Acute and chronic changes in diffusivity measures after sports concussion

Journal of Neurotrauma

Volumn 28, Issue 10, 2011, Pages 2049-2059

  Henry, Luke C ^a   Tremblay, Julie ^b   Tremblay, Sebastien ^a   Lee, Agatha ^e   Brun, Caroline ^c   Lepore, Natasha ^d   Theoret, Hugo ^a,b   Ellemberg, Dave ^a   Lassonde, Maryse ^a,b  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b UNIVERSITY OF MONTREAL   (Canada)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

acute; chronic; diffusion tensor imaging; sports concussion

Indexed keywords

ADULT; ARTICLE; AXIAL DIFFUSIVITY; CONCUSSION; CONTROLLED STUDY; CORPUS CALLOSUM; DIFFUSION TENSOR IMAGING; FOOTBALL; FRACTIONAL ANISOTROPY; HUMAN; MALE; MEAN DIFFUSIVITY; PHYSICAL PARAMETERS; PYRAMIDAL TRACT; SPORT INJURY; WHITE MATTER;

ADOLESCENT; ALGORITHMS; ANALYSIS OF VARIANCE; ANISOTROPY; ATHLETIC INJURIES; AXONS; BRAIN CONCUSSION; CORPUS CALLOSUM; DIFFUSE AXONAL INJURY; DIFFUSION TENSOR IMAGING; FOOTBALL; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MALE; PYRAMIDAL TRACTS; YOUNG ADULT;

EID: 80054746892     PISSN: 08977151     EISSN: 15579042     Source Type: Journal    
DOI: 10.1089/neu.2011.1836     Document Type: Article

References (83)

1. Alexander, D.C., Pierpaoli, C., Basser, P.J., and Gee, J.C. (2001). Spatial transformations of diffusion tensor magnetic resonance images. IEEE Trans. Med. Imaging 20, 1131-1139. (Pubitemid 33106067)
2. Arfanakis, K., Haughton, V.M., Carew, J.D., Rogers, B.P., Dempsey, R.J., and Meyerand, M.E. (2002). Diffusion tensor MR imaging in diffuse axonal injury. AJNR Am. J. Neuror-adiol. 23, 794-802. (Pubitemid 34525695)
3. Aubry, M., Cantu, R., Dvorak, J., Graf-Baumann, T., Johnston, K., Kelly, J., Lovell, M., McCrory, P., Meeuwisse, W., and Schamasch, P. (2002). Summary and agreement statement of the First International Conference on Concussion in Sport, Vienna 2001. Recommendations for the improvement of safety and health of athletes who may suffer concussive injuries. Br. J. Sports Med. 36, 6-10.
4. Bain, A.C., and Meaney, D.F. (2000). Tissue-level thresholds for axonal damage in an experimental model of central nervous system white matter injury. J. Biomech. Eng. 122, 615-622. (Pubitemid 32047025)
5. Barr, M. (2005). The Human Nervous System: An Anatomical Viewpoint, 8th ed. Lippincott Williams & Wilkins: Baltimore.
6. Bhagat, Y.A., Emery, D.J., Shuaib, A., Sher, F., Rizvi, N.H., Akh-tar, N., Clare, T.L., Leatherdale, T., and Beaulieu, C. (2006). The relationship between diffusion anisotropy and time of onset after stroke. J. Cereb. Blood Flow Metab. 26, 1442-1450. (Pubitemid 44629891)
7. Bigler, E.D. (1999). Neuroimaging in pediatric traumatic head injury: diagnostic considerations and relationships to neuro-behavioral outcome. J. Head Trauma Rehabil. 14, 406-423. (Pubitemid 29372865)
8. Bruce, J.M., and Echemendia, R.J. (2009). History of multiple self-reported concussions is not associated with reduced cognitive abilities. Neurosurgery 64, 100-106; discussion 106.
9. Buki, A., and Povlishock, J.T. (2006). All roads lead to discon-nection?-Traumatic axonal injury revisited. Acta Neurochir. (Wien.) 148, 181-193; discussion 193-194.
