Characterization of a graded cervical hemicontusion spinal cord injury model in adult male rats

Journal of Neurotrauma

Volumn 27, Issue 11, 2010, Pages 2091-2106

  Dunham, Kelly A ^a   Siriphorn, Akkradate ^b   Chompoopong, Supin ^b   Floyd, Candace L ^a  

^a University of Alabama at Birmingham   (United States)

^b MAHIDOL UNIVERSITY   (Thailand)

Author keywords

forepaw function; gliosis; gray matter sparing; white matter sparing

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR; CERVICAL SPINE; CONTROLLED STUDY; CONTUSION; FORCE; FORELIMB; GAIT; GLIOSIS; HISTOLOGY; INJURY SEVERITY; LOCOMOTION; MALE; NERVE CELL; NONHUMAN; RAT; SKILL; SPINAL CORD INJURY; TASK PERFORMANCE; WHITE MATTER;

ANIMALS; CELL COUNT; CONTUSIONS; DISEASE MODELS, ANIMAL; FLUORESCENCE; FORELIMB; FUNCTIONAL LATERALITY; GLIAL FIBRILLARY ACIDIC PROTEIN; GLIOSIS; HEALTH; IMMUNOHISTOCHEMISTRY; LOCOMOTION; MALE; MOTOR SKILLS; MYELIN BASIC PROTEINS; NEUROGLIA; NEURONS; OXAZINES; PSYCHOMOTOR PERFORMANCE; RATS; RATS, SPRAGUE-DAWLEY; RECOVERY OF FUNCTION; SPINAL CORD; SPINAL CORD INJURIES;

EID: 78649339239     PISSN: 08977151     EISSN: None     Source Type: Journal    
DOI: 10.1089/neu.2010.1424     Document Type: Article

References (64)

