Anatomical and functional outcomes following a precise, graded, dorsal laceration spinal cord injury in C57BL/6 mice

Journal of Neurotrauma

Volumn 26, Issue 1, 2009, Pages 1-15

  Hill, Rachel L ^a,b   Zhang, Yi Ping ^a,b   Burke, Darlene A ^b   Devries, William H ^a,b,c   Zhang, Yongjie ^a,b   Magnuson, David S K ^a,b   Whittemore, Scott R ^a,b   Shields, Christopher B ^a,b  

^a University of Louisville School of Medicine   (United States)

^b UNIVERSITY OF LOUISVILLE   (United States)

^c NANJING MEDICAL UNIVERSITY   (China)

Author keywords

Behavioral assessments; Locomotor function; Models of injury; Recovery; Traumatic spinal cord injury

Indexed keywords

ACCURACY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; C57BL 6 MOUSE; CONTROLLED STUDY; CONVALESCENCE; ELECTROPHYSIOLOGY; EVOKED RESPONSE; FUNCTIONAL ASSESSMENT; FUNCTIONAL DISEASE; HISTOPATHOLOGY; LACERATION; LAMINECTOMY; MOTOR PERFORMANCE; MOUSE; NONHUMAN; OUTCOME ASSESSMENT; PATHOPHYSIOLOGY; POSTOPERATIVE CARE; SENSORIMOTOR FUNCTION; SENSORY EVALUATION; SPINAL CORD INJURY; SURGICAL TECHNIQUE;

ANIMALS; AXOTOMY; DISABILITY EVALUATION; DISEASE MODELS, ANIMAL; EFFERENT PATHWAYS; EVOKED POTENTIALS, MOTOR; FEMALE; GAIT DISORDERS, NEUROLOGIC; HINDLIMB; LOCOMOTION; MICE; MICE, INBRED C57BL; MOVEMENT DISORDERS; NEURONAL PLASTICITY; OUTCOME ASSESSMENT (HEALTH CARE); PREDICTIVE VALUE OF TESTS; RECOVERY OF FUNCTION; REPRODUCIBILITY OF RESULTS; SEVERITY OF ILLNESS INDEX; SPINAL CORD; SPINAL CORD INJURIES; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 59849088007     PISSN: 08977151     EISSN: None     Source Type: Journal    
DOI: 10.1089/neu.2008.0543     Document Type: Article

References (75)

