Diffusion Tensor Imaging at 3 Hours after Traumatic Spinal Cord Injury Predicts Long-Term Locomotor Recovery
Abstract
Accurate diagnosis of spinal cord injury (SCI) severity must be achieved before highly aggressive experimental therapies can be tested responsibly in the early phases after trauma. These studies demonstrate for the first time that axial diffusivity (λ||), derived from diffusion tensor imaging (DTI) within 3 h after SCI, accurately predicts long-term locomotor behavioral recovery in mice. Female C57BL/6 mice underwent sham laminectomy or graded contusive spinal cord injuries at the T9 vertebral level (5 groups, n = 8 for each group). In-vivo DTI examinations were performed immediately after SCI. Longitudinal measurements of hindlimb locomotor recovery were obtained using the Basso mouse scale (BMS). Injured and spared regions of ventrolateral white matter (VLWM) were reliably separated in the hyperacute phase by threshold segmentation. Measurements of λ|| were compared with histology in the hyperacute phase and 14 days after injury. The spared normal VLWM determined by hyperacute λ|| and 14-day histology correlated well (r = 0.95). A strong correlation between hindlimb locomotor function recovery and λ||-determined spared normal VLWM was also observed. The odds of significant locomotor recovery increased by 18% with each 1% increase in normal VLWM measured in the hyperacute phase (odds ratio = 1.18, p = 0.037). The capability of measuring subclinical changes in spinal cord physiology and murine genetic advantages offer an early window into the basic mechanisms of SCI that was not previously possible. Although significant obstacles must still be overcome to derive similar data in human patients, the path to clinical translation is foreseeable and achievable.
Get full access to this article
View all available purchase options and get full access to this article.
References
Banik N.L.Matzelle D.C.Gantt-Wilford G.Osborne A.Hogan E.L.1997. Increased calpain content and progressive degradation of neurofilament protein in spinal cord injuryBrain Res.752301-306. Banik, N.L., Matzelle, D.C., Gantt-Wilford, G., Osborne, A., and Hogan, E.L. (1997). Increased calpain content and progressive degradation of neurofilament protein in spinal cord injury. Brain Res. 752, 301–306.
Basso D.M.Beattie M.S.Bresnahan J.C.1996. Graded histological and locomotor outcomes after spinal cord contusion using the NYU weight-drop device versus transectionExp. Neurol.139244-256. Basso, D.M., Beattie, M.S., and Bresnahan, J.C. (1996). Graded histological and locomotor outcomes after spinal cord contusion using the NYU weight-drop device versus transection. Exp. Neurol. 139, 244–256.
Basso D.M.Fisher L.C.Anderson A.J.Jakeman L.B.McTigue D.M.Popovich P.G.2006. Basso Mouse Scale for locomotion detects differences in recovery after spinal cord injury in five common mouse strainsJ. Neurotrauma23635-659. Basso, D.M., Fisher, L.C., Anderson, A.J., Jakeman, L.B., McTigue, D.M., and Popovich, P.G. (2006). Basso Mouse Scale for locomotion detects differences in recovery after spinal cord injury in five common mouse strains. J. Neurotrauma 23, 635–659.
Bilgen M.Abbe R.Narayana P.A.2001. Dynamic contrast-enhanced MRI of experimental spinal cord injury: in vivo serial studiesMagn. Reson. Med.45614-622. Bilgen, M., Abbe, R., and Narayana, P.A. (2001). Dynamic contrast-enhanced MRI of experimental spinal cord injury: in vivo serial studies. Magn. Reson. Med. 45, 614–622.
Blight A.R.1992. Macrophages and inflammatory damage in spinal cord injuryJ. Neurotrauma9Suppl. 1S83-S91. Blight, A.R. (1992). Macrophages and inflammatory damage in spinal cord injury. J. Neurotrauma 9(Suppl. 1), S83–S91.
