Are rodents an appropriate pre-clinical model for treating spinal cord injury? Examples from the respiratory system

Experimental Neurology

Volumn 213, Issue 2, 2008, Pages 249-256

  Kastner, Anne ^a   Gauthier, Patrick ^a  

^a AIX MARSEILLE UNIVERSITY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

MUSCULOSKELETAL SYSTEM; NERVE CELL PLASTICITY; NERVE REGENERATION; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL TRACT; RESPIRATORY FUNCTION; RESPIRATORY SYSTEM; REVIEW; SPINAL CORD INJURY;

ANIMALS; DISEASE MODELS, ANIMAL; HUMANS; PYRAMIDAL TRACTS; RESPIRATORY SYSTEM; RODENTIA; SPECIES SPECIFICITY; SPINAL CORD INJURIES;

EID: 51349092472     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2008.07.008     Document Type: Review

References (106)

1. Antal M., Sholomenko G.N., Moschovakis A.K., Storm-Mathisen J., Heizmann C.W., and Hunziker W. The termination pattern and postsynaptic targets of rubrospinal fibers in the rat spinal cord: a light and electron microscopic study. J. Comp. Neurol. 325 (1992) 22-37
2. Bailey E.F., and Fregosi R.F. Coordination of intrinsic and extrinsic tongue muscles during spontaneous breathing in the rat. J. Appl. Physiol. 96 2 (2004) 440-449
3. Bareyre F.M., Kerschensteiner M., Raineteau O., Mettenleiter T.C., Weinmann O., and Schwab M.E. The injured spinal cord spontaneously forms a new intraspinal circuit in adult rats. Nature Neurosci. 7 (2004) 269-277
4. Barrière G., Leblond H., Provencher J., and Rossignol S. Prominent role of the spinal central pattern generator in the recovery of locomotion after partial spinal cord injuries. J. Neurosci. 28 (2008) 3976-3987
5. Baussart B., Stamegna J.C., Polentes J., Tadié M., and Gauthier P. A new model of upper cervical spinal contusion inducing a persistent unilateral diaphragmatic deficit in the adult rat. Neurobiol. Dis. 22 (2006) 562-574
6. Benarroch E.E., Schmeichel A.M., Low P.A., and Parisi J.E. Depletion of ventromedullary NK-1 receptor-immunoreactive neurons in multiple system atrophy. Brain 126 (2003) 2183-2190
7. Blesch A., Yang H., Weidner N., Hoang A., and Otero D. Axonal responses to cellularly delivered NT-4/5 after spinal cord injury. Mol. Cell. Neurosci. 27 (2004) 190-201
8. Blits B., Dijkhuizen P.A., Boer G.J., and Verhaagen J. Intercostal nerve implants transduced with an adenoviral vector encoding neurotrophin-3 promote regrowth of injured rat corticospinal tract fibers and improve hindlimb function. Exp. Neurol. 164 (2000) 25-37
9. Bogousslavsky J., Khurana R., Deruaz J.P., Hornung J.P., Regli F., Janzer R., and Perret C. Respiratory failure and unilateral caudal brainstem infarction. Ann. Neurol. 28 (1990) 668-673
10. Boulenguez P., Gauthier P., and Kastner A. Respiratory neuron subpopulations and pathways potentially involved in the reactivation of phrenic motoneurons after C2 hemisection. Brain Res. 1148 (2007) 96-104
11. Bradbury E.J., and McMahon S.B. Spinal cord repair strategies: why do they work?. Nature Rev. Neurosci. 7 (2006) 53-644
12. Butler J.E. Drive to the human respiratory muscles. Resp. Physiol. Neurobiol. 159 (2007) 115-126
13. Carlstedt T., Anand P., Htut M., Misra P., and Svensson M. Restoration of hand function and so called "breathing arm" after intraspinal repair of C5-T1 brachial plexus avulsion injury. Case report. Neurosurg. Focus 16 (2004) E7
14. Cheng H., Cao Y., and Olson L. Spinal cord repair in adult paraplegic rats: partial restoration of hind limb function. Science 273 (1996) 510-513
