Sprouting of primary afferent fibers after spinal cord transection in the rat

Neuroscience

Volumn 85, Issue 2, 1998, Pages 443-458

  Krenz, N R ^a   Weaver, L C ^a  

^a ROBARTS RESEARCH INSTITUTE   (Canada)

Author keywords

Autonomic dysreflexia; Muscle spasticity; Myelinated primary afferent fibers; Spinal cord injury; Sympathetic preganglionic neurons; Unmyelinated primary afferent fibers

Indexed keywords

CALCITONIN GENE RELATED PEPTIDE; CHOLERA TOXIN B SUBUNIT;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTONOMIC NERVE; CONTROLLED STUDY; HYPERREFLEXIA; INTERNEURON; MALE; MOTONEURON; NONHUMAN; PRIORITY JOURNAL; RAT; SENSORY NERVE; SPINAL CORD TRANSSECTION; SPINAL GANGLION;

ANIMALS; CALCITONIN GENE-RELATED PEPTIDE; CELL DIVISION; CHOLERA TOXIN; FLUORESCENT DYES; GANGLIA, SPINAL; IMMUNOHISTOCHEMISTRY; MALE; NERVE FIBERS, MYELINATED; NEURAL PATHWAYS; NEURONS, AFFERENT; PEPTIDE FRAGMENTS; RATS; RATS, WISTAR; RHIZOTOMY; SPINAL CORD;

EID: 0032495838     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(97)00622-2     Document Type: Article

References (72)

1. Arvidsson U., Cullheim S., Ulfhake B., Hokfelt T., Terenius L. Altered levels of calcitonin gene-related peptide (CGRP)-like immunoