The injured spinal cord spontaneously forms a new intraspinal circuit in adult rats

Nature Neuroscience

Volumn 7, Issue 3, 2004, Pages 269-277

  Bareyre, Florence M ^a,b,c   Kerschensteiner, Martin ^a,b,c   Raineteau, Olivier ^a   Mettenleiter, Thomas C ^d   Weinmann, Oliver ^a,b   Schwab, Martin E ^a,b  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b ETH ZURICH   (Switzerland)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d FEDERAL RESEARCH INSTITUTE FOR ANIMAL HEALTH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CERVICAL SPINAL CORD; CONTROLLED STUDY; CONVALESCENCE; ELECTROPHYSIOLOGY; FEMALE; FUNCTIONAL ASSESSMENT; GRAY MATTER; LUMBAR SPINAL CORD; MOTONEURON; NERVE CELL; NERVE FIBER; NERVE FIBER GROWTH; NERVE FIBER REGENERATION; NERVE REGENERATION; NERVE TRANSECTION; NONHUMAN; PERIPHERAL NERVE; PRIORITY JOURNAL; PYRAMIDAL TRACT; RAT; SPINAL CORD INJURY;

ACTION POTENTIALS; ANIMALS; AXOTOMY; CELL DIFFERENTIATION; ELECTROMYOGRAPHY; FEMALE; GROWTH CONES; HINDLIMB; INTERNEURONS; MOTOR CORTEX; MOTOR NEURONS; NERVE REGENERATION; NEURAL CONDUCTION; NEURONAL PLASTICITY; PRESYNAPTIC TERMINALS; PYRAMIDAL TRACTS; RATS; RATS, INBRED LEW; RECOVERY OF FUNCTION; SPINAL CORD; SPINAL CORD INJURIES;

EID: 1442348904     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn1195     Document Type: Article

References (50)