1. Alaverdashvili, M., and Whishaw, I. (2008). Motor cortex stroke impairs individual digit movement in skilled reaching by the rat. Eur. J. Neurosci. 28, 311-322.
2. Allred, R., Adkins, D., Woodlee, M., Husbands, L., Maldonado, M., Kane, J., Schallert, T., and Jones, T. (2008). The vermicelli handling test: a simple quantitative measure of dexterous forepaw function in rats. J. Neurosci. Methods 170, 229-244.
3. Anderson, T., and Stokes, B. (1992). Experimental models for spinal cord injury research: physical and physiological considerations. J. Neurotrauma 9, S135-S142.
4. Anderson, K., Gunawan, A., and Steward, O. (2005). Quantitative assessment of forelimb motor function after cervical spinal cord injury in rats: relationship to the corticospinal tract. Exp. Neurol. 194, 161-174.
5. Anderson, K., Gunawan, A., and Steward, O. (2007). Spinal pathways involved in the control of forelimb motor function in rats. Exp. Neurol. 206, 318-331.
6. Anderson, K., Sharp, K., and Steward, O. (2009b). Bilateral cervical contusion spinal cord injury in rats. Exp. Neurol. 220, 9-22.
7. Anderson, K., Sharp, K., Hofstadter, M., Irvine, K., Murray, M., and Steward, O. (2009a). Forelimb locomotor assessment scale (FLAS): novel assessment of forelimb dysfunction after cervical spinal cord injury. Exp. Neurol. 220, 23-33.
8. Basso, D. (2000). Neuroanatomical substrates of functional recovery after experimental spinal cord injury: implications of basic science research for human spinal cord injury. Phys. Ther. 80, 808-817.
9. Baussart, B., Stamegna, J., Polentes, J., Tadie, M., and Gauthier, P. (2006). A new model of upper cervical spinal contusion inducing a persistent unilateral diaphragmatic deficit in the adult rat. Neurobiol. Dis. 22, 562-574.
10. Behrmann, D., Bresnahan, J., Beattie, M., and Shah, B. (1992). Spinal cord injury produced by consistent mechanical displacement of the cord in rats: behavioral and histologic analysis. J. Neurotrauma 9, 197-217.
11. Bunge, R., Puckett, W., Becerra, J., Marcillo, A., and Quencer, R. (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. Adv. Neurol. 59, 75-89.
12. Collazos-Castro, J., Soto, V., Gutierrez-Davila, M., and Nieto-Sampedro, M. (2005). Motoneuron loss associated with chronic locomotion impairments after spinal cord contusion in the rat. J. Neurotrauma 22, 544-558.
13. Chaovipoch, P., Jelks, K., Gerhold, L., West, E., Chongth-ammakun, S., and Floyd, C. (2006). 17Beta-estradiol is protective in spinal cord injury in post-and pre-menopausal rats. J. Neurotrauma 23, 830-852.
14. De Rivero, V., Marcillo, A., Nonner, D., Dietrich, W., and Keane, R. (2009). Neuroprotective effects of bone morphogenetic protein 7 (BMP7) treatment after spinal cord injury. Neurosci. Lett. 465, 226-229.
15. Engesser-Cesar, C., Anderson, A., Basso, D., Edgerton, V., and Cotman, C. (2005). Voluntary wheel running improves recovery from a moderate spinal cord injury. J. Neurotrauma 22, 157-171.
16. El-Bohy, A., Schrimsher, G., Reier, P., and Goshgarian, H. (1998). Quantitative assessment of respiratory function following contusion injury of the cervical spinal cord. Exp. Neurol. 150, 143-152.
17. Fuller, D., Doperalski, N., Dougherty, B., Sandhu, M., Bolser, D., and Reier, P. (2008). Modest spontaneous recovery of ventilation following chronic high cervical hemisection in rats. Exp. Neurol. 211, 97-106.
18. Fuller, D., Sandhu, M., Doperalski, N., Lane, M., White, T., Bishop, M., and Reier, P. (2009). Graded unilateral cervical spinal cord injury and respiratory motor recovery. Respir. Physiol. Neurobiol. 165, 245-253.
19. Gabriel, A., Marcus, M., Honig, W., Walenkamp, G., and Joos-ten, E. (2007). The CatWalk method: a detailed analysis of behavioral changes after acute inflammatory pain in the rat. J. Neurosci. Methods 163, 9-16.
20. Gensel, J., Tovar, C., Hamers, F., Deibert, R., Beattie, M., and Bresnahan, J. (2006). Behavioral and histological characterization of unilateral cervical spinal cord contusion injury in rats. J. Neurotrauma 23, 36-54.
21. Ghosh, A., Sydekum, E., Haiss, F., Peduzzi, S., Zorner, B., Schneider, R., Baltes, C., Rudin, M., Weber, B., and Schwab, M. (2009). Functional and anatomical reorganization of the sensory-motor cortex after incomplete spinal cord injury in adult rats. J. Neurosci. 29, 12210-12219.
22. Hamers, F., Koopmans, G., and Joosten, E. (2006). CatWalk-assisted gait analysis in the assessment of spinal cord injury. J. Neurotrauma 23, 537-548.