10. Chappell, M.H., Ulug, A.M., Zhang, L., Heitger, M.H., Jordan, B.D., Zimmerman, R.D., and Watts, R. (2006). Distribution of microstructural damage in the brains of professional boxers: a diffusion MRI study. J. Magn. Reson. Imaging 24, 537-542. (Pubitemid 44320554)
11. Chu, Z., Wilde, E.A., Hunter, J.V., McCauley, S.R., Bigler, E.D., Troyanskaya, M., Yallampalli, R., Chia, J.M., and Levin, H.S. (2010). Voxel-based analysis of diffusion tensor imaging in mild traumatic brain injury in adolescents. AJNR Am. J. Neuroradiol. 31, 340-346.
12. Cubon, V.A., Putukian, M., Boyer, C., and Dettwiler, A. (2011). A diffusion tensor imaging study on the white matter skeleton in individuals with sports-related concussion. J. Neurotrauma 28, 189-201.
13. De Beaumont, L., Brisson, B., Lassonde, M., and Jolicoeur, P. (2007). Long-term electrophysiological changes in athletes with a history of multiple concussions. Brain Inj. 21, 631-644. (Pubitemid 46993189)
14. De Beaumont, L., Lassonde, M., Leclerc, S., and Theoret, H. (2007). Long-term and cumulative effects of sports concussion on motor cortex inhibition. Neurosurgery 61, 329-336; discussion 336-327. (Pubitemid 47357326)
15. De Beaumont, L., Mongeon, D., Tremblay, S., Messier, J., Prince, F., Leclerc, S., Lassonde, M., and Theoret, H. (accepted). Persistent motor system abnormalities in active concussed athletes. Neurology.
16. De Beaumont, L., Theoret, H., Mongeon, D., Messier, J., Leclerc, S., Tremblay, S., Ellemberg, D., and Lassonde, M. (2009). Brain function decline in healthy retired athletes who sustained their last sports concussion in early adulthood. Brain 132, 695-708.
17. Dikmen, S., McLean, A., and Temkin, N. (1986). Neuropsycho-logical and psychosocial consequences of minor head injury. J. Neurol. Neurosurg. Psychiatry 49, 1227-1232. (Pubitemid 17174022)
18. Ducreux, D., Huynh, I., Fillard, P., Renoux, J., Petit-Lacour, M.C., Marsot-Dupuch, K., and Lasjaunias, P. (2005). Brain MR diffusion tensor imaging and fibre tracking to differentiate between two diffuse axonal injuries. Neuroradiology 47, 604-608. (Pubitemid 41258709)
19. Ducreux, D., Nasser, G., Lacroix, C., Adams, D., and Lasjaunias, P. (2005). MR diffusion tensor imaging, fiber tracking, and single-voxel spectroscopy findings in an unusual MELAS case. AJNR Am. J. Neuroradiol. 26, 1840-1844. (Pubitemid 43853689)
20. Ellemberg, D., Henry, L.C., Macciocchi, S.N., Guskiewicz, K.M., and Broglio, S.P. (2009). Advances in sport concussion assessment: from behavioral to brain imaging measures. J. Neurotrauma 26, 2365-2382.
21. Farkas, O., Lifshitz, J., and Povlishock, J.T. (2006). Mechanopora-tion induced by diffuse traumatic brain injury: an irreversible or reversible response to injury? J. Neurosci. 26, 3130-3140.
22. Gaetz, M., Goodman, D., and Weinberg, H. (2000). Electro-physiological evidence for the cumulative effects of concussion. Brain Inj. 14, 1077-1088. (Pubitemid 32013966)
23. Gasparovic, C., Yeo, R., Mannell, M., Ling, J., Elgie, R., Phillips, J., Doezema, D., and Mayer, A.R. (2009). Neurometabolite concentrations in gray and white matter in mild traumatic brain injury: an 1H-magnetic resonance spectroscopy study. J. Neurotrauma 26, 1635-1643.
24. Gennarelli, T.A. (1996). The spectrum of traumatic axonal injury. Neuropathol. Appl. Neurobiol. 22, 509-513. (Pubitemid 27023364)
25. Gennarelli, T.A., Thibault, L.E., Tipperman, R., Tomei, G., Sergot, R., Brown, M., Maxwell, W.L., Graham, D.I., Adams, J.H., and Irvine, A. (1989). Axonal injury in the optic nerve: a model simulating diffuse axonal injury in the brain. J. Neurosurg. 71, 244-253. (Pubitemid 19194943)
26. Gentry, L.R. (1994). Imaging of closed head injury. Radiology 191, 1-17. (Pubitemid 24098193)
27. Gerberding, J.L., and Binder, S. (2003). Report to Congress on Mild Traumatic Brain Injury in the United States: Steps to Prevent a Serious Public Health Problem. National Center for Injury Prevention and Control, Centers for Disease Control and Prevention: Atlanta, p. 56.