Blight A.R.Decrescito V.1986. Morphometric analysis of experimental spinal cord injury in the cat: the relation of injury intensity to survival of myelinated axonsNeuroscience19321-341. Blight, A.R., and Decrescito, V. (1986). Morphometric analysis of experimental spinal cord injury in the cat: the relation of injury intensity to survival of myelinated axons. Neuroscience 19, 321–341.
Bracken M.B.Shepard M.J.Holford T.R.Leo-Summers L.Aldrich E.F.Fazl M.Fehlings M.Herr D.L.Hitchon P.W.Marshall L.F.Nockels R.P.Pascale V.Perot P.L. Jr.Piepmeier J.Sonntag V.K.Wagner F.Wilberger J.E.Winn H.R.Young W.1997. Administration of methylprednisolone for 24 or 48 hours or tirilazad mesylate for 48 hours in the treatment of acute spinal cord injury. Results of the Third National Acute Spinal Cord Injury Randomized Controlled Trial. National Acute Spinal Cord Injury StudyJAMA2771597-1604. Bracken, M.B., Shepard, M.J., Holford, T.R., Leo-Summers, L., Aldrich, E.F., Fazl, M., Fehlings, M., Herr, D.L., Hitchon, P.W., Marshall, L.F., Nockels, R.P., Pascale, V., Perot, P.L., Jr., Piepmeier, J., Sonntag, V.K., Wagner, F., Wilberger, J.E., Winn, H.R., and Young, W. (1997). Administration of methylprednisolone for 24 or 48 hours or tirilazad mesylate for 48 hours in the treatment of acute spinal cord injury. Results of the Third National Acute Spinal Cord Injury Randomized Controlled Trial. National Acute Spinal Cord Injury Study. JAMA 277, 1597–1604.
Brody D.L.Mac Donald C.Kessens C.C.Yuede C.Parsadanian M.Spinner M.Kim E.Schwetye K.E.Holtzman D.M.Bayly P.V.2007. Electromagnetic controlled cortical impact device for precise, graded experimental traumatic brain injuryJ. Neurotrauma24657-673. Brody, D.L., Mac Donald, C., Kessens, C.C., Yuede, C., Parsadanian, M., Spinner, M., Kim, E., Schwetye, K.E., Holtzman, D.M., and Bayly, P.V. (2007). Electromagnetic controlled cortical impact device for precise, graded experimental traumatic brain injury. J. Neurotrauma 24, 657–673.
Budde M.D.Kim J.H.Liang H.F.Russell J.H.Cross A.H.Song S.K.2008. Axonal injury detected by in vivo diffusion tensor imaging correlates with neurological disability in a mouse model of multiple sclerosisNMR Biomed.21589-597. Budde, M.D., Kim, J.H., Liang, H.F., Russell, J.H., Cross, A.H., and Song, S.K. (2008). Axonal injury detected by in vivo diffusion tensor imaging correlates with neurological disability in a mouse model of multiple sclerosis. NMR Biomed. 21, 589–597.
DeBoy C.A.Zhang J.Dike S.Shats I.Jones M.Reich D.S.Mori S.Nguyen T.Rothstein B.Miller R.H.Griffin J.T.Kerr D.A.Calabresi P.A.2007. High resolution diffusion tensor imaging of axonal damage in focal inflammatory and demyelinating lesions in rat spinal cordBrain1302199-2210. DeBoy, C.A., Zhang, J., Dike, S., Shats, I., Jones, M., Reich, D.S., Mori, S., Nguyen, T., Rothstein, B., Miller, R.H., Griffin, J.T., Kerr, D.A., and Calabresi, P.A. (2007). High resolution diffusion tensor imaging of axonal damage in focal inflammatory and demyelinating lesions in rat spinal cord. Brain 130, 2199–2210.
Ditunno J.F.Little J.W.Tessler A.Burns A.S.2004. Spinal shock revisited: a four-phase modelSpinal Cord42383-395. Ditunno, J.F., Little, J.W., Tessler, A., and Burns, A.S. (2004). Spinal shock revisited: a four-phase model. Spinal Cord 42, 383–395.