1. Allen, A.R. (1911). Surgery of experimental lesion of spinal cord equivalent to crush injury of fracture dislocation of spinal column: a preliminary report. JAMA 57, 878-880.
2. Balantine, J.D. (1978). Pathology of experimental spinal cord trauma. I. The necrotic lesion as a function of vascular injury. Lab. Invest. 39, 236-253.
3. Bartholdi, D., and Schwab, M.E. (1997). Expression of pro-inflammatory cytokine and chemokine mRNA upon experimental spinal cord injury in mouse: an in situ hybridization study. Euro. J. Neurosci. 9, 1422-1438.
4. Basso, D.M., and Fisher, L.C. (2003) The Basso Mouse Scale for Locomotion (BMS) is a more sensitive indicator of recovery than the BBB scale in mice with spinal cord injury. In Society for Neuroscience Abstract.
5. 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.
6. Beattie, M.S., Stokes, B.T., and Bresnahan, J.C. (1988). Experimental spinal cord injury: strategies for acute and chronic intervention based on anatomic, physiologic, and behavioral studies, in: Pharmacological Approaches to the Treatment of Brain and Spinal Cord Injury. D. Stein, and B. Sabel (eds), Plenum Publishing: New York, pps. 43-74.
7. Beaumont, E., Onifer, S.M., Reed, W.R., and Magnuson, D.S.K. (2006). Magnetically evoked inter-enlargement response: An assessment of ascending propriospinal fibers following spinal cord injury. Exp. Neurol. 201, 428-440.
8. 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.
9. Blight, A.R. (1983). Cellular morphology of chronic spinal cord injury in the cat: analysis of myelinated axons by line-sampling. Neuroscience 10, 521-543.
10. Bresnahan, J.C., Beattie, M.S., Todd, F.D.I., and Noyes, D.H. (1987). A behavioral and anatomical analysis of spinal cord injury produced by a feedback-controlled impaction device. Exp. Neurol. 95, 548-570.
11. Bresnahan, J.C., King, J.S., Martin, G.F., and Yashon, D. (1976). A neuroanatomical analysis of spinal cord injury in the rhesus monkey (Macaca mulatta). J. Neurol. Sci. 28, 521-542.
12. Bunge, R.P., Puckett, W.R., Becerra, J.L., Marcillo, A., and Quencer, R.M. (1993). Observations on the pathology of human spinal cord injury: a review and classification of 22 new cases with details from a case of chronic cord compression with extensive focal demyelination, in: Advances in Neurology. F.J. Seil (ed), Raven Press: New York, pps. 75-89.
13. Cao, Q., Zhang, Y.P., Iannotti, C., Devries, W.H., Xu, X.-M., Shields, C.B., and Whittemore, S.R. (2005). Functional and electrophysiological changes after graded traumatic spinal cord injury in adult rat. Exp. Neurol. 2005 (Suppl. 1), S3-S16.
14. Constantini, S., and Young, W. (1994). The effects of methylprednisolone and the ganglioside GM1 on acute spinal cord injury in rats. J. Neurosurg. 80, 97-111.
15. De Medinacelli, L., Freed, W.J., and Wyatt, R.J. (1982). An index of the functional condition of rat sciatic nerve based on measurements made from walking tracks. Exp. Neurol. 77, 634-643.
16. Eidelberg, E., Nguyen, L.H., and Deza, L.D. (1986). Recovery of locomotor function after hemisection of the spinal cord of cats. Brain Res. Bull. 16, 507-515.
17. Engesser-Cesar, C., Anderson, A.J., Basso, D.M., Edgerton, V.R., and Cotman, C.W. (2005). Voluntary wheel running improves recovery from a moderate spinal cord injury. J. Neurotrauma 22, 157-171.
18. Farooque, M. (2000). Spinal cord compression injury in the mouse: presentation of a model including assessment of motor dysfunction. Acta Neuropathology 100, 13-22.
19. Fehlings, M.G., and Tator, C.H. (1988). A review of experimental models of acute spinal cord injury, in: Spinal Cord Dysfunction: Assessment. L. Illis (ed), Oxford University Press: New York, pps. 3-33.
20. Fehlings, M.G., and Tator, C.H. (1995). The relationship among the severity of spinal cord injury, residual neurological function, axon counts, and counts of retrogradely labeled neurons after experimental spinal cord injury. Exp. Neurol. 132, 220-228.
21. Fiore, C., Inman, D.M., Hirose, S., Noble, L.J., Igarashi, T., and Compagnone, N.A. (2004). Treatment with the neurosteroid dehydroepiandrosterone (DHEA) promotes recovery of motor behavior after moderate contusive SCI in the mouse. J. Neurosci. Res. 75, 391-400.
22. Fujiki, M., Zhang, Z., Guth, L., and Steward, O. (1996). Genetic influences on cellular reactions to spinal cord injury: activation of macrophages/microglia and astrocytes is delayed in mice carrying a mutation (WldS) that causes delayed Wallerian degeneration. J. Comp. Neurol. 371, 469-484.
23. Ghasemlou, N., Kerr, B.J., and David, S. (2005). Tissue displacement and impact force are important contributors to outcome after spinal cord contusion injury. Exp. Neurol. 196, 9-17.
24. Goldberger, M.E., Murray, M., and Tessler, A. (1993). Sprouting and regeneration in the spinal cord. Their roles in recovery of function after spinal cord injury, in: Neuroregeneration. A. Gorio (ed), Raven: New York, pps. 241-264.
