brain volume preserved in healthy elderly through the eleventh decade Neurology 51 1998 1555 1562 10.1212/WNL.51.6.1555
61. L. Nyberg, M. Lövdén, K. Riklund, U. Lindenberger, and L. Bäckman Memory aging and brain maintenance Trends Cogn. Sci. 16 2012 292 305 10.1016/j.tics.2012.04.005
62. H.R. Pardoe, D.F. Abbott, G.D. Jackson The Alzheimer's Disease Neuroimaging Sample size estimates for well-powered cross-sectional cortical thickness studies Hum. Brain Mapp. 34 2013 1 19
63. R.C. Petersen, C.R. Jack, Y.-C. Xu, S.C. Waring, P.C. O'Brien, G.E. Smith, and E. Kokmen Memory and MRI-based hippocampal volumes in aging and AD Neurology 54 2000 581 10.1212/WNL.54.3.581
64. N. Raz, F. Gunning-Dixon, D. Head, K.M. Rodrigue, A. Williamson, and J.D. Acker Aging, sexual dimorphism, and hemispheric asymmetry of the cerebral cortex: replicability of regional differences in volume Neurobiol. Aging 25 3 2004 377 396 10.1016/S0197-4580(03)00118-0
65. N. Raz, U. Lindenberger, K.M. Rodrigue, K.M. Kennedy, D. Head, A. Williamson, and J.D. Acker Regional brain changes in aging healthy adults: general trends, individual differences and modifiers Cereb. Cortex 15 2005 1676 1689 10.1093/cercor/bhi044
66. A. Raznahan, J.P. Lerch, N. Lee, D. Greenstein, G.L. Wallace, M. Stockman, L. Clasen, P.W. Shaw, and J.N. Giedd Patterns of coordinated anatomical change in human cortical development: a longitudinal neuroimaging study of maturational coupling Neuron 72 2011 873 884
67. R.M. Reitan Validity of the trail making test as an indicator of organic brain damage Percept. Mot. Skills 8 1958 271 276 10.2466/pms.1958.8.3.271
68. S.M. Resnick, A.F. Goldszal, C. Davatzikos, S. Golski, M.A. Kraut, E.J. Metter, and A.B. Zonderman One-year age changes in MRI brain volumes in older adults Cereb. Cortex 10 2000 464 472 10.1093/cercor/10.5.464
69. S.M. Resnick, D.L. Pham, M.A. Kraut, A.B. Zonderman, and C. Davatzikos Longitudinal magnetic resonance imaging studies of older adults: a shrinking brain J. Neurosci. 23 2003 3295 3301
70. L.A. Ross, D. McCoy, D.A. Wolk, H.B. Coslett, and I.R. Olson Improved proper name recall by electrical stimulation of the anterior temporal lobes Neuropsychologia 48 12 2010 3671 3674 10.1016/j.neuropsychologia.2010.07.024
71. D.H. Salat, D.N. Greve, J.L. Pacheco, B.T. Quinn, K.G. Helmer, R.L. Buckner, and B. Fischl Regional white matter volume differences in nondemented aging and Alzheimer's disease NeuroImage 44 2009 1247 1258 10.1016/j.neuroimage.2008.10.030
72. J.L. Salvatierra, and M. Rosselli The effect of bilingualism and age on inhibitory control Int. J. Biling. 15 1 2010 26 37 10.1177/1367006910371021
73. G. Schlaug, L. Jäncke, Y. Huang, J.F. Staiger, and H. Steinmetz Increased corpus callosum size in musicians Neuropsychologia 33 1995 1047 1055
74. A.A. Schlegel, J.J. Rudelson, and P.U. Tse White matter structure changes as adults learn a second language J. Cogn. Neurosci. 24 8 2012 1664 1670 10.1162/jocn-a-00240
75. S.R. Schroeder, and V. Marian A bilingual advantage for episodic memory in older adults J. Cogn. Psychol. 24 2012 591 601 10.1080/20445911.2012.669367
76. F. Ségonne, A.M. Dale, E. Busa, M. Glessner, D. Salat, H.K. Hahn, and B. Fischl A hybrid approach to the skull stripping problem in MRI NeuroImage 22 3 2004 1060 1075 10.1016/j.neuroimage.2004.03.032
77. F. Ségonne, J. Pacheco, and B. Fischl Geometrically accurate topology-correction of cortical surfaces using nonseparating loops IEEE Trans. Med. Imaging 26 4 2007 518 529
78. J.G. Sled, A.P. Zijdenbos, and A.C. Evans A nonparametric method for automatic correction of intensity nonuniformity in MRI data IEEE Trans. Med. Imaging 17 1998 87 97 10.1109/42.668698
79. M. Stein, A. Federspiel, T. Koenig, M. Wirth, W. Strik, R. Wiest, and T. Dierks Structural plasticity in the language system related to increased second language proficiency Cortex 48 4 2012 458 465 10.1016/j.cortex.2010.10.007
80. M. Stein, C. Winkler, A. Kaiser, and T. Dierks Structural brain changes related to bilingualism: does immersion make a difference? Front. Psychol. 5 2014 1116 10.3389/fpsyg.2014.01116
81. Y. Stern What is cognitive reserve? Theory and research application of the reserve concept J. Int. Neuropsychol. Soc. 8 2002 448 460 doi:10.1017.S1355617701020240
82. J.R. Stroop Studies of interference in serial verbal reactions J. Exp. Psychol. 28 1935 643 662 10.1037/h0054651
83. H. Takeuchi, Y. Taki, Y. Sassa, H. Hashizume, A. Sekiguchi, T. Nagase, and R. Kawashima Regional gray and white matter volume associated with Stroop interference: evidence from voxel-based morphometry NeuroImage 59 3 2012 2899 2907 10.1016/j.neuroimage.2011.09.064
84. J. Tohka, A. Zijdenbos, and A. Evans Fast and robust parameter estimation for statistical partial volume models in brain MRI NeuroImage 23 2004 84 97 10.1016/j.neuroimage.2004.05.007
85. D. Tranel The left temporal pole is important for retrieving words for unique concrete entities Aphasiology 23 23 2009 867 884 10.1080/02687030802586498
86. K.B. Walhovd, A.M. Fjell, I. Reinvang, A. Lundervold, A.M. Dale, D.E. Eilertsen, and B. Fischl Effects of age on volumes of cortex, white matter and subcortical structures Neurobiol. Aging 26 2005 1261 1270 10.1016/j.neurobiolaging.2005.05.020
87. K.B. Walhovd, L.T. Westlye, I. Amlien, T. Espeseth, I. Reinvang, N. Raz, and A.M. Fjell Consistent neuroanatomical age-related volume differences across multiple samples Neurobiol. Aging 32 5 2011 916 932 10.1016/j.neurobiolaging.2009.05.013
88. C.Y. Wan, and G. Schlaug Music making as a tool for promoting brain plasticity across the life span Neuroscientist 16 2010 566 577 10.1177/1073858410377805
89. R.S. Wilson, P.A. Boyle, J. Yang, B.D. James, and D.A. Bennett Early life instruction in foreign language and music and incidence of mild cognitive impairment Neuropsychology 2015 10.1037/neu0000129, in pres
90. R.A. Zachary, and W.C. Shipley Shipley Institute of Living Scale: Revised Manual 1986 Psychology Services Los Angeles, CA: Western
91. R.J. Zatorre, R.D. Fields, and H. Johansen-Berg Plasticity in gray and white: neuroimaging changes in brain structure during learning Nat. Neurosci. 15 2012 114 146 10.1038/nn.3045
92. A.P. Zijdenbos, R. Forghani, and A.C. Evans Automatic "pipeline" analysis of 3-D MRI data for clinical trials: application to multiple sclerosi IEEE Trans. Med. Imaging 21 2002 1280 1291 10.1109/TMI.2002.806283