15. Colebatch J.G., Adams L., Murphy K., Martin A.J., Lammertsma A.A., Tochon-Danguy H.J., Clark J.C., Friston K.J., and Guz A. Regional cerebral blood flow during volitional breathing in man. J. Physiol. 443 (1991) 91-103
16. Corfield D.R., Murphy K., and Guz A. Does the motor cortical control of the diaphragm "bypass" the brain stem respiratory centres in man? Resp. Physiol. 114 (1998) 109-117
17. Courtine G., Bunge M.B., Fawcett J.W., Grossman R.G., Kaas J.H., Lemon R., Maier I., Martin J., Nudo R.J., Ramon-Cueto A., Rouiller E.M., Schnell L., Wannier T., Schwab M.E., and Edgerton V.R. Can experiments in nonhuman primates expedite the translation of treatments for spinal cord injury in humans?. Nature Med. 13 (2007) 561-566
18. Courtine G., Song B., Roy R.R., Zhong H., Herrmann J.E., Ao Y., Qi J., Edgerton V.R., and Sofroniew M.V. Recovery of supraspinal control of stepping via indirect propriospinal relay connections after spinal cord injury. Nature Med. 14 (2008) 69-74
19. Decherchi P., and Gauthier P. Regrowth of acute and chronic injured spinal pathways within supra-lesional post-traumatic nerve grafts. Neuroscience 101 (2000) 197-210
20. Decherchi P., and Gauthier P. Regeneration of acutely and chronically injured descending respiratory pathways within post-traumatic nerve grafts. Neuroscience 112 (2002) 141-152
21. DiMarco A.F. Restoration of respiratory muscle function following spinal cord injury; review of electrical and magnetic stimulation techniques. Resp. Physiol. Neurobiol. 147 (2005) 273-287
22. Dobbins E.G., and Feldman J.L. Brainstem network controlling descending drive to phrenic motoneurons in rat. J. Comp. Neurol. 347 (1994) 64-86
23. Duffin J. Functional organization of respiratory neurons: a brief review of current questions and speculations. Exp. Physiol. 5 (2004) 517-529
24. Duffin J., and Iscoe S. The possible role of C5 segment inspiratory interneurons investigated by cross-correlation with phrenic motoneurons in decerebrate cats. Exp. Brain Res. 112 (1996) 35-40
25. El Bohy A.A., Schrimsher G.W., Reier P.J., and Goshgarian H.G. Quantitative assessment of respiratory function following contusion injury of the cervical spinal cord. Exp. Neurol. 150 (1998) 143-152
26. Ellenberger H.H., and Feldman J.L. Monosynaptic transmission of respiratory drive to phrenic motoneurons from brainstem bulbospinal neurons in rats. J. Comp. Neurol. 269 (1988) 47-57
27. Ellenberger H.H., Vera P.L., Haselton J.R., Haselton C.L., and Schneiderman N. Brainstem projections to the phrenic nucleus: an anterograde and retrograde HRP study in the rabbit. Brain Res. Bull. 24 (1990) 163-174
28. Evans K.C., Shea S.A., and Saykin A.J. Functional MRI localisation of central nervous system regions associated with volitional inspiration in humans. J. Physiol. 520 (1999) 383-392
29. Feldman J.L., Loewy A.D., and Speck D.F. Projections from the ventral respiratory group to phrenic and intercostals motoneurons in cat: an autoradiographic study. J. Neurosci. 5 (1985) 1993-2000
30. Feldman J.L., Mitchell G.S., and Nattie E.E. Breathing: respiratory, plasticity, chemosensitivity. Annu. Rev. Neurosci. 26 (2003) 239-266
31. Ford T.W., and Kirkwood P.A. Respiratory drive in hindlimb motoneurones of the anaesthetized female cat. Brain Res. Bull. 70 (2006) 56-450
32. Fouad K., Pedersen V., Schwab M.E., and Brösamle C. Cervical sprouting of corticospinal fibers after thoracic spinal cord injury accompanies shifts in evoked motor responses. Curr. Biol. 11 (2001) 1766-1770
