Restorative respiratory pathways after partial cervical spinal cord injury: Role of ipsilateral phrenic afferents

European Journal of Neuroscience

Volumn 25, Issue 12, 2007, Pages 3551-3560

  Vinit, Stéphane ^a   Stamegna, Jean Claude ^a   Boulenguez, Pascale ^a   Gauthier, Patrick ^a   Kastner, Anne ^a  

^a AIX MARSEILLE UNIVERSITY   (France)

Author keywords

Crossed phrenic pathways; Plasticity; Rat; Respiratory network; Rewiring; Spinal cord injury

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CERVICAL SPINAL CORD INJURY; CERVICAL SPINE; CONTROLLED STUDY; DIAPHRAGM PARALYSIS; ELECTROPHYSIOLOGY; FEMALE; GANGLION; NERVE CELL PLASTICITY; NERVE CONDUCTION; NONHUMAN; PHRENIC NERVE; PHRENICOTOMY; PRIORITY JOURNAL; RAT; RESPIRATORY FUNCTION; SENSORY NERVE CONDUCTION; SURGICAL TECHNIQUE;

AFFERENT PATHWAYS; ANIMALS; CERVICAL VERTEBRAE; FEMALE; FUNCTIONAL LATERALITY; MODELS, BIOLOGICAL; PHRENIC NERVE; RATS; RATS, SPRAGUE-DAWLEY; RECOVERY OF FUNCTION; RESPIRATORY MECHANICS; SPINAL CORD INJURIES; STILBAMIDINES; TIME FACTORS;

EID: 34347387118     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2007.05619.x     Document Type: Article

References (51)