25. Goldberger, M.E. (1991). The use of behavioral methods to predict spinal cord plasticity. J. Restor. Neurol. Neurosci. 2, 339-350.
26. Grant, G. (1993). Projection patterns of primary sensory neurons studied by transganglionic methods: Somatotopy and target-related organization. Brain Res. Bull. 30, 199-208.
27. Gruner, J.A. (1992). A monitored contusion model of spinal cord injury in the rat. J. Neurotrauma 9, 123-136.
28. Hamers, F.P.T., Lankhorst, A.J., Jan Van Laar, T., Veldhuis, W.B., and Gispen, W.H. (2001). Automated quantitative gait analysis during overground locomotion in the rat: Its application to spinal cord contusion and transection injuries. J. Neurotrauma 18, 187-201.
29. Hargreaves, K., Dubner, R., Brown, F., Flores, C., and Joris, J. (1988). A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 32, 77-88.
30. Helgren, M.E., and Goldberger, M.E. (1993). The recovery of postural reflexes and locomotion following low thoracic hemisection in adult cats involves compensation by undamaged primary afferent pathways. Exp. Neurol. 123, 17-34.
31. Huang, P.P., and Young, W. (1994). The effects of arterial blood gas values on lesion volumes in a graded rat spinal cord contusion model. J. Neurotrauma 11, 547-562.
32. Inman, D.M., and Steward, O. (2003b). Ascending sensory, but not other long-tract axons, regenerate into the connective tissue matrix that forms at the site of a spinal cord injury in mice. J. Comp. Neurol. 462, 431-449.
33. Inman, D.M., and Steward, O. (2003a). Physical size does not determine the unique histopathological response seen in the injured mouse spinal cord. J. Neurotrauma 20, 33-42.
34. Inman, D.M., Guth, L., and Steward, O. (2002). Genetic influences on secondary degeneration and wound healing following spinal cord injury in various strains of mice. J. Comp. Neurol. 451, 225-235.
35. Jacob, J.E., Pniak, A., Weaver, L.C., and Brown, A. (2001). Autonomic dysreflexia in a mouse model of spinal cord injury. Neuroscience 108, 687-693.
36. 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 the mouse. J. Neurotrauma 17, 299-319.
37. Joshi, M., and Fehlings, M.G. (2002b). Development and characterization of a novel, graded model of clip compressive spinal cord injury in the mouse: Part 1. Clip design, behavioral outcomes, and histopathology. J. Neurotrauma 19, 175-190.
38. Joshi, M., and Fehlings, M.G. (2002a). Development and characterization of a novel, graded model of clip compressive spinal cord injury in the mouse: Part 2. Relationships between axonal tracts, residual tissue and locomotor recovery. J. Neurotrauma 19, 191-203.
39. Kakulas, B.A. (1999). A review of neuropathology of human spinal cord injury with emphasis on special features. J. Spinal Cord Med. 22, 119-124.
40. Krenz, N.R., and Weaver, L.C. (1998). Sprouting of primary afferent fibers after spinal cord transection in the rat. Neuroscience 85, 443-458.
41. Kuhn, P.L., and Wrathall, J.R. (1998). A mouse model of graded contusive spinal cord injury. J. Neurotrauma 15, 125-140.
42. Kunkel-Bagden, E., Dai, H.N., and Bregman, B.S. (1993). Methods to assess the development and recovery of locomotor function after spinal cord injury in rats. Exp. Neurol. 119, 153-164.
43. Loy, D.N., Magnuson, D.S.K., Zhang, Y.P., Onifer, S.M., Mills, M.D., Cao, Q., 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.
44. Loy, D.N., Talbott, J.F., Onifer, S.M., Mills, M.D., Burke, D.A., Dennison, J.B., Fajardo, L.C., Magnuson, D.S.K., 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.
45. Ma, M., Basso, D.M., Walters, P., Strokes, 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.
46. Maxwell, D., and Rethelyi, R. (1987). Ultrastructure and synaptic connections of cutaneous afferent fibres in the spinal cord. Trends Neurosci. 10, 117-122.
47. Metz, G.A.S., Merkler, D., Dietz, V., Schwab, M.E., and Fouad, K. (2000). Efficient testing of motor function in spinal cord injured rats. J. Neurotrauma 17, 1-17.
48. Muir, G.D., and Webb, A.A. (2000). Assessment of behavioral recovery following spinal cord injury in rats. Euro. J. Neurosci. 12, 3079-3086.
49. Noble, L.J., and Wrathall, J.R. (1985). Spinal cord contusion in the rat: morphometric analyses of alterations in the spinal cord. Exp. Neurol. 88, 135-149.
50. Plemel, J.R., Duncan, G., Chen, K.W., Shannon, C., Park, S., Sparling, J.S., and Tetzlaff, W. (2008). A graded forceps crush spinal cord injury model in mice. J. Neurotrauma 25, 350-370.
51. Ramer, L.M., Ramer, M.S., and Steeves, J.D. (2005). Setting the stage for functional repair of spinal cord injuries: a cast of thousands. Spinal Cord 43, 134-161.
52. Scheff, S.W., Rabchevsky, A.G., Fugaccia, I., Main, J.A., Lumpp, J., and James, E. (2003). Experimental modeling of spinal cord injury: characterization of a force-defined injury device. J. Neurotrauma 20, 179-193.