33. Franssen E.H., de Bree F.M., and Verhaagen J. Olfactory ensheathing glia: their contribution to primary olfactory nervous system regeneration and their regenerative potential following transplantation into the injured spinal cord. Brain Res. Rev. 56 (2007) 236-258
34. Fuller D.D., Golder F.J., Olson E.B., and Mitchell G.S. Recovery of phrenic activity and ventilation after cervical spinal hemisection in rats. J. Appl. Physiol. 100 (2006) 800-806
35. Fuller D.D., Doperalki N.J., Dougherty B.J., Sandhu M.S., Bolser D.C., and Reier P.J. Modest spontaneous recovery of ventilation following chronic high cervical hemisection in rats. Exp Neurol. 21 (2008) 97-106
36. Gandevia S.C., and Rothwell J.C. Activation of the human diaphragm from the motor cortex. J. Physiol. 384 (1987) 109-118
37. Gaudy J.H., Quignon M., Sicard J.F., and Maneglia R. Effets de l'halothane sur la ventilation et les gaz du sang arteriel chez le rat avec ou sans paralysie diaphragmatique. Can. J. Anaesth. 42 (1995) 249-255
38. Gauthier P., Rega P., Lammari-Barreault N., and Polentes J. Functional reconnections established by central respiratory neurons regenerating axons into a nerve graft bridging the respiratory centers to the cervical spinal cord. J. Neurosci. Res. 70 (2002) 65-81
39. Gauthier P., Baussart B., Stamegna J.C., Tadié M., and Vinit S. Diaphragm recovery by laryngeal innervation after bilateral phrenicotomy or complete C2 spinal section in rats. Neurobiol. Dis. 24 (2006) 53-66
40. Gaytan S.P., and Pasaro R. Connections of the rostral ventral respiratory neuronal cell group: an anterograde and retrograde tracing study in the rat. Brain Res. Bull. 47 (1998) 625-642
41. Golder F.J., Fuller D.D., Davenport P.W., Johnson R.D., Reier P.J., and Bolser D.C. Respiratory motor recovery after unilateral spinal cord injury: eliminating crossed phrenic activity decreases tidal volume and increases contralateral respiratory motor output. J. Neurosci. 23 (2003) 2494-2501
42. Golder F.J., and Mitchell G.S. Spinal synaptic enhancement with acute intermittent hypoxia improves respiratory function after chronic cervical spinal cord injury. J. Neurosci. 25 (2005) 2925-2932
43. Goshgarian H.G. The crossed phrenic phenomenon: a model for plasticity in the respiratory pathways following spinal cord injury. J. Appl. Physiol. 94 (2003) 795-810
44. Gray P.A., Janczewski W.A., Mellen N., McCrimmon D.R., and Feldman J.L. Normal breathing requires preBotzinger complex neurokinin-1 receptor-expressing neurons. Nature Neurosci. 4 (2001) 927-930
45. Hagg T. Collateral sprouting as a target for improved function after spinal cord injury. J. Neurotrauma 23 (2006) 281-294
46. Hagg T., and Oudega M. Degenerative and spontaneous regenerative processes after spinal cord injury. J. Neurotrauma 23 (2006) 264-280
47. Hilaire G., Monteau R., Gauthier P., Rega P., and Morin D. Functional significance of the dorsal respiratory group in adult and newborn rats: in vivo and in vitro studies. Neurosci. Lett. 111 (1990) 133-138
48. Hilaire G., and Pasaro R. Genesis and control of the respiratory rhythm in adult mammals. News Physiol. Sci. 18 (2003) 23-28
49. Holstege G., Blok B.F., and Ralston D.D. Anatomical evidence for red nucleus projections to motoneuronal cell groups in the spinal cord of the monkey. Neurosci. Lett. 95 (1988) 97-101
50. Houle J.D., Schramm P., and Herdegen T. Trophic factors modulation of c-jun expression in supraspinal neurons after chronic spinal cord injury. Exp. Neurol. 154 (1998) 602-611
