Chronic spinal hemisection in rats induces a progressive decline in transmission in uninjured fibers to motoneurons

Experimental Neurology

Volumn 216, Issue 2, 2009, Pages 471-480

  Arvanian, Victor L ^a   Schnell, Lisa ^b   Lou, Li ^a   Golshani, Roozbeh ^c   Hunanyan, Arsen ^a   Ghosh, Arko ^b   Pearse, Damien D ^c   Robinson, John K ^a   Schwab, Martin E ^b   Fawcett, James W ^d   Mendell, Lorne M ^a  

^a STONY BROOK UNIVERSITY   (United States)

^b UNIVERSITY OF ZURICH   (Switzerland)

^c UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Conduction velocity; Demyelination; EPSP; Hemisection; Motoneuron; Spinal cord injury; Synaptic transmission; Ventrolateral funiculus; White matter

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; ELECTROSTIMULATION; EVOKED SPINAL CORD RESPONSE; FEMALE; MOTONEURON; NERVE FIBER; NONHUMAN; PRIORITY JOURNAL; RAT; SPINAL CORD INJURY; THORACIC SPINAL CORD;

ACTION POTENTIALS; ANALYSIS OF VARIANCE; ANIMALS; AXONS; BIOPHYSICS; CHRONIC DISEASE; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; ELECTRIC STIMULATION; EVOKED POTENTIALS; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; FUNCTIONAL LATERALITY; MOTOR ACTIVITY; MOTOR NEURONS; NERVE FIBERS, MYELINATED; NEURAL CONDUCTION; NEURONAL PLASTICITY; PSYCHOMOTOR PERFORMANCE; RATS; RATS, SPRAGUE-DAWLEY; RECOVERY OF FUNCTION; SPINAL CORD; SPINAL CORD INJURIES;

EID: 62049083009     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2009.01.004     Document Type: Article

References (52)