Ellingson B.M.Ulmer J.L.Kurpad S.N.Schmit B.D.2008a. Diffusion tensor MR imaging in chronic spinal cord injuryAJNR Am. J. Neuroradiol.291976-1982. Ellingson, B.M., Ulmer, J.L., Kurpad, S.N., and Schmit, B.D. (2008a). Diffusion tensor MR imaging in chronic spinal cord injury. AJNR Am. J. Neuroradiol. 29, 1976–1982.
Ellingson B.M.Ulmer J.L.Schmit B.D.2008b. Morphology and morphometry of human chronic spinal cord injury using diffusion tensor imaging and fuzzy logicAnn. Biomed. Eng.36224-236. Ellingson, B.M., Ulmer, J.L., and Schmit, B.D. (2008b). Morphology and morphometry of human chronic spinal cord injury using diffusion tensor imaging and fuzzy logic. Ann. Biomed. Eng. 36, 224–236.
Facon D.Ozanne A.Fillard P.Lepeintre J.F.Tournoux-Facon C.Ducreux D.2005. MR diffusion tensor imaging and fiber tracking in spinal cord compressionAJNR Am. J. Neuroradiol.261587-1594. Facon, D., Ozanne, A., Fillard, P., Lepeintre, J.F., Tournoux-Facon, C., and Ducreux, D. (2005). MR diffusion tensor imaging and fiber tracking in spinal cord compression. AJNR Am. J. Neuroradiol. 26, 1587–1594.
Fehlings M.G.Perrin R.G.2006. The timing of surgical intervention in the treatment of spinal cord injury: a systematic review of recent clinical evidenceSpine31S28-S35discussion S36. Fehlings, M.G., and Perrin, R.G. (2006). The timing of surgical intervention in the treatment of spinal cord injury: a systematic review of recent clinical evidence. Spine 31, S28–S35; discussion S36.
Gallyas F.Farkas O.Mazlo M.2002. Traumatic compaction of the axonal cytoskeleton induces argyrophilia: histological and theoretical importanceActa Neuropathol.10336-42. Gallyas, F., Farkas, O., and Mazlo, M. (2002). Traumatic compaction of the axonal cytoskeleton induces argyrophilia: histological and theoretical importance. Acta Neuropathol. 103, 36–42.
Gaviria M.Bonny J.M.Haton H.Jean B.Teigell M.Renou J.P.Privat A.2006. Time course of acute phase in mouse spinal cord injury monitored by ex vivo quantitative MRINeurobiol. Dis.22694-701. Gaviria, M., Bonny, J.M., Haton, H., Jean, B., Teigell, M., Renou, J.P., and Privat, A. (2006). Time course of acute phase in mouse spinal cord injury monitored by ex vivo quantitative MRI. Neurobiol. Dis. 22, 694–701.
Guleria S.Gupta R.K.Saksena S.Chandra A.Srivastava R.N.Husain M.Rathore R.Narayana P.A.2008. Retrograde Wallerian degeneration of cranial corticospinal tracts in cervical spinal cord injury patients using diffusion tensor imagingJ. Neurosci. Res.862271-2280. Guleria, S., Gupta, R.K., Saksena, S., Chandra, A., Srivastava, R.N., Husain, M., Rathore, R., and Narayana, P.A. (2008). Retrograde Wallerian degeneration of cranial corticospinal tracts in cervical spinal cord injury patients using diffusion tensor imaging. J. Neurosci. Res. 86, 2271–2280.
Hasan K.M.Narayana P.A.2006. Retrospective measurement of the diffusion tensor eigenvalues from diffusion anisotropy and mean diffusivity in DTIMagn. Reson. Med.56130-137. Hasan, K.M., and Narayana, P.A. (2006). Retrospective measurement of the diffusion tensor eigenvalues from diffusion anisotropy and mean diffusivity in DTI. Magn. Reson. Med. 56, 130–137.