28. Giza, C.C., and Hovda, D.A. (2001). The neurometabolic cascade of concussion. J. Athl. Train. 36, 228-235. (Pubitemid 33685230)
29. Green, H.A., Pena, A., Price, C.J., Warburton, E.A., Pickard, J.D., Carpenter, T.A., and Gillard, J.H. (2002). Increased anisotropy in acute stroke: a possible explanation. Stroke 33, 1517-1521. (Pubitemid 34619950)
30. Guskiewicz, K.M., Bruce, S.L., Cantu, R.C., Ferrara, M.S., Kelly, J.P., McCrea, M., Putukian, M., and McLeod, T.C. (2004). Recommendations on management of sport-related concussion: summary of the National Athletic Trainers' Association position statement. Neurosurgery 55, 891-895; discussion 896.
31. Guskiewicz, K.M., Bruce, S.L., Cantu, R.C., Ferrara, M.S., Kelly, J.P., McCrea, M., Putukian, M., and Valovich McLeod, T.C. (2004). National Athletic Trainers' Association Position Statement: Management of Sport-Related Concussion. J. Athl. Train. 39, 280-297. (Pubitemid 39318954)
32. Guskiewicz, K.M., McCrea, M., Marshall, S.W., Cantu, R.C., Randolph, C., Barr, W., Onate, J.A., and Kelly, J.P. (2003). Cumulative effects associated with recurrent concussion in collegiate football players: the NCAA Concussion Study. JAMA 290, 2549-2555. (Pubitemid 37443284)
33. Hartikainen, K.M., Waljas, M., Isoviita, T., Dastidar, P., Liima-tainen, S., Solbakk, A.K., Ogawa, K.H., Soimakallio, S., Ylinen, A., and Ohman, J. (2010). Persistent symptoms in mild to moderate traumatic brain injury associated with executive dysfunction. J. Clin. Exp. Neuropsychol. 32, 767-774.
34. Henry, L.C., Tremblay, S., Boulanger, Y., Ellemberg, D., and Lassonde, M. (2010). Neurometabolic changes in the acute phase after sports concussions correlate with symptom severity. J. Neurotrauma 27, 65-76.
35. Henry, L.C., Tremblay, S., Leclerc, S., Khiat, A., Boulanger, Y., Ellemberg, D., and Lassonde, M. (submitted). Metabolic changes in concussed athletes during the acute and chronic post-injury phases.
36. Hinton-Bayre, A.D., and Geffen, G. (2002). Severity of sports-related concussion and neuropsychological test performance. Neurology 59, 1068-1070.
37. Hofer, S., and Frahm, J. (2006). Topography of the human corpus callosum revisited-comprehensive fiber tractography using diffusion tensor magnetic resonance imaging. Neuroimage 32, 989-994. (Pubitemid 44278703)