23. Hermer-Vazquez, L., Hermer-Vazquez, R., Moxon, K., Kuo, K., Viau, V., Zhan, Y., and Chapin, J. (2004). Distinct temporal activity patterns in the rat M1 and red nucleus during skilled versus unskilled limb movement. Behav. Brain Res. 150, 93-107.
24. Jones, T., and Schallert, T. (1994). Use-dependent growth of pyramidal neurons after neocortical damage. J. Neurosci. 14, 2140-2152.
25. Kachadroka, S., Hall, A., Niedzielko, T., Chongthammakun, S., and Floyd, C. (2010). Effect of endogenous androgens on 17beta-estradiol-mediated protection after spinal cord injury in male rats. J. Neurotrauma 27, 611-626.
26. Koopmans, G., Deumens, R., Honig, W., Hamers, F., Steinbusch, H., and Joosten, E. (2005). The assessment of locomotor function in spinal cord injured rats: the importance of objective analysis of coordination. J. Neurotrauma 22, 214-225.
27. Kuchler, M., Fouad, K., Weinmann, O., Schwab, M., and Rain-eteau, O. (2002). Red nucleus projections to distinct motor neuron pools in the rat spinal cord. J. Comp. Neurol. 448, 349-359.
28. Liang, F., Moret, V., Wiesendanger, M., and Rouiller, E. (1991). Corticomotoneuronal connections in the rat: evidence from double-labeling of motoneurons and corticospinal axon arborizations. J. Comp. Neurol. 311, 356-366.
29. Liu, Y., Kim, D., Himes, B., Chow, S., Schallert, T., Murray, M., Tessler, A., and Fischer, I. (1999). Transplants of fibroblasts genetically modified to express BDNF promote regeneration of adult rat rubrospinal axons and recovery of forelimb function. J. Neurosci. 19, 4370-4387.
30. Lo, T. Jr., Cho, K., Garg, M., Lynch, M., Marcillo, A., Koivisto, D., Stagg, M., Abril, R., Patel, S., Dietrich, W., and Pearse, D. (2009). Systemic hypothermia improves histological and functional outcome after cervical spinal cord contusion in rats. J. Comp. Neurol. 514, 433-448.
31. Lynskey, J., Sandhu, F., Dai, H., McAtee, M., Slotkin, J., Ma-cArthur, L., and Bregman, B. (2006). Delayed intervention with transplants and neurotrophic factors supports recovery of forelimb function after cervical spinal cord injury in adult rats. J. Neurotrauma 23, 617-634.
32. Magnuson, D., Trinder, T., Zhang, Y., Burke, D., Morassutti, D., and Shields, C. (1999). Comparing deficits following excitotoxic and contusion injuries in the thoracic and lumbar spinal cord of the adult rat. Exp. Neurol. 156, 191-204.
33. Martinez, M., Brezun, J., Bonnier, L., and Xerri, C. (2009). A new rating scale for open-field evaluation of behavioral recovery after cervical spinal cord injury in rats. J. Neurotrauma 26, 1043-1053.
34. McKenna, J., and Whishaw, I. (1999). Complete compensation in skilled reaching success with associated impairments in limb synergies, after dorsal column lesion in the rat. J. Neurosci. 19, 1885-1894.
35. McKenna, J., Prusky, G., and Whishaw, I. (2000). Cervical mo-toneuron topography reflects the proximodistal organization of muscles and movements of the rat forelimb: a retrograde carbocyanine dye analysis. J. Comp. Neurol. 419, 286-296.
36. Metz, G., and Whishaw, I. (2002). Cortical and subcortical lesions impair skilled walking in the ladder rung walking test: a new task to evaluate fore-and hindlimb stepping, placing, and co-ordination. J. Neurosci. Methods 115, 169-179.
37. Muir, G., and Webb, A. (2000). Mini-review: assessment of behavioural recovery following spinal cord injury in rats. Eur. J. Neurosci. 12, 3079-3086.
38. Muir, G., Webb, A., Kanagal, S., and Taylor, L. (2007). Dorso-lateral cervical spinal injury differentially affects forelimb and hindlimb action in rats. Eur. J. Neurosci. 25, 1501-1510.
39. National Spinal Cord Injury Statistical Center. (2006). NSCISC Annual Report for the Model Spinal Cord Injury Care Systems. http://www.spinalcord.uab. edu/.
40. National Spinal Cord Injury Statistical Center. (2008). Spinal cord injury information network. http://www.spinalcord.uab.edu/.
41. Nishi, R., Liu, H., Chu, Y., Hamamura, M., Su, M., Nalcioglu, O., and Anderson, A. (2007). Behavioral, histological, and ex vivo magnetic resonance imaging assessment of graded contusion spinal cord injury in mice. J. Neurotrauma 24, 674-689.
42. Noble, L., and Wrathall, J. (1987). An inexpensive apparatus for producing graded spinal cord contusive injury in the rat. Exp. Neurol. 95, 530-533.