Hashimoto M.Sun D.Rittling S.R.Denhardt D.T.Young W.2007. Osteopontin-deficient mice exhibit less inflammation, greater tissue damage, and impaired locomotor recovery from spinal cord injury compared with wild-type controlsJ. Neurosci.273603-3611. Hashimoto, M., Sun, D., Rittling, S.R., Denhardt, D.T., and Young, W. (2007). Osteopontin-deficient mice exhibit less inflammation, greater tissue damage, and impaired locomotor recovery from spinal cord injury compared with wild-type controls. J. Neurosci. 27, 3603–3611.
Jakeman L.B.Guan Z.Wei P.Ponnappan R.Dzwonczyk R.Popovich P.G.Stokes B.T.2000. Traumatic spinal cord injury produced by controlled contusion in mouseJ. Neurotrauma17299-319. Jakeman, L.B., Guan, Z., Wei, P., Ponnappan, R., Dzwonczyk, R., Popovich, P.G., and Stokes, B.T. (2000). Traumatic spinal cord injury produced by controlled contusion in mouse. J. Neurotrauma 17, 299–319.
Keirstead H.S.Blakemore W.F.1997. Identification of post-mitotic oligodendrocytes incapable of remyelination within the demyelinated adult spinal cordJ. Neuropathol. Exp. Neurol.561191-1201. Keirstead, H.S., and Blakemore, W.F. (1997). Identification of post-mitotic oligodendrocytes incapable of remyelination within the demyelinated adult spinal cord. J. Neuropathol. Exp. Neurol. 56, 1191–1201.
Kim J.H.Budde M.D.Liang H.F.Klein R.S.Russell J.H.Cross A.H.Song S.K.2006. Detecting axon damage in spinal cord from a mouse model of multiple sclerosisNeurobiol. Dis.21626-632. Kim, J.H., Budde, M.D., Liang, H.F., Klein, R.S., Russell, J.H., Cross, A.H., and Song, S.K. (2006). Detecting axon damage in spinal cord from a mouse model of multiple sclerosis. Neurobiol. Dis. 21, 626–632.
Kim J.H.Haldar J.Liang Z.P.Song S.K.2009a. Diffusion tensor imaging of mouse brain stem and cervical spinal cordJ. Neurosci. Methods.176186-191. Kim, J.H., Haldar, J., Liang, Z.P., and Song, S.K. (2009a). Diffusion tensor imaging of mouse brain stem and cervical spinal cord. J. Neurosci. Methods. 176, 186–191.
Kim J.H.Loy D.N.Liang H.F.Trinkaus K.Schmidt R.E.Song S.K.2007. Noninvasive diffusion tensor imaging of evolving white matter pathology in a mouse model of acute spinal cord injuryMagn. Reson. Med.58253-260. Kim, J.H., Loy, D.N., Liang, H.F., Trinkaus, K., Schmidt, R.E., and Song, S.K. (2007). Noninvasive diffusion tensor imaging of evolving white matter pathology in a mouse model of acute spinal cord injury. Magn. Reson. Med. 58, 253–260.
Kim J.H.Tu T.W.Bayly P.Song S.K.2009b. Impact speed does not determine severity of spinal cord injury in mice with fixed impact displacementJ. Neurotrauma. Kim, J.H., Tu, T.W., Bayly, P., and Song, S.K. (2009b). Impact speed does not determine severity of spinal cord injury in mice with fixed impact displacement. J. Neurotrauma, DOI 10.1089/neu.2008-0728.
Koay C.G.Chang L.C.Carew J.D.Pierpaoli C.Basser P.J.2006. A unifying theoretical and algorithmic framework for least squares methods of estimation in diffusion tensor imagingJ. Magn. Reson.182115-125. Koay, C.G., Chang, L.C., Carew, J.D., Pierpaoli, C., and Basser, P.J. (2006). A unifying theoretical and algorithmic framework for least squares methods of estimation in diffusion tensor imaging. J. Magn. Reson. 182, 115–125.