38. Holbourn, A. (1943). Mechanisms of head injuries. Lancet 2, 438-441.
39. Holbourn, A. (1945). The mechanics of brain injuries. Br. Med. Bulletin 3, 147-149.
40. Holm, L., Cassidy, J.D., Carroll, L.J., and Borg, J. (2005). Summary of the WHO Collaborating Centre for Neurotrauma Task Force on Mild Traumatic Brain Injury. J. Rehabil. Med. 37, 137-141. (Pubitemid 40775151)
41. Huisman, T.A., Schwamm, L.H., Schaefer, P.W., Koroshetz, W.J., Shetty-Alva, N., Ozsunar, Y., Wu, O., and Sorensen, A.G. (2004). Diffusion tensor imaging as potential biomarker of white matter injury in diffuse axonal injury. AJNR Am. J. Neuroradiol. 25, 370-376. (Pubitemid 38374913)
42. Hurley, R.A., McGowan, J.C., Arfanakis, K., and Taber, K.H. (2004). Traumatic axonal injury: novel insights into evolution and identification. J. Neuropsychiatry Clin. Neurosci. 16, 1-7. (Pubitemid 38233358)
43. Jenkinson, M., and Smith, S. (2001). A global optimisation method for robust affine registration of brain images. Med. Image Anal. 5, 143-156. (Pubitemid 35282800)
44. Johnston, K.M., Ptito, A., Chankowsky, J., and Chen, J.K. (2001). New frontiers in diagnostic imaging in concussive head injury. Clin. J. Sport Med. 11, 166-175. (Pubitemid 32667129)
45. Kochunov, P., Lancaster, J.L., Thompson, P., Woods, R., Maz-ziotta, J., Hardies, J., and Fox, P. (2001). Regional spatial normalization: toward an optimal target. J. Comput. Assist. Tomogr. 25, 805-816. (Pubitemid 32861709)
46. Kraus, M.F., Susmaras, T., Caughlin, B.P., Walker, C.J., Sweeney, J.A., and Little, D.M. (2007). White matter integrity and cognition in chronic traumatic brain injury: a diffusion tensor imaging study. Brain 130, 2508-2519. (Pubitemid 47511721)
47. Kumar, R., Gupta, R.K., Husain, M., Chaudhry, C., Srivastava, A., Saksena, S., and Rathore, R.K. (2009). Comparative evaluation of corpus callosum DTI metrics in acute mild and moderate traumatic brain injury: its correlation with neu-ropsychometric tests. Brain Inj. 23, 675-685.
48. Lang, F., Busch, G.L., Ritter, M., Volkl, H., Waldegger, S., Gul-bins, E., and Haussinger, D. (1998). Functional significance of cell volume regulatory mechanisms. Physiol. Rev. 78, 247-306. (Pubitemid 28070981)
49. Lee, J.W., Choi, C.G., and Chun, M.H. (2006). Usefulness of diffusion tensor imaging for evaluation of motor function in patients with traumatic brain injury: three case studies. J. Head Trauma Rehabil. 21, 272-278. (Pubitemid 44309960)
50. Lepore, N., Brun, C.A., Chiang, M.C., Chou, Y.Y., Dutton, R.A., Hayashi, K.M., Lopez, O.L., Aizenstein, H.J., Toga, A.W., Becker, J.T., and Thompson, P.M. (2006). Multivariate statistics of the Jacobian matrices in tensor based morphometry and their application to HIV/AIDS. Med. Image Comput. Com-put. Assist. Interv. Int. Conf. Med. Image Comput. Comput. Assist. Interv. 9, 191-198. (Pubitemid 44609106)
51. Lepore, N., Brun, C., Chou, Y.Y., Chiang, M.C., Dutton, R.A., Hayashi, K.M., Luders, E., Lopez, O.L., Aizenstein, H.J., Toga, A.W., Becker, J.T., and Thompson, P.M. (2008). Generalized tensor-based morphometry of HIV/AIDS using multivariate statistics on deformation tensors. IEEE Trans. Med. Imaging 27, 129-141.
52. Le, T.H., Mukherjee, P., Henry, R.G., Berman, J.I., Ware, M., and Manley, G.T. (2005). Diffusion tensor imaging with three-dimensional fiber tractography of traumatic axonal shearing injury: an imaging correlate for the posterior callosal "disconnection" syndrome: case report. Neurosurgery 56, 189. (Pubitemid 40054011)
53. Maxwell, W.L., Kansagra, A.M., Graham, D.I., Adams, J.H., and Gennarelli, T.A. (1988). Freeze-fracture studies of reactive myelinated nerve fibres after diffuse axonal injury. Acta Neuropathol. 76, 395-406.
54. Mayer, A.R., Ling, J., Mannell, M.V., Gasparovic, C., Phillips, J.P., Doezema, D., Reichard, R., and Yeo, R.A. (2010). A prospective diffusion tensor imaging study in mild traumatic brain injury. Neurology 74, 643-650.