53. 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.
54. Schwab, J.M., Brechtel, K., Mueller, C.-A., Failli, V., Kaps, H.-P., Tuli, S.K., and Schluesener, H.J. (2006). Experimental strategies to promote spinal cord regeneration - an integrative perspective. Prog. Neurobiol. 78, 91-116.
55. Seitz, A., Aglow, E., and Heber-Katz, E. (2002). Recovery from spinal cord injury: A new transection model in the C57Bl/6 mouse. J. Neurosci. Res. 67, 337-345.
56. Seki, T., Hida, K., Tada, M., Koyanagi, I., and Iwasaki, Y. (2002). Graded contusion model of the mouse spinal cord using a pneumatic impact device. Neurosurgery 50, 1075-1082.
57. Sivasankaran, R., Pei, J., Wang, K.C., Zhang, Y.P., Shields, C.B., Xu, X.-M., and He, Z. (2004). PKC mediates inhibitory effects of myelin and chondroitin sulfate proteoglycans on axonal regeneration. Nature Neurosci. 7, 261-268.
58. Sroga, J.M., Jones, T.B., Kigerl, K.A., McGaughy, V.M., and Popovich, P.G. (2003). Rats and mice exhibit distinct inflammatory reactions after spinal cord injury. J. Comp. Neurol. 462, 223-240.
59. Steward, O., Schauwecker, P.E., Guth, L., Zhang, Z., Fujiki, M., Inman, D.M., Wrathall, J.R., Kempermann, G., Gage, F.H., Saatman, K.E., Raghupathi, R., and McIntosh, T.K. (1999). Genetic approaches to neurotrauma research: opportunities and potential pitfalls of murine models. Exp. Neurol. 157, 19-42.
60. Steward, O., Zheng, B., Ho, C., Anderson, K., and Tessier-Lavigne, M. (2004). The dorsolateral corticospinal tract in mice: an alternative route for corticospinal input to caudal segments following dorsal column lesions. J. Comparative Neurol. 472, 463-477.
61. Stokes, B.T. (1992). Experimental spinal cord injury: a dynamic and verifiable injury device. J. Neurotrauma 9, 129-134.
62. Taoka, Y., and Okajima, K. (1998). Spinal cord injury in the rat. Prog. Neurobiol. 56, 341-358.
63. Trojanowski, J.Q., Gonatas, J.O., and Gonatas, N.K. (1982). Horseradish peroxidase (HRP) conjugates of cholera toxin and lectins are more sensitive retrogradely transported markers than free HRP. Brain Res. 231, 33-50.
64. Wan, X.-C.S., Trojanowski, J.Q., and Gonatas, J.O. (1982). Cholera toxin and wheat germ agglutinin conjugates as neuroanatomical probes: their uptake and clearance, transganglionic and retrograde transport and sensitivity. Brain Res. 243, 215-224.
65. Whishaw, I.Q., Pellis, S.M., and Pellis, V.C. (1992). A behavioral study of the contributions of cells and fibers of passage in the red nucleus of the rat to postural righting, skilled movements, and learning. Behav. Brain Res. 52, 29-44.
66. White, F.A., and Kocsis, J.D. (2002). A-fiber sprouting in spinal cord dorsal horn is attentuated by proximal nerve stump encapsulation. Exp. Neurol. 177, 385-395.
67. Willis, W.J., and Coggeshall, I.R. (1991). Dorsal root ganglion cells and their processes, in: Sensory Mechanisms of the Spinal Cord. Plenum: New York, pps. 49-78.
68. Willis, W.J., and Westlund, K.N. (1997). Neuroanatomy of the pain system and of the pathways that modulate pain. J. Clin. Neurophysiol. 14, 2-31.
69. Wong, S.T., Atkinson, B.A., and Weaver, L.C. (2000). Confocal microscopic analysis reveals sprouting of primary afferent fibers in rat dorsal horn after spinal cord injury. Neurosci. Lett. 296, 65-88.
70. Wrathall, J.R., Pettegrew, R.K., and Harvey, F. (1985). Spinal cord contusion in the rat: production of graded, reproducible, injury groups. Exp. Neurol. 88, 108-122.
71. Zang, D.W., and Cheema, S.S. (2003). Leukemia inhibitory factor promotes recovery of locomotor function following spinal cord injury in the mouse. J. Neurotrauma 20, 1215-1222.
72. Zhang, Y.P., Iannotti, C., Shields, L., Han, E., Burke, Y., Xu, D.A., and Shields, C.B. (2004). Dural closure, cord approximation, and clot removal: enhancement of tissue sparing in a novel laceration spinal cord injury model. J. Neurosurg. Spine 100, 343-352.
73. Zhang, Y.P., Shields, L.B.E., Zhang, Y., Pei, J., Xu, X.-M., Hoskins, R., Cai, J., Qiu, M.S., Magnuson, D.S.K., Burke, D.A., and Shields, C.B. (2007b). Use of magnetic stimulation to elicit motor evoked potentials, somatosensory evoked potentials, and H-reflexes in non-sedated rodents. J. Neurosci. Methods 165, 9-17.
74. Zhang, Y.P., Shields, L., Chekmenev, S., Dincman, T., Zhang, Y., Zheng, Y., Smith, R., Devries, W.H., Hu, X., Magnuson, D.S.K., Whittemore, S.R., and Shields, C.B. (2007a). Combined assessment to discriminate small functional differences following spinal cord contusion based on precise vertebral stabilization and tissue displacement. J. Neurotrauma (manuscript submitted).
75. Zhang, Z., Fujiki, M., Guth, L., and Steward, O. (1996). Genetic influences on cellular reactions to spinal cord injury: A wound healing response in normal mice is impaired in mice carrying a mutation (WldS) that causes delayed Wallerian degeneration. J. Comp. Neurol. 371, 485-495.