Little J.W.Ditunno J.F. Jr.Stiens S.A.Harris R.M.1999. Incomplete spinal cord injury: neuronal mechanisms of motor recovery and hyperreflexiaArch. Phys. Med. Rehabil.80587-599. Little, J.W., Ditunno, J.F., Jr., Stiens, S.A., and Harris, R.M. (1999). Incomplete spinal cord injury: neuronal mechanisms of motor recovery and hyperreflexia. Arch. Phys. Med. Rehabil. 80, 587–599.
Loy D.N.Kim J.H.Xie M.Schmidt R.E.Trinkaus K.Song S.K.2007. Diffusion tensor imaging predicts hyperacute spinal cord injury severityJ. Neurotrauma24979-990. Loy, D.N., Kim, J.H., Xie, M., Schmidt, R.E., Trinkaus, K., and Song, S.K. (2007). Diffusion tensor imaging predicts hyperacute spinal cord injury severity. J. Neurotrauma 24, 979–990.
Loy D.N.Magnuson D.S.Zhang Y.P.Onifer S.M.Mills M.D.Cao Q.L.Darnall J.B.Fajardo L.C.Burke D.A.Whittemore S.R.2002a. Functional redundancy of ventral spinal locomotor pathwaysJ. Neurosci.22315-323. Loy, D.N., Magnuson, D.S., Zhang, Y.P., Onifer, S.M., Mills, M.D., Cao, Q.L., Darnall, J.B., Fajardo, L.C., Burke, D.A., and Whittemore, S.R. (2002a). Functional redundancy of ventral spinal locomotor pathways. J. Neurosci. 22, 315–323.
Loy D.N.Talbott J.F.Onifer S.M.Mills M.D.Burke D.A.Dennison J.B.Fajardo L.C.Magnuson D.S.Whittemore S.R.2002b. Both dorsal and ventral spinal cord pathways contribute to overground locomotion in the adult ratExp. Neurol.177575-580. Loy, D.N., Talbott, J.F., Onifer, S.M., Mills, M.D., Burke, D.A., Dennison, J.B., Fajardo, L.C., Magnuson, D.S., and Whittemore, S.R. (2002b). Both dorsal and ventral spinal cord pathways contribute to overground locomotion in the adult rat. Exp. Neurol. 177, 575–580.
Ma M.Basso D.M.Walters P.Stokes B.T.Jakeman L.B.2001. Behavioral and histological outcomes following graded spinal cord contusion injury in the C57Bl/6 mouseExp. Neurol.169239-254. Ma, M., Basso, D.M., Walters, P., Stokes, B.T., and Jakeman, L.B. (2001). Behavioral and histological outcomes following graded spinal cord contusion injury in the C57Bl/6 mouse. Exp. Neurol. 169, 239–254.
Madi S.Hasan K.M.Narayana P.A.2005. Diffusion tensor imaging of in vivo and excised rat spinal cord at 7 T with an icosahedral encoding schemeMagn. Reson. Med.53118-125. Madi, S., Hasan, K.M., and Narayana, P.A. (2005). Diffusion tensor imaging of in vivo and excised rat spinal cord at 7 T with an icosahedral encoding scheme. Magn. Reson. Med. 53, 118–125.
Maxwell W.L.1996. Histopathological changes at central nodes of Ranvier after stretch-injuryMicrosc. Res. Tech.34522-535. Maxwell, W.L. (1996). Histopathological changes at central nodes of Ranvier after stretch-injury. Microsc. Res. Tech. 34, 522–535.
McEwen M.L.Springer J.E.2006. Quantification of locomotor recovery following spinal cord contusion in adult ratsJ. Neurotrauma231632-1653. McEwen, M.L., and Springer, J.E. (2006). Quantification of locomotor recovery following spinal cord contusion in adult rats. J. Neurotrauma 23, 1632–1653.