55. McCrory, P., Johnston, K., Meeuwisse, W., Aubry, M., Cantu, R., Dvorak, J., Graf-Baumann, T., Kelly, J., Lovell, M., and Scha-masch, P. (2005). Summary and agreement statement of the 2nd International Conference on Concussion in Sport, Prague 2004. Br. J. Sports Med. 39, 196-204. (Pubitemid 40478202)
56. McCrory, P., Meeuwisse, W., Johnston, K., Dvorak, J., Aubry, M., Molloy, M., and Cantu, R. (2009). Consensus statement on Concussion in Sport 3rd International Conference on Concussion in Sport held in Zurich, November 2008. Clin. J. Sport Med. 19, 185-200.
57. Messé, A., Caplain, S., Paradot, G., Garrigue, D., Mineo, J.F., Soto Ares, G., Ducreuy, D., Vignaud, F., Rozec, G., Desal, H., Pélègrini-Issac, M., Montreuil, M., Benail, H., Lehéricy, S. (2010). Diffusion tensor imaging and white matter lesions at the subacute stage in mild traumatic brain injury with persistent neurobehavioral impairment. Human Brain Mapping 32, 999-1011.
58. Meythaler, J.M., Peduzzi, J.D., Eleftheriou, E., and Novack, T.A. (2001). Current concepts: diffuse axonal injury-associated traumatic brain injury. Arch. Phys. Med. Rehabil. 82, 1461-1471. (Pubitemid 32952371)
59. Miles, L., Grossman, R.I., Johnson, G., Babb, J.S., Diller, L., and Inglese, M. (2008). Short-term DTI predictors of cognitive dysfunction in mild traumatic brain injury. Brain Inj. 22, 115-122. (Pubitemid 351233920)
60. Newcombe, V.F., Williams, G.B., Nortje, J., Bradley, P.G., Chatfield, D.A., Outtrim, J.G., Harding, S.G., Coles, J.P., Maiya, B., Gillard, J.H., Hutchinson, P.J., Pickard, J.D., Carpenter, T.A., and Menon, D.K. (2008). Concordant biology underlies discordant imaging findings: diffusivity behaves differently in grey and white matter post acute neurotrauma. Acta Neurochir. Suppl. 102, 247-251.
61. Newcombe, V.F., Williams, G.B., Nortje, J., Bradley, P.G., Harding, S.G., Smielewski, P., Coles, J.P., Maiya, B., Gillard, J.H., Hutchinson, P.J., Pickard, J.D., Carpenter, T.A., and Me-non, D.K. (2007). Analysis of acute traumatic axonal injury using diffusion tensor imaging. Br. J. Neurosurg. 21, 340-348. (Pubitemid 47221522)
62. Niogi, S.N., Mukherjee, P., Ghajar, J., Johnson, C., Kolster, R.A., Sarkar, R., Lee, H., Meeker, M., Zimmerman, R.D., Manley, G.T., and McCandliss, B.D. (2008). Extent of microstructural white matter injury in postconcussive syndrome correlates with impaired cognitive reaction time: a 3T diffusion tensor imaging study of mild traumatic brain injury. AJNR Am. J. Neuroradiol. 29, 967-973. (Pubitemid 351684976)
63. Okumura, A., Yasokawa, Y., Nakayama, N., Miwa, K., Shinoda, J., and Iwama, T. (2005). [The clinical utility of MR diffusion tensor imaging and spatially normalized PET to evaluate traumatic brain injury patients with memory and cognitive impairments]. No To Shinkei 57, 115-122. (Pubitemid 40562997)
64. Ommaya, A.K., and Gennarelli, T.A. (1974). Cerebral concussion and traumatic unconsciousness. Correlation of experimental and clinical observations of blunt head injuries. Brain 97, 633-654.
65. Peerless, S.J., and Rewcastle, N.B. (1967). Shear injuries of the brain. Can. Med. Assoc. J. 96, 577-582.
66. Pfefferbaum, A., and Sullivan, E.V. (2003). Increased brain white matter diffusivity in normal adult aging: relationship to an-isotropy and partial voluming. Magn. Reson. Med. 49, 953-961. (Pubitemid 36523483)
67. Pierpaoli, C., Jezzard, P., Basser, P.J., Barnett, A., and Di Chiro, G. (1996). Diffusion tensor MR imaging of the human brain. Radiology 201, 637-648.
68. Pudenz, R.H., and Shelden, C.H. (1946). The lucite calvarium; a method for direct observation of the brain; cranial trauma and brain movement. J. Neurosurg. 3, 487-505.