1. Schwab, M.E. & Bartholdi, D. Degeneration and regeneration of axons in the lesioned spinal cord. Physiol. Rev. 76, 319-370 (1996).
2. Rossignol, S., Drew, T., Brustein, E. & Jiang, W. Locomotor performance and adaptation after partial or complete spinal cord lesions in the cat. Prog. Brain Res. 123, 349-365 (1999).
3. Wernig, A. & Muller, S. Laufband locomotion with body weight support improved walking in persons with severe spinal cord injuries. Paraplegia 30, 229-238 (1992).
4. Dietz, V., Wirz, M., Curt, A. & Colombo, G. Locomotor pattern in paraplegic patients: training effects and recovery of spinal cord function. Spinal Cord 36, 380-390 (1998).
5. Hiersemenzel, L.P., Curt, A. & Dietz, V. From spinal shock to spasticity: neuronal adaptations to a spinal cord injury. Neurology 54, 1574-1582 (2000).
6. Holaday, J.W. & Faden, A.I. Spinal shock and injury: experimental therapeutic approaches. Adv. Shock Res. 10, 95-98 (1983).
7. Gensert, J.M. & Goldman, J.E. Endogenous progenitors remyelinate demyelinated axons in the adult CNS. Neuron 19, 197-203 (1997).
8. Lawrence, D.G. & Kuypers, H.G. The functional organization of the motor system in the monkey. I. The effects of bilateral pyramidal lesions. Brain 91, 1-14 (1968).
9. Pettersson, L.G., Lundberg, A., Alstermark, B., Isa, T. & Tantisira, B. Effect of spinal cord lesions on forelimb target-reaching and on visually guided switching of target-reaching in the cat. Neurosci. Res. 29, 241-256 (1997).
10. Weidner, N., Ner, A., Salimi, N. & Tuszynski, M.H. Spontaneous corticospinal axonal plasticity and functional recovery after adult central nervous system injury. Proc. Natl. Acad. Sci. USA 98, 3513-3518 (2001).
11. Fouad, K., Pedersen, V., Schwab, M.E. & Brosamle, C. Cervical sprouting of corticospinal fibers after thoracic spinal cord injury accompanies shifts in evoked motor responses. Curr. Biol. 11, 1766-1770 (2001).
12. Raineteau, O. & Schwab, M.E. Plasticity of motor systems after incomplete spinal cord injury. Nat. Rev. Neurosci. 2, 263-273 (2001).
13. Murray, M. & Goldberger, M.E. Restitution of function and collateral sprouting in the cat spinal cord: the partially hemisected animal. J. Comp. Neurol. 158, 19-36 (1974).
14. Jankowska, E., Lundberg, A., Roberts, W.J. & Stuart, D. A long propriospinal system with direct effect on motoneurones and on interneurones in the cat lumbosacral cord. Exp. Brain Res. 21, 169-194 (1974).
15. Miller, S., van Berkum, R., van der Burg, J. & van der Meche, F.G. Interlimb coordination in stepping in the cat. J. Physiol. 230, 30P-31P (1973).
16. Giovanelli Barilari, M. & Kuypers, H.G. Propriospinal fibers interconnecting the spinal enlargements in the cat. Brain Res. 14, 321-330 (1969).
17. Alstermark, B., Lundberg, A., Pinter, M. & Sasaki, S. Subpopulations and functions of long C3-C5 propriospinal neurones. Brain Res. 404, 395-400 (1987).
18. Alstermark, B., Lundberg, A., Pinter, M. & Sasaki, S. Long C3-C5 propriospinal neurones in the cat. Brain Res. 404, 382-388 (1987).
19. Alstermark, B., Kummel, H., Pinter, M.J. & Tantisira, B. Branching and termination of C3-C4 propriospinal neurones in the cervical spinal cord of the cat. Neurosci. Lett. 74, 291-296 (1987).
20. Alstermark, B., Isa, T., Kummel, H. & Tantisira, B. Projection from excitatory C3-C4 propriospinal neurones to lamina VII and VIII neurones in the C6-Th1 segments of the cat. Neurosci. Res. 8, 131-137 (1990).
21. Neafsey, E.J. et al. The organization of the rat motor cortex: a microstimulation mapping study. Brain Res. 396, 77-96 (1986).
22. De Ryck, M., Van Reempts, J., Duytschaever, H., Van Deuren, B. & Clincke, G. Neocortical localization of tactile/proprioceptive limb placing reactions in the rat. Brain Res. 573, 44-60 (1992).
23. Z'Graggen, W.J. et al. Compensatory sprouting and impulse rerouting after unilateral pyramidal tract lesion in neonatal rats. J. Neurosci. 20, 6561-6569 (2000).
24. Li, W.W., Yew, D.T., Chuah, M.I., Leung, P.C. & Tsang, D.S. Axonal sprouting in the hemisected adult rat spinal cord. Neuroscience 61, 133-139 (1994).
25. Aoki, M., Fujito, Y., Satomi, H., Kurosawa, Y. & Kasaba, T. The possible role of collateral sprouting in the functional restitution of corticospinal connections after spinal hemisection. Neurosci. Res. 3, 617-627 (1986).