Miyanji F.Furlan J.C.Aarabi B.Arnold P.M.Fehlings M.G.2007. Acute cervical traumatic spinal cord injury: MR imaging findings correlated with neurologic outcome—prospective study with 100 consecutive patientsRadiology243820-827. Miyanji, F., Furlan, J.C., Aarabi, B., Arnold, P.M., and Fehlings, M.G. (2007). Acute cervical traumatic spinal cord injury: MR imaging findings correlated with neurologic outcome—prospective study with 100 consecutive patients. Radiology 243, 820–827.
Narayana P.Abbe R.Liu S.J.Johnston D.1999. Does loss of gray- and white-matter contrast in injured spinal cord signify secondary injury? In vivo longitudinal MRI studiesMagn. Reson. Med.41315-320. Narayana, P., Abbe, R., Liu, S.J., and Johnston, D. (1999). Does loss of gray- and white-matter contrast in injured spinal cord signify secondary injury? In vivo longitudinal MRI studies. Magn. Reson. Med. 41, 315–320.
Nishi R.A.Liu H.Chu Y.Hamamura M.Su M.Y.Nalcioglu O.Anderson A.J.2007. Behavioral, histological, and ex vivo magnetic resonance imaging assessment of graded contusion spinal cord injury in miceJ. Neurotrauma24674-689. Nishi, R.A., Liu, H., Chu, Y., Hamamura, M., Su, M.Y., Nalcioglu, O., and Anderson, A.J. (2007). Behavioral, histological, and ex vivo magnetic resonance imaging assessment of graded contusion spinal cord injury in mice. J. Neurotrauma 24, 674–689.
Pierpaoli C.Basser P.J.1996. Toward a quantitative assessment of diffusion anisotropyMagn. Reson. Med.36893-906. Pierpaoli, C., and Basser, P.J. (1996). Toward a quantitative assessment of diffusion anisotropy. Magn. Reson. Med. 36, 893–906.
Rasband W.S.1997–2005. Image processing and Analysis in Java. Rasband, W.S. (1997–2005). Image processing and Analysis in Java.
Schucht P.Raineteau O.Schwab M.E.Fouad K.2002. Anatomical correlates of locomotor recovery following dorsal and ventral lesions of the rat spinal cordExp. Neurol.176143-153. Schucht, P., Raineteau, O., Schwab, M.E., and Fouad, K. (2002). Anatomical correlates of locomotor recovery following dorsal and ventral lesions of the rat spinal cord. Exp. Neurol. 176, 143–153.
Schwartz E.D.Hackney D.B.2003. Diffusion-weighted MRI and the evaluation of spinal cord axonal integrity following injury and treatmentExp. Neurol.184570-589. Schwartz, E.D., and Hackney, D.B. (2003). Diffusion-weighted MRI and the evaluation of spinal cord axonal integrity following injury and treatment. Exp. Neurol. 184, 570–589.
Schwartz E.D.Shumsky J.S.Wehrli S.Tessler A.Murray M.Hackney D.B.2003. Ex vivo MR determined apparent diffusion coefficients correlate with motor recovery mediated by intraspinal transplants of fibroblasts genetically modified to express BDNFExp. Neurol.18249-63. Schwartz, E.D., Shumsky, J.S., Wehrli, S., Tessler, A., Murray, M., and Hackney, D.B. (2003). Ex vivo MR determined apparent diffusion coefficients correlate with motor recovery mediated by intraspinal transplants of fibroblasts genetically modified to express BDNF. Exp. Neurol. 182, 49–63.
Shanmuganathan K.Gullapalli R.P.Zhuo J.Mirvis S.E.2008. Diffusion tensor MR imaging in cervical spine traumaAJNR Am. J. Neuroradiol.29655-659. Shanmuganathan, K., Gullapalli, R.P., Zhuo, J., and Mirvis, S.E. (2008). Diffusion tensor MR imaging in cervical spine trauma. AJNR Am. J. Neuroradiol. 29, 655–659.
