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The Journal of Neuroscience, March 11, 2009, 29(10):3160-3171; doi:10.1523/JNEUROSCI.3941-08.2009

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Neurobiology of Disease
Diffusion Tensor Magnetic Resonance Imaging of Wallerian Degeneration in Rat Spinal Cord after Dorsal Root Axotomy

Jiangyang Zhang,¹ Melina Jones,² Cynthia A. DeBoy,² Daniel S. Reich,^1,2 Jonathan A. D. Farrell,^1,3,7 Paul N. Hoffman,^2,4 John W. Griffin,² Kazim A. Sheikh,² Michael I. Miller,^5,6 Susumu Mori,^1,7 and Peter A. Calabresi²

¹Russel H. Morgan Department of Radiology and Radiological Science, Departments of ²Neurology, ³Biophysics and Biophysical Chemistry, ⁴Ophthalmology, and ⁵Biomedical Engineering, Johns Hopkins University School of Medicine, Baltimore, Maryland 21205, ⁶Center of Imaging Science, Johns Hopkins University, Baltimore, Maryland 21218, and ⁷F. M. Kirby Research Center for Functional Brain Imaging, Kennedy Krieger Institute, Baltimore, Maryland 21205

Correspondence should be addressed to either of the following: Dr. Jiangyang Zhang, Johns Hopkins University School of Medicine, Traylor Building, Room #208, 720 Rutland Avenue, Baltimore, MD 21205, Email: jzhang3{at}jhmi.edu; or Dr. Peter A. Calabresi, Johns Hopkins Hospital, Pathology Building, Suite 627, 600 North Wolfe Street, Baltimore, MD 21287, Email: calabresi{at}jhmi.edu

Diffusion tensor imaging (DTI) and immunohistochemistry were used to examine axon injury in the rat spinal cord after unilateral L₂–L₄ dorsal root axotomy at multiple time points (from 16 h to 30 d after surgery). Three days after axotomy, DTI revealed a lesion in the ipsilateral dorsal column extending from the lumbar to the cervical cord. The lesion showed significantly reduced parallel diffusivity and increased perpendicular diffusivity at day 3 compared with the contralateral unlesioned dorsal column. These findings coincided with loss of phosphorylated neurofilaments, accumulation of nonphosphorylated neurofilaments, swollen axons and formation of myelin ovoids, and no clear loss of myelin (stained by Luxol fast blue and 2'-3'-cyclic nucleotide 3'-phosphodiesterase). At day 30, DTI of the lesion continued to show significantly decreased parallel diffusivity. There was a slow but significant increase in perpendicular diffusivity between day 3 and day 30, which correlated with gradual clearance of myelin without further significant changes in neurofilament levels. These results show that parallel diffusivity can detect axon degeneration within 3 d after injury. The clearance of myelin at later stages may contribute to the late increase in perpendicular diffusivity, whereas the cause of its early increase at day 3 may be related to changes associated with primary axon injury. These data suggest that there is an early imaging signature associated with axon transections that could be used in a variety of neurological disease processes.

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Received Aug. 18, 2008; revised Jan. 27, 2009; accepted Jan. 30, 2009.

Correspondence should be addressed to either of the following: Dr. Jiangyang Zhang, Johns Hopkins University School of Medicine, Traylor Building, Room #208, 720 Rutland Avenue, Baltimore, MD 21205, Email: jzhang3{at}jhmi.edu; or Dr. Peter A. Calabresi, Johns Hopkins Hospital, Pathology Building, Suite 627, 600 North Wolfe Street, Baltimore, MD 21287, Email: calabresi{at}jhmi.edu

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