26. Jankowska, E. & Hammar, I. Spinal interneurones; how can studies in animals contribute to the understanding of spinal interneuronal systems in man? Brain Res. Brain Res. Rev. 40, 19-28 (2002).
27. Mariani, J. Elimination of synapses during the development of the central nervous system. Prog. Brain Res. 58, 383-392 (1983).
28. Chen, C. & Regehr, W.G. Developmental remodeling of the retinogeniculate synapse. Neuron 28, 955-966 (2000).
29. Hubel, D.H., Wiesel, T.N. & LeVay, S. Plasticity of ocular dominance columns in monkey striate cortex. Philos. Trans. R. Soc. Lond. B Biol. Sci. 278, 377-409 (1977).
30. Colman, H., Nabekura, J. & Lichtman, J.W. Alterations in synaptic strength preceding axon withdrawal. Science 275, 356-361 (1997).
31. Masson, R.L., Jr., Sparkes, M.L. & Ritz, L.A. Descending projections to the rat sacrocaudal spinal cord. J. Comp. Neurol. 307, 120-130 (1991).
32. Jankowska, E., Lundberg, A. & Stuart, D. Propriospinal control of last order interneurones of spinal reflex pathways in the cat. Brain Res. 53, 227-231 (1973).
33. Raineteau, O., Fouad, K., Noth, P., Thallmair, M. & Schwab, M.E. Functional switch between motor tracts in the presence of the mAb IN-1 in the adult rat. Proc. Natl. Acad. Sci. USA 98, 6929-6934 (2001).
34. Bareyre, F.M., Haudenschild, B. & Schwab, M.E. Long-lasting sprouting and gene expression changes induced by the monoclonal antibody IN-1 in the adult spinal cord. J. Neurosci. 22, 7097-7110 (2002).
35. Gordon, T., Yang, J.F., Ayer, K., Stein, R.B. & Tyreman, N. Recovery potential of muscle after partial denervation: a comparison between rats and humans. Brain Res. Bull. 30, 477-482 (1993).
36. Card, J.P. et al. Neurotropic properties of pseudorabies virus: uptake and transneuronal passage in the rat central nervous system. J. Neurosci. 10, 1974-1994 (1990).
37. Strack, A.M., Sawyer, W.B., Platt, K.B. & Loewy, A.D. CNS cell groups regulating the sympathetic outflow to adrenal gland as revealed by transneuronal cell body labeling with pseudorabies virus. Brain Res. 491, 274-296 (1989).
38. Steward, O., Zheng, B. & Tessier-Lavigne, M. False resurrections: Distinguishing regenerated from spared axons in the injured central nervous system. J. Comp. Neurol. 459, 1-8 (2003).
39. Sloan, T.B. Anesthetic effects on electrophysiologic recordings. J. Clin. Neurophysiol. 15, 217-226 (1998).
40. Sanes, J.N., Suner, S. & Donoghue, J.P. Dynamic organization of primary motor cortex output to target muscles in adult rats. I. Long-term patterns of reorganization following motor or mixed peripheral nerve lesions. Exp. Brain Res. 79, 479-491 (1990).
41. Donoghue, J.P. Plasticity of adult sensorimotor representations. Curr. Opin. Neurobiol. 5, 749-754 (1995).
42. Kaas, J.H., Florence, S.L. & Jain, N. Subcortical contributions to massive cortical reorganizations. Neuron 22, 657-660 (1999).
43. Bruehlmeier, M. et al. How does the human brain deal with a spinal cord injury? Eur. J. Neurosci. 10, 3918-3922 (1998).
44. Chen, R., Corwell, B., Yaseen, Z., Hallett, M. & Cohen, L.G. Mechanisms of cortical reorganization in lower-limb amputees. J. Neurosci. 18, 3443-3450 (1998).
45. Nguyen, Q.T., Sanes, J.R. & Lichtman, J.W. Pre-existing pathways promote precise projection patterns. Nat. Neurosci. 5, 861-867 (2002).
46. Schnell, L. & Schwab, M.E. Sprouting and regeneration of lesioned corticospinal tract fibres in the adult rat spinal cord. Eur. J. Neurosci. 5, 1156-1171 (1993).
47. Merkler, D. et al. Locomotor recovery in spinal cord-injured rats treated with an antibody neutralizing the myelin-associated neurite growth inhibitor Nogo-A. J. Neurosci. 21, 3665-3673 (2001).
48. Jons, A. & Mettenleiter, T.C. Green fluorescent protein expressed by recombinant pseudorabies virus as an in vivo marker for viral replication. J. Virol. Methods 66, 283-292 (1997).
49. Herzog, A. & Brosamle, C. 'Semifree-floating' treatment: a simple and fast method to process consecutive sections for immunohistochemistry and neuronal tracing. J. Neurosci. Methods 72, 57-63 (1997).
50. Roof, R.L., Schielke, G.P., Ren, X. & Hall, E.D. A comparison of long-term functional outcome after 2 middle cerebral artery occlusion models in rats. Stroke 32, 2648-2657 (2001).