51. Howard R.S., Wiles C.M., Hirsch N.P., Loh L., Spencer G.T., and Newsom-Davis J. Respiratory involvement in multiple sclerosis. Brain 115 (1992) 479-494
52. Isaev G.G., Gerasimenko Y.P., Selionov V.A., and Kartashova N.A. Respiratory responses to voluntary and reflexly-induced stepping movements in normal subjects and spinal patients. J. Physiol. Pharmacol. 55 (2004) 77-82
53. Jankowska E. Target cells of rubrospinal tract fibres within the lumbar spinal cord. Behav. Brain Res. 28 (1988) 91-96
54. Janssen B.J., and Smits J.F. Autonomic control of blood pressure in mice: basic physiology and effects of genetic modification. Am. J. Physiol. Regul. Integr. Comp. Physiol. 282 (2002) R1545-R1564
55. Jenkins R., Tetzlaff W., and Hunt S.P. Differential expression of immediate early genes in rubrospinal neurons following axotomy in rat. Eur. J. Neurosci. 5 (1993) 203-209
56. Juvin L., and Morin D. Descending respiratory polysynaptic inputs to cervical and thoracic motoneurons diminish during early postnatal maturation in rat spinal cord. Eur. J. Neurosci. 21 (2005) 808-813
57. Kim J.E., Liu B.P., Park J.H., and Strittmatter S.M. Nogo-66 receptor prevents raphespinal and rubrospinal axon regeneration and limits functional recovery from spinal cord injury. Neuron 44 (2004) 439-451
58. Küchler M., Fouad K., Weinmann O., Schwab M.E., and Raineteau O. Red nucleus projections to distinct motor neuron pools in the rat spinal cord. J. Comp. Neurol. 448 (2002) 349-359
59. Lane M.A., White T.E., Coutts M.A., Sandhu M.S., Siegel K.A., O'steen B.E., Fuller D.D., and Reier P.J. Plasticity in Respiratory Circuitry Following Partial Spinal Cord Injury (SCI) in the Adult Rat.. Neuroscience Meeting Planner (2007), Society for Neuroscience, San Diego, CA Program No. 600.29
60. Larson C.R., Yajima Y., and Ko P. Modification in activity of medullary respiratory-related neurons for vocalization and swallowing. J. Neurophysiol. 71 (1994) 2294-2304
61. Lee Y.S., Hsiao I., and Lin V.W. Peripheral nerve grafts and aFGF restore partial hindlimb function in adult paraplegic rats. J. Neurotrauma 19 (2002) 1203-1216
62. Lemon R.N., Kirkwood P.A., Maier M.A., Nakajima K., and Nathan P. Direct and indirect pathways for corticospinal control of upper limb motoneurons in the primate. Prog. Brain Res. 143 (2004) 263-279
63. Li Y., Decherchi P., and Raisman G. Transplantation of olfactory ensheathing cells into spinal cord lesions restores breathing and climbing. J. Neurosci. 23 (2003) 727-731
64. Lipski J., Bektas A., and Porter R. Short latency inputs to phrenic motoneurons from the sensorimotor cortex in the cat. Exp. Brain Res. 61 (1986) 280-290
65. Lipski J., Duffin J., Kruszewska B., and Zhang X. Upper cervical inspiratory neurons in the rat: an electrophysiological and morphological study. Exp. Brain Res. 95 (1993) 477-487
66. Lipski J.X., Zhang B., Kruszewska B., and Kanjhan R. Morphological study of long axonal projections of ventral medullary inspiratory neurons in the rat. Brain. Res. 640 (1994) 171-184
67. Lopez-Vales R., Fores J., Navarro X., and Verdu E. Chronic transplantation of olfactory ensheathing cells promotes partial recovery after complete spinal cord transection in the rat. Glia 55 (2007) 303-311
68. Lu F., Qin C., Foreman R.D., and Farber J.P. Chemical activation of C1-C2 spinal neurons modulates intercostals and phrenic nerve activity in rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 286 (2004) R1069-R1076
69. Majczynski H., and Slawinska U. Locomotor recovery after thoracic spinal cord lesions in cats, rats and humans. Acta Neurobiol. Exp. 67 (2007) 235-257