1. Bareyre, F.M., Kerschensteiner, M., Raineteau, O., Mettenleiter, T.C., Weinmann, O. Schwab, M.E. (2004) The injured spinal cord spontaneously forms a new intraspinal circuit in adult rats. Nat. Neurosci., 7, 269 277.
2. Boulenguez, P., Gauthier, P. Kastner, A. (2007) Respiratory neuron subpopulations and pathways potentially involved in the reactivation of phrenic motoneurons after C2 hemisection. Brain Res., 1148, 96 104.
3. Bouyer, L.J.G. Rossignol, S. (2003) Contribution of cutaneous inputs from the hindpaw to the control of locomotion. II. Spinal cats. J. Neurophysiol., 90, 3640 3653.
4. Corda, M., von Euler, C. Lennerstrand, G. (1965) Proprioceptive innervation of the diaphragm. J. Physiol. (Lond.), 178, 161 177.
5. Dobbins, E.G. Feldman, J.L. (1994) Brainstem network controlling descending drive to phrenic motoneurons in rat. J. Comp. Neurol., 347, 64 86.
6. Duffin, J. Li, Y.M. (2006) Transmission of respiratory rhythm: midline-crossing connections at the level of the phrenic motor nucleus? Respir. Physiol. Neurobiol., 153, 139 147.
7. Edgerton, V.R., Tillakaratne, N.J., Bigbee, A.J., de Leon, E.D. Roy, R.R. (2004) Plasticity of the spinal neural circuitry after injury. Annu. Rev. Neurosci., 27, 145 167.
8. Erickson, B.K., Forster, H.V., Lowry, T.F., Pan, L.G., Korducki, M.J., Forster, A.L. Forster, M.A. (1994) Changes in respiratory muscle activity in ponies when end-expiratory lung volume is increased. J. Appl. Physiol., 76, 2015 2025.
9. Feldman, J.L., Loewy, A.D. Speck, D.F. (1985) Projections from the ventral respiratory group to phrenic and intercostals motoneurons in cat: an autoradiographic study. J. Neurosci., 5, 1993 2000.
10. Forster, H.V. (2003) Plasticity in the control of breathing following sensory denervation. J. Appl. Physiol., 94, 784 794.
11. Frigon, A. Rossignol, S. (2006) Functional plasticity following spinal cord lesions. Prog. Brain. Res., 157, 231 260.
12. Fuller, D.D., Golder, F.J., Olson, E.B. Jr. Mitchell, G.S. (2006) Recovery of phrenic activity and ventilation after cervical spinal hemisection in rats. J. Appl. Physiol., 100, 800 806.
13. Fuller, D.D., Johnson, S.M., Johnson, R.A. Mitchell, G.S. (2002) Chronic cervical spinal sensory denervation reveals ineffective spinal pathways to phrenic motoneurons in the rat. Neurosci. Lett., 323, 25 28.
14. Fuller, D.D., Johnson, S.M., Olson, E.B. Jr. Mitchell, G.S. (2003) Synaptic pathways to phrenic motoneurons are enhanced by chronic intermittent hypoxia after cervical spinal cord injury. J. Neurosci., 23, 2993 3000.
15. Gauthier, P., Rega, P., Lammari-Barreault, N. Polentes, J. (2002) 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, 65 81.
16. Golder, F.J., Fuller, D.D., Davenport, P.W., Johnson, R.D., Reier, P.J. Bolser, D.C. (2003) Respiratory motor recovery after unilateral spinal cord injury: eliminating crossed phrenic activity decreases tidal volume and increases contralateral respiratory motor output. J. Neurosci., 23, 2494 2501.
17. Golder, F.J. Mitchell, G.S. (2005) Spinal synaptic enhancement with acute intermittent hypoxia improves respiratory function after chronic cervical spinal cord injury. J. Neurosci., 25, 2925 2932.
18. Golder, F.J., Reier, P.J. Bolser, D.C. (2001) Altered respiratory motor drive after spinal cord injury: supraspinal and bilateral effects of a unilateral lesion. J. Neurosci., 21, 8680 8689.
19. Goshgarian, H.G., Ellenberger, H.H. Feldman, J.L. (1991) Decussation of bulbospinal respiratory axons at the level of the phrenic nuclei in adult rats: a possible substrate for the crossed phrenic phenomenon. Exp. Neurol., 111, 135 139.
20. Goshgarian, H.G. (1981) The role of cervical afferent nerve fiber inhibition of the crossed phrenic phenomenon. Exp. Neurol., 72, 211 225.
21. Goshgarian, H.G. (2003) The crossed phrenic phenomenon: a model for plasticity in the respiratory pathways following spinal cord injury. J. Appl. Physiol., 94, 795 810.
22. Greer, J.J., Allan, D.W., Martin-Caraballo, M. Lemke, R.P. (1999) An overview of phrenic nerve and diaphragm muscle development in the perinatal rat. J. Appl. Physiol., 86, 779 786.
23. Hagg, T. (2006) Collateral sprouting as a target for improved function after spinal cord injury. J. Neurotrauma, 23, 281 294.
24. Hagg, T. Oudega, M. (2006) Degenerative and spontaneous regenerative processes after spinal cord injury. J. Neurotrauma, 3/4, 264 280.
25. Harel, N.Y. Strittmatter, S.M. (2006) Can regenerating axons recapitulate developmental guidance during recovery from spinal cord injury? Nat. Rev. Neurosci., 7, 603 616.
26. Hilaire, G. Monteau, R. (1997) Brainstem and spinal control of respiratory muscles during breathing. In Miller, A.D., Bianchi, A.L. Bishop, B.P. (Eds), Neural Control of the Respiratory Muscles. CRC Press, New York, pp. 91 105.
27. Hussain, S.N., Magder, S., Chatillon, A. Roussos, C. (1990) Chemical activation of thin-fiber phrenic afferents: respiratory responses. J. Appl. Physiol., 69, 1002 1011.
28. Lewis, L.J. Brookhart, J.M. (1951) Significance of the crossed phrenic phenomenon. Am. J. Physiol., 166, 241 254.
29. Li, Y., Decherchi, P. Raisman, G. (2003) Transplantation of olfactory ensheathing cells into spinal cord lesions restores breathing and climbing. J. Neurosci., 23, 727 731.
30. Ling, L., Bach, K.B. Mitchell, G.S. (1994) Serotonin reveals ineffective spinal pathways to contralateral phrenic motoneurons in spinally hemisected rats. Exp. Brain Res., 101, 35 43.
31. Liou, W.W. Goshgarian, H.G. (1994) Quantitative assessment of the effect of chronic phrenicotomy on the induction of the crossed phrenic phenomenon. Exp. Neurol., 127, 145 153.
32. Lipski, J.X., Zhang, B., Kruszewska, B. Kanjhan, R. (1994) Morphological study of long axonal projections of ventral medullary inspiratory neurons in the rat. Brain Res., 640, 171 184.
33. Minor, K.H., Akison, L.K., Goshgarian, H.G. Seeds, N.W. (2006) Spinal cord injury-induced plasticity in the mouse - the crossed phrenic phenomenon. Exp. Neurol., 200, 486 495.
34. Mitchell, G.S. Johnson, S.M. (2003) Neuroplasticity in respiratory motor control. J. Appl. Physiol., 94, 358 374.
35. Moreno, D.E., Yu, X.J. Goshgarian, H.G. (1992) Identification of the axon pathways which mediate functional recovery of a paralyzed hemidiaphragm following spinal cord hemisection in the adult rat. Exp. Neurol., 116, 219 228.
36. Nantwi, K.D., El-Bohy, A.A., Schrimsher, G.W., Reier, P.J. Goshgarian, H.G. (1999) Spontaneous functional recovery in a paralyzed hemidiaphragm following upper cervical spinal cord injury in adult rats. Neurorehab. Neural Report, 13, 225 234.
37. Onai, T., Saji, M. Miura, M. (1987) Projections of supraspinal structures to the phrenic motor nucleus in rats studied by a horseradish peroxidase microinjection method. J. Auton. Nerv. Syst., 21, 233 239.
38. Oo, T., Watt, J.W., Soni, B.M. Sett, P.K. (1999) 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, 117 122.
39. Polentes, J., Stamegna, J.C., Nieto-Sampedro, M. Gauthier, P. (2004) Phrenic rehabilitation and diaphragm recovery after cervical injury and transplantation of olfactory ensheathing cells. Neurobiol. Dis., 16, 638 653.
40. Porter, W.T. (1895) The path of the respiratory impulse from the bulb to the phrenic nuclei. J. Physiol., 17, 455 485.
41. Raineteau, O. Schwab, M.E. (2001) Plasticity of motor systems after incomplete spinal cord injury. Nat. Rev. Neurosci., 2, 263 273.
42. Road, J.D. (1990) Phrenic afferents and ventilatory control. Lung, 168, 137 149.
43. Song, A., Tracey, D.J. Ashwell, K.W. (1999) Development of the rat phrenic nerve and the terminal distribution of phrenic afferents in the cervical cord. Anat. Embryol., 200, 625 643.
44. Teitelbaum, J., Vanelli, G. Hussain, S.N. (1993) Thin-fiber phrenic afferents mediate the ventilatory response to diaphragmatic ischaemia. Respir. Physiol., 91, 195 206.
45. Vinit, S., Boulenguez, P., Efthimiadi, L., Stamegna, J.C., Gauthier, P. Kastner, A. (2005) Axotomized bulbospinal neurons express c-Jun after cervical spinal cord injury. Neuroreport, 16, 1535 1539.
46. Vinit, S., Gauthier, P., Stamegna, J.C. Kastner, A. (2006) High cervical lateral spinal cord injury results in long-term ipsilateral hemidiaphragm paralysis. J. Neurotrauma, 23, 1137 1146.
47. Weidner, N., Ner, A., Salimi, N. Tuszynski, M.H. (2001) Spontaneous corticospinal axonal plasticity and functional recovery after adult central nervous system injury. PNAS, 98, 3513 3518.
48. Winslow, C. Rozovsky, J. (2003) Effect of spinal cord injury on the respiratory system. Am. J. Phys. Med. Rehabil., 82, 803 814.
49. Yu, J. Younes, M. (1999) Powerful respiratory stimulation by thin muscle afferents. Respir. Physiol., 117, 1 12.
50. Zhou, S.Y., Basura, G.J. Goshgarian, H.G. (2001) Serotonin(2) receptors mediate respiratory recovery after spinal cord hemisection in adult rats. J. Appl. Physiol., 91, 2665 2673.
51. Zimmer, M.B. Goshgarian, H.G. (2007) GABA, not glycine, mediates inhibition of latent respiratory motor pathways after spinal cord injury. Exp. Neurol., 203, 493 501.