69. Quality Standards Subcommittee and Neurology AAo. (1997). Practice parameter. Neurobiology (Bp). 1-5.
70. Shen, S., Szameitat, A.J., and Sterr, A. (2007). VBM lesion detection depends on the normalization template: a study using simulated atrophy. Magn. Reson. Imaging 25, 1385-1396. (Pubitemid 350122911)
71. Song, S.K., Sun, S.W., Ramsbottom, M.J., Chang, C., Russell, J., and Cross, A.H. (2002). Dysmyelination revealed through MRI as increased radial (but unchanged axial) diffusion of water. Neuroimage 17, 1429-1436. (Pubitemid 35333862)
72. Strange, K. (1992). Regulation of solute and water balance and cell volume in the central nervous system. J. Am. Soc. Ne-phrol. 3, 12-27.
73. Theriault, M., De Beaumont, L., Tremblay, S., Lassonde, M., and Jolicoeur, P. (2010). Cumulative effects of concussions in athletes revealed by electrophysiological abnormalities on visual working memory. J. Clin. Exp. Neuropsychol. 1-12.
74. Toga, A.W., and Mazziotta, J.C. (2002). Brain Mapping: The Methods, 2nd ed. Academic Press: San Diego.
75. Vagnozzi, R., Signoretti, S., Cristofori, L., Alessandrini, F., Floris, R., Isgro, E., Ria, A., Marziale, S., Zoccatelli, G., Tavazzi, B., Del Bolgia, F., Sorge, R., Broglio, S.P., McIntosh, T.K., and Lazzarino, G. (2010). Assessment of metabolic brain damage and recovery following mild traumatic brain injury: a multi-centre, proton magnetic resonance spectroscopic study in concussed patients. Brain 133, 3232-3242.
76. Vagnozzi, R., Signoretti, S., Tavazzi, B., Floris, R., Ludovici, A., Marziali, S., Tarascio, G., Amorini, A.M., Di Pietro, V., Delfini, R., and Lazzarino, G. (2008). Temporal window of metabolic brain vulnerability to concussion: a pilot 1H-magnetic resonance spectroscopic study in concussed athletes-part III. Neurosurgery 62, 1286-1295; discussion 1295-1286.
77. Westlye, L.T., Walhovd, K.B., Dale, A.M., Bjornerud, A., Due-Tonnessen, P., Engvig, A., Grydeland, H., Tamnes, C.K., Ostby, Y., and Fjell, A.M. (2010). Life-span changes of the human brain white matter: diffusion tensor imaging (DTI) and volumetry. Cereb. Cortex 20, 2055-2068.
78. Wilde, E.A., McCauley, S.R., Hunter, J.V., Bigler, E.D., Chu, Z., Wang, Z.J., Hanten, G.R., Troyanskaya, M., Yallampalli, R., Li, X., Chia, J., and Levin, H.S. (2008). Diffusion tensor imaging of acute mild traumatic brain injury in adolescents. Neurology 70, 948-955. (Pubitemid 351430744)
79. Wilde, E.A., Ramos, M.A., Yallampalli, R., Bigler, E.D., McCauley, S.R., Chu, Z., Wu, T.C., Hanten, G., Scheibel, R.S., Li, X., Vasquez, A.C., Hunter, J.V., and Levin, H.S. (2010). Diffusion tensor imaging of the cingulum bundle in children after traumatic brain injury. Dev. Neuropsychol. 35, 333-351.
80. Wozniak, J.R., and Lim, K.O. (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. (Pubitemid 44292285)
81. Wozniak, J.R., Krach, L., Ward, E., Mueller, B.A., Muetzel, R., Schnoebelen, S., Kiragu, A., and Lim, K.O. (2007). Neurocog-nitive and neuroimaging correlates of pediatric traumatic brain injury: a diffusion tensor imaging (DTI) study. Arch. Clin. Neuropsychol. 22, 555-568. (Pubitemid 46921419)
82. Zhang, H., Yushkevich, P.A., Alexander, D.C., and Gee, J.C. (2006). Deformable registration of diffusion tensor MR images with explicit orientation optimization. Med. Image Anal. 10, 764-785. (Pubitemid 44283800)
83. Zillmer, E.A., and Spiers, M.V. (2001). Principles of Neu-ropsychology, 1st ed. Wadsworth: Belmont, CA.