1. Antonino-Green D.M., Cheng J., and Magnuson D.S. Neurons labeled from locomotor-related ventrolateral funiculus stimulus sites in the neonatal rat spinal cord. J. Comp. Neurol. 442 (2002) 226-238
2. Arvanian V.L., Bowers W.J., Anderson A., Horner P.J., Federoff H.J., and Mendell L.M. Combined delivery of neurotrophin-3 and NMDA receptors 2D subunit strengthens synaptic transmission in contused and staggered double hemisected spinal cord of neonatal rat. Exp. Neurol. 197 (2006) 347-352
3. Arvanian, V.L., Schnell, L., Horner, P.J., Bowers, W.J., Federoff, H.J., Schwab, M.E., Mendell, L.M., 2006b. Combination Treatment With NT-3, NMDA-2d Subunits, And Anti-Nogo-A Antibody Increases Connections Of Transected Lateral Funiculus Fibers To Lumbar Motoneurons Society For Neuroscience Abstracts #555.2.
4. Ballermann M., and Fouad K. Spontaneous locomotor recovery in spinal cord injured rats is accompanied by anatomical plasticity of reticulospinal fibers. Eur. J. Neurosci. 23 (2006) 1988-1996
5. 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. Nat. Neurosci. 7 (2004) 269-277
6. Basso D.M., Beattie M.S., and Bresnahan J.C. A sensitive and reliable locomotor rating scale for open filed testing in rats. J. Neurotrauma 12 (1995) 1-21
7. Black J.A., Waxman S.G., and Smith K.J. Remyelination of dorsal column axons by endogenous Schwann cells restores the normal pattern of Nav1.6 and Kv1.2 at nodes of Ranvier. Brain 129 (2006) 1319-1329
8. Blight A.R. Axonal physiology of chronic spinal cord injury in the cat: intracellular recording in vitro. Neuroscience 10 (1983) 1471-1486
9. Blight A.R. Miracles and molecules-progress in spinal cord repair. Nat. Neurosci. 5 Suppl (2002) 1051-1054
10. Bunge R.P., Puckett W.R., and Hiester E.D. Observations on the pathology of several types of human spinal cord injury, with emphasis on the astrocyte response to penetrating injuries. Adv. Neurol. 72 (1997) 305-315
11. Burns S.P., Golding D.G., Rolle Jr. W.A., Graziani V., and Ditunno Jr. J.F. Recovery of ambulation in motor-incomplete tetraplegia. Arch. Phys. Med. Rehabil. 78 (1997) 1169-1172
12. Christensen M.D., Everhart A.W., Pickelman J.T., and Hulsebosch C.E. Mechanical and thermal allodynia in chronic central pain following spinal cord injury. Pain 68 (1996) 97-107
13. 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. Nat. Med. 14 (2008) 69-74
14. Crang A.J., Gilson J.M., Li W.W., and Blakemore W.F. The remyelinating potential and in vitro differentiation of MOG-expressing oligodendrocyte precursors isolated from the adult rat CNS. Eur. J. Neurosci. 20 (2004) 1445-1460
15. Donnelly D.J., and Popovich P.G. Inflammation and its role in neuroprotection, axonal regeneration and functional recovery after spinal cord injury. Exp. Neurol. 209 (2008) 378-388
16. Eccles J.C., Krnjevic K., and Miledi R. Delayed effects of peripheral severance of afferent nerve fibres on the efficacy of their central synapses. J. Physiol. 145 (1959) 204-220
17. Felts P.A., Baker T.A., and Smith K.J. Conduction in segmentally demyelinated mammalian central axons. J. Neurosci. 17 (1997) 7267-7277
18. Fouad K., et al. Combining Schwann cell bridges and olfactory-ensheathing glia grafts with chondroitinase promotes locomotor recovery after complete transection of the spinal cord. J. Neurosci. 25 (2005) 1169-1178
19. Golshani, R., Pearse, D.D., Lou, L., Mendell, L.M., Arvanian, V.L., 2008. Decline of transmission to motoneurons from surviving fibers induced by chronic spinal cord hemisection in adult rats. Society for Neuroscience Abstract #617.4.
20. Gramsbergen A. Normal and abnormal development of motor behavior: lessons from experiments in rats. Neural Plast. 8 (2001) 17-29
21. Guest J.D., Hiester E.D., and Bunge R.P. Demyelination and Schwann cell responses adjacent to injury epicenter cavities following chronic human spinal cord injury. Exp. Neurol. 192 (2005) 384-393
22. Hains B.C., Everhart A.W., Fullwood S.D., and Hulsebosch C.E. Changes in serotonin, serotonin transporter expression and serotonin denervation supersensitivity: involvement in chronic central pain after spinal hemisection in the rat. Exp. Neurol. 175 (2002) 347-362
23. Hagg T., and Oudega M. Degenerative and spontaneous regenerative processes after spinal cord injury. J. Neurotrauma 23 (2006) 264-280
24. Jankowska E., and Edgley S.A. How can corticospinal tract neurons contribute to ipsilateral movements? A question with implications for recovery of motor functions. Neuroscientist 12 (2006) 67-79
25. Jankowska E., Hammar I., Slawinska U., Maleszak K., and Edgley S.A. Neuronal basis of crossed actions from the reticular formation on feline hindlimb motoneurons. J. Neurosci. 23 (2003) 1867-1878
26. Johnson R.D. Descending pathways modulating the spinal circuitry for ejaculation: effects of chronic spinal cord injury. Prog. Brain Res. 152 (2006) 415-426
27. Kapoor R., Davies M., and Smith K.J. Temporary axonal conduction block and axonal loss in inflammatory neurological disease. A potential role for nitric oxide?. Ann. N.Y. Acad. Sci. 893 (1999) 304-308
28. Keirstead H.S., Nistor G., Bernal G., Totoiu M., Cloutier F., Sharp K., and Steward O. Human embryonic stem cell-derived oligodendrocyte progenitor cell transplants remyelinate and restore locomotion after spinal cord injury. J. Neurosci. 25 (2005) 4694-4705
29. Liebscher T., Schnell L., Schnell D., Scholl J., Schneider R., Gullo M., Fouad K., Mir A., Rausch M., Kindler D., Hamers F.P., and Schwab M.E. Nogo-A antibody improves regeneration and locomotion of spinal cord-injured rats. Ann. Neurol. 58 (2005) 706-719
30. Little J.W., Ditunno Jr. J.F., Stiens S.A., and Harris R.M. Incomplete spinal cord injury: neuronal mechanisms of motor recovery and hyperreflexia. Arch. Phys. Med. Rehabil. 80 (1999) 587-599
31. Lou, L., Garcia-Alias, G., Mendell, L.M., Fawcett, J.W., Arvanian, V.L., 2007. Transmission through white matter contralateral to thoracic hemisection declines beginning several days after injury in parallel with enhanced expression of CSPGs in the vicinity of the lesion. Society for Neuroscience Abstracts #801.1.
32. Mayer N.H., and Esquenazi A. Muscle overactivity and movement dysfunction in the upper motoneuron syndrome. Phys. Med. Rehabil. Clin. North Am. 14 (2003) 855-883
33. McTigue D.M., Popovich P.G., Jakeman L.B., and Stokes B.T. Strategies for spinal cord injury repair. Prog. Brain Res. 128 (2000) 3-8
34. Mendell L.M., Taylor J.S., Johnson R.D., and Munson J.B. Rescue of motoneuron and muscle afferent function in cats by regeneration into skin. II. Ia-motoneuron synapse. J. Neurophysiol. 73 (1995) 662-673
35. Nashmi R., and Fehlings M.G. Changes in axonal physiology and morphology after chronic compressive injury of the rat thoracic spinal cord. Neuroscience 104 (2001) 235-251
36. Park J.P., Kim K.J., Phi J.H., Park C.K., Kim J.H., Kang H.J., Lee D., Han K.H., Wang K.C., and Paek S.H. Simple measurement of spinal cord evoked potential: a valuable data source in the rat spinal cord injury model. J. Clin. Neurosci. 14 (2007) 1099-1105
37. Paxinos G., Watson C., Pennisi M., and Topple A. Bregma, lambda and the interaural midpoint in stereotaxic surgery with rats of different sex, strain and weight. J. Neurosci. Methods 13 (1985) 139-143
38. Pearse D.D., et al. Histopathological and behavioral characterization of a novel cervical spinal cord displacement contusion injury in the rat. J. Neurotrauma 22 (2005) 680-702
39. Petruska J.C., Ichiyama R.M., Jindrich D.L., Crown E.D., Tansey K.E., Roy R.R., Edgerton V.R., and Mendell L.M. Changes in motoneuron properties and synaptic inputs related to step training after spinal cord transection in rats. J. Neurosci. 27 (2007) 4460-4471
40. Raineteau O., and Schwab M.E. Plasticity of motor systems after incomplete spinal cord injury. Nat. Rev. Neurosci. 2 (2001) 263-273
41. Reed W.R., Shum-Siu A., Onifer S.M., and Magnuson D.S. Inter-enlargement pathways in the ventrolateral funiculus of the adult rat spinal cord. Neuroscience 142 (2006) 1195-1207
42. Reed W.R., Shum-Siu A., and Magnuson D.S. Reticulospinal pathways in the ventrolateral funiculus with terminations in the cervical and lumbar enlargements of the adult rat spinal cord. Neuroscience 151 (2008) 505-517
43. Schallert T., and Woodlee M.T. Brain-dependent movements and cerebral-spinal connections: key targets of cellular and behavioral enrichment in CNS injury models. J. Rehabil. Res. Dev. 40 (2003) 9-17
44. Schwartz G., and Fehlings M.G. Evaluation of the neuroprotective effects of sodium channel blockers after spinal cord injury: improved behavioral and neuroanatomical recovery with riluzole. J. Neurosurg. 94 (2001) 245-256
45. Shefchyk S.J. Spinal mechanisms contributing to urethral striated sphincter control during continence and micturition: "how good things might go bad". Prog. Brain Res. 152 (2006) 85-95
46. Shi R., and Blight A.R. Compression injury of mammalian spinal cord in vitro and the dynamics of action potential conduction failure. J. Neurophysiol. 76 (1996) 1572-1580
47. Shuman S.L., Bresnahan J.C., and Beattie M.S. Apoptosis of microglia and oligodendrocytes after spinal cord contusion in rats. J. Neurosci. Res. 50 (1997) 798-808
48. Shumsky J.S., Tobias C.A., Tumolo M., Long W.D., Giszter S.F., and Murray M. Delayed transplantation of fibroblasts genetically modified to secrete BDNF and NT-3 into a spinal cord injury site is associated with limited recovery of function. Exp. Neurol. 184 (2003) 114-130
49. Siegenthaler M.M., Tu M.K., and Keirstead H.S. The extent of myelin pathology differs following contusion and transection spinal cord injury. J. Neurotrauma 24 (2007) 1631-1646
50. Webb A.A., and Muir G.D. Course of motor recovery following ventrolateral spinal cord injury in the rat. Behav. Brain Res. 155 (2004) 55-65
51. You S.W., Chen B.Y., Liu H.L., Lang B., Xia J.L., Jiao X.Y., and Ju G. Spontaneous recovery of locomotion induced by remaining fibers after spinal cord transection in adult rats. Restor. Neurol. Neurosci. 21 (2003) 39-45
52. Yukawa Y., Kato F., Ito K., Horie Y., Hida T., Machino M., Ito Z.Y., and Matsuyama Y. Postoperative changes in spinal cord signal intensity in patients with cervical compression myelopathy: comparison between preoperative and postoperative magnetic resonance images. J. Neurosurg. Spine 8 (2008) 524-528