Shepard M.J.Bracken M.B.1999. Magnetic resonance imaging and neurological recovery in acute spinal cord injury: observations from the National Acute Spinal Cord Injury Study 3Spinal Cord37833-837. Shepard, M.J., and Bracken, M.B. (1999). Magnetic resonance imaging and neurological recovery in acute spinal cord injury: observations from the National Acute Spinal Cord Injury Study 3. Spinal Cord 37, 833–837.
Song S.K.Sun S.W.Ju W.K.Lin S.J.Cross A.H.Neufeld A.H.2003. Diffusion tensor imaging detects and differentiates axon and myelin degeneration in mouse optic nerve after retinal ischemiaNeuroimage201714-1722. Song, S.K., Sun, S.W., Ju, W.K., Lin, S.J., Cross, A.H., and Neufeld, A.H. (2003). Diffusion tensor imaging detects and differentiates axon and myelin degeneration in mouse optic nerve after retinal ischemia. Neuroimage 20, 1714–1722.
Song S.K.Sun S.W.Ramsbottom M.J.Chang C.Russell J.Cross A.H.2002. Dysmyelination revealed through MRI as increased radial (but unchanged axial) diffusion of waterNeuroimage171429-1436. 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.
Stejskal E.OTanner J.E.1965. Spin echoes in the presence of a time-dependent field gradientJ. Chem. Phys.42288-292. Stejskal, E.O, and Tanner, J.E. (1965). Spin echoes in the presence of a time-dependent field gradient. J. Chem. Phys. 42, 288–292.
Sun S.W.Liang H.F.Trinkaus K.Cross A.H.Armstrong R.C.Song S.K.2006. Noninvasive detection of cuprizone induced axonal damage and demyelination in the mouse corpus callosumMagn. Reson. Med.55302-308. Sun, S.W., Liang, H.F., Trinkaus, K., Cross, A.H., Armstrong, R.C., and Song, S.K. (2006). Noninvasive detection of cuprizone induced axonal damage and demyelination in the mouse corpus callosum. Magn. Reson. Med. 55, 302–308.
Yeatman J.D.Ben-Shachar M.Bammer R.Feldman H.M.2009. Using diffusion tensor imaging and fiber tracking to characterize diffuse perinatal white matter injury: a case reportJ. Child. Neurol.24795-800. Yeatman, J.D., Ben-Shachar, M., Bammer, R., and Feldman, H.M. (2009). Using diffusion tensor imaging and fiber tracking to characterize diffuse perinatal white matter injury: a case report. J. Child. Neurol. 24, 795–800.
You S.W.Chen B.Y.Liu H.L.Lang B.Xia J.L.Jiao X.Y.Ju G.2003. Spontaneous recovery of locomotion induced by remaining fibers after spinal cord transection in adult ratsRestor. Neurol. Neurosci.2139-45. You, S.W., Chen, B.Y., Liu, H.L., Lang, B., Xia, J.L., Jiao, X.Y., and Ju, G. (2003). Spontaneous recovery of locomotion induced by remaining fibers after spinal cord transection in adult rats. Restor. Neurol. Neurosci. 21, 39–45.
Information & Authors
Information
Published In
Copyright
Copyright 2010, Mary Ann Liebert, Inc.
History
Published online: 29 March 2010
Published in print: March 2010
Published ahead of production: 14 December 2009
Topics
Authors
Author Disclosure Statement
No conflicting financial interests exist.
Metrics & Citations
Metrics
Citations
Export Citation
Export citation
Select the format you want to export the citations of this publication.
View Options
Get Access
Access content
To read the fulltext, please use one of the options below to sign in or purchase access.⚠ Society Access
If you are a member of a society that has access to this content please log in via your society website and then return to this publication.