70. Maskrey M., Evans S.E., Mesch U., Andersen N.A., and Sherrey J.H. Phrenicotomy in the rat: acute changes in blood gases, pH and body temperature. Respir. Physiol. 90 (1992) 47-54
71. Mason M.R., Lieberman A.R., and Anderson P.N. Corticospinal neurons up-regulate a range of growth-associated genes following intracortical, but not spinal, axotomy. Eur. J. Neurosci. 18 (2003) 789-802
72. Mitchell G.S., and Johnson S.M. Neuroplasticity in respiratory motor control. J. Appl. Physiol. 94 (2003) 358-374
73. Mognoni P., Saibene F., and Sant'ambrogio G. Contribution of the diaphragm and the other muscles to different levels of tidal volume and static inspiratory effort in the rabbit. J. Physiol. 202 (1969) 517-534
74. Monteau R., Erchidi S., Gauthier P., Hilaire G., and Rega P. Pneumotaxic centre and apneustic breathing: interspecies differences between rat and cat. Neurosci. Lett., 99 (1989) 311-316
75. Muir G.D., and Whishaw I.Q. Complete locomotor recovery following corticospinal tract lesions: measurement of ground reaction forces during overground locomotion in rats. Behav. Brain Res. 103 (1999) 45-53
76. Nantwi K.D., El-Bohy A.A., Schrimsher G.W., Reier P.J., and Goshgarian H.G. Spontaneous functional recovery in a paralyzed hemidiaphragm following upper cervical spinal cord injury in adult rats. Neurorehab. Neural. Rep. 13 (1999) 225-234
77. Nathan P.W., Smith M., and Deacon P. Vestibulospinal, reticulospinal and descending propriospinal nerve fibres in man. Brain 119 (1996) 1809-1833
78. Nogues M.A., Roncoroni A.J., and Benarroch E. Breathing control in neurological diseases. Clin. Auton. Res. 12 (2002) 440-449
79. Okano H., Kanedo S., Okada S., Iwanami A., Nakamura M., and Toyama Y. Regeneration based therapies for spinal cord injuries. Neurochem. Int. 51 (2007) 68-73
80. Onai T., Saji M., and Miura M. Projections of supraspinal structures to the phrenic motor nucleus in rats studied by a horseradish peroxidase microinjection method. J. Auton. Nerv. Syst. 21 (1987) 233-240
81. Oo T., Watt J.W., Soni B.M., and Sett P.K. Delayed diaphragm recovery in 12 patients after high cervical spinal cord injury. A retrospective review of the diaphragm status of 107 patients ventilated after acute spinal cord injury. Spinal Cord 37 (1999) 117-122
82. Polentes J., Stamegna J.C., Nieto-Sampedro M., and Gauthier P. Phrenic rehabilitation and diaphragm recovery after cervical injury and transplantation of olfactory ensheathing cells. Neurobiol. Dis. 16 (2004) 638-653
83. Porter W.T. The path of the respiratory impulse from the bulb to the phrenic nuclei. J. Physiol. 17 (1895) 455-485
84. Qin C., Farber J.P., Chandler M.J., and Foreman R.D. Chemical activation of C1-C2 spinal neurons modulates activity of thoracic respiratory interneurons in rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 283 (2002) R843-R852
85. Ralston D.D., Milroy A.M., and Holstege G. Ultrastructural evidence for direct monosynaptic rubrospinal connections to motoneurons in Macaca mulatto. Neurosci. Lett. 95 (1988) 102-106
86. Rikard-Bell G.C., Bystrzycka E.K., and Nail B.S. Cells of origin of corticospinal projections to phrenic and thoracic respiratory motoneurones in the cat as shown by retrograde transport of HRP. Brain Res. Bull. 14 (1985) 39-47
87. Rossignol S., Schwab M., Schwartz M., and Fehlings M.G. Spinal cord injury: time to move? J. Neurosci. 27 (2007) 11782-11792
88. Routal R.V., and Pal G.P. Location of the phrenic nucleus in the human spinal cord. J. Anat. 195 (1999) 617-621
89. Ruitenberg M.J., Vukovic J., Sarich J., Busfield S.J., and Plant G.W. Olfactory ensheathing cells: characteristics, genetic engineering and therapeutic potential. J. Neurotrauma 23 (2006) 468-478
90. Shea S.A. Behavioural and arousal-related influences on breathing in humans. Exp. Physiol. 81 (1996) 1-26
91. Tan W., Janczewski W.A., Yang P., Shao X.M., Callaway E.M., and Feldman J.L. Silencing preBötzinger complex somatostatin-expressing neurons induces persistent apnea in awake rat. Nature Neurosci. 11 (2008) 538-540
92. Thuret S., Moon L.D., and Gage F.H. Therapeutic interventions after spinal cord injury. Nat. Rev. Neurosci. 7 (2006) 628-643
93. Tian G.F., and Duffin J. Connections from upper cervical inspiratory neurons to phrenic and intercostals motoneurons studied with cross-correlation in the decerebrate rat. Exp. Brain Res. 110 (1996) 196-204
94. Tian G.F., and Duffin J. Spinal connections of ventral group bulbospinal inspiratory neurons studied with cross-correlation in the decerebrate rat. Exp. Brain Res. 111 (1996) 178-186
95. Urban P.P., Morgenstern M., Brause K., Wicht S., Vukurevic G., Kessler S., and Stoeter P. Distribution and course of cortico-respiratory projections for voluntary activation in man- a transcranial magnetic stimulation study in healthy subjects and patients with cerebral ischemia. J. Neurol. 249 (2002) 735-744
96. Vavrek R., Pearse D.D., and Fouad K. Neuronal populations capable of regeneration following a combined treatment in rats with spinal cord transection. J. Neurotrauma 24 (2007) 1667-1673
97. Vinit S., Boulenguez P., Efthimiadi L., Stamegna J.C., Gauthier P., and Kastner A. Axotomized bulbospinal neurons express c-jun after cervical spinal cord injury. Neuroreport 16 (2005) 1535-1539
98. Vinit S., Gauthier P., Stamegna J.C., and Kastner A. High cervical lateral spinal cord injury results in long-term ipsilateral hemidiaphragm paralysis. J. Neurotrauma 23 (2006) 1137-1146
99. Vinit S., Stamegna J.C., Boulenguez P., Gauthier P., and Kastner A. Restorative respiratory pathways after partial cervical spinal cord injury: role of ipsilateral phrenic afferents. Eur. J. Neurosci. 25 (2007) 3551-3560
100. Vinit S., Darlot F., Stamegna J.C., Sanchez P., Gauthier P., and Kastner A. Long-term respiratory pathways reorganization after partial cervical spinal cord injury. Eur. J. Neurosci. 27 (2008) 897-908
101. Wakabayashi Y., Komori H., Kawa-Uchi T., Mochida K., Takahashi M., Qi M., Otake K., and Shinomiya K. Functional recovery and regeneration of descending tracts in rats after spinal cord transection in infancy. Spine 26 (2001) 1215-1522
102. Wang H., Stornetta R.L., Rosin D.L., and Guyenet P.G. Neurokinin-1 receptor-immunoreactive neurons of the ventral respiratory group in the rat. J. Comp. Neurol. 434 (2001) 128-146
103. Weidner N., Ner A., Salimi N., and Tuszynski M.H. Spontaneous corticospinal axonal plasticity and functional recovery after adult central nervous system injury. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 3513-3518
104. Winslow C., and Rozovsky J. Effect of spinal cord injury on the respiratory system. Am. J. Phys. Med. Rehabil. 82 (2003) 803-814
105. Ye J.H., and Houle J.D. Treatment of the chronically injured spinal cord with neurotrophic factors can promote axonal regeneration from supraspinal neurons. Exp. Neurol. 143 (1997) 70-81
106. Zimmer M.B., Nantwi K., and Goshgarian H.G. Effect of spinal cord injury on the neural regulation of respiratory function. Exp. Neurol. 209 (2008) 399-406