43. Pearse, D., Lo, T. Jr., Cho, K., Lynch, M., Garg, M., Marcillo, A., Sanchez, A., Cruz, Y., and Dietrich, W. (2005). Histopatholo-gical and behavioral characterization of a novel cervical spinal cord displacement contusion injury in the rat. J. Neurotrauma 22, 680-702.
44. Piecharka, D., Kleim, J., and Whishaw, I. (2005). Limits on recovery in the corticospinal tract of the rat: partial lesions impair skilled reaching and the topographic representation of the forelimb in motor cortex. Brain Res. Bull 66, 203-211.
45. Rabchevsky, A., Sullivan, P., Fugaccia, I., and Scheff, S. (2003). Creatine diet supplement for spinal cord injury: influences on functional recovery and tissue sparing in rats. J. Neurotrauma 7, 659-669.
46. Reier, P., Golder, F., Bolser, D., Hubscher, C., Johnson, R., Schrimsher, G., and Velardo, M. (2002). Gray matter repair in the cervical spinal cord. Prog. Brain Res. 137, 49-70.
47. Rouiller, E., Moret, V., and Liang, F. (1993). Comparison of the connectional properties of the two forelimb areas of the rat sensorimotor cortex: support for the presence of a premotor or supplementary motor cortical area. Somatosens. Mot. Res. 10, 269-289.
48. Sandrow-Feinberg, H., Zhukareva, V., Santi, L., Miller, K., Shumsky, J., Baker, D., and Houle, J. (2010). PEGylated interferon-beta modulates the acute inflammatory response and recovery when combined with forced exercise following cervical spinal contusion injury. Exp. Neurol. 223, 439-451.
49. Scheff, S., Rabchevsky, A., Fugaccia, I., Main, J., and Lumpp, J. Jr. (2003). Experimental modeling of spinal cord injury: characterization of a force-defined injury device. J. Neurotrauma 20, 179-193.
50. Schrimsher, G., and Reier, P. (1992). Forelimb motor performance following cervical spinal cord contusion injury in the rat. Exp. Neurol. 117, 287-298.
51. Schrimsher, G., and Reier, P. (1993). Forelimb motor performance following dorsal column, dorsolateral funiculi, or ventrolateral funiculi lesions of the cervical spinal cord in the rat. Exp. Neurol. 120, 264-276.
52. Smith, J., Lunga, P., Story, D., Harris, N., Le, B., James, M., Pickard, J., and Fawcett, J. (2007). Inosine promotes recovery of skilled motor function in a model of focal brain injury. Brain 130, 915-925.
53. Soblosky, J., Song, J., and Dinh, D. (2001). Graded unilateral cervical spinal cord injury in the rat: evaluation of forelimb recovery and histological effects. Behav. Brain Res. 119, 1-13.
54. Starkey, M., Barritt, A., Yip, P., Davies, M., Hamers, F., McMahon, S., and Bradbury, E. (2005). Assessing behavioural function following a pyramidotomy lesion of the corticospinal tract in adult mice. Exp. Neurol. 195, 524-539.
55. Van Hedel, H., and Curt, A. (2006). Fighting for each segment: estimating the clinical value of cervical and thoracic segments in SCI. J. Neurotrauma 23, 1621-1631.
56. Webb, A., and Muir, G. (2002). Compensatory locomotor adjustments of rats with cervical or thoracic spinal cord hemi-sections. J. Neurotrauma 19, 239-256.
57. Webb, A., and Muir, G. (2004). Course of motor recovery following ventrolateral spinal cord injury in the rat. Behav. Brain Res. 155, 55-65.
58. Webb, A., and Muir, G. (2005). Sensorimotor behaviour following incomplete cervical spinal cord injury in the rat. Behav. Brain Res. 165, 147-159.
59. Webb, A., and Muir, G. (2003). Unilateral dorsal column and rubrospinal tract injuries affect overground locomotion in the unrestrained rat. Eur. J. Neurosci. 18, 412-422.
60. West, M., Slomianka, L., and Gundersen, H. (1991). Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical frac-tionator. Anat. Rec. 231, 482-497.
61. Whishaw, I., and Gorny, B. (1994). Arpeggio and fractionated digit movements used in prehension by rats. Behav. Brain Res. 60, 15-24.
62. Whishaw, I., Gorny, B., and Sarna, J. (1998). Paw and limb use in skilled and spontaneous reaching after pyramidal tract, red nucleus and combined lesions in the rat: behavioral and anatomical dissociations. Behav. Brain Res. 93, 167-183.
63. Whishaw, I., Pellis, S., and Gorny, B. (1992). Skilled reaching in rats and humans: evidence for parallel development or ho-mology. Behav. Brain Res. 47, 59-70.
64. Zai, L., Ferrari, C., Subbaiah, S., Havton, L., Coppola, G., Strittmatter, S., Irwin, N., Geschwind, D., and Benowitz, L. (2009). Inosine alters gene expression and axonal projections in neurons contralateral to a cortical infarct and improves skilled use of the impaired limb. J. Neurosci. 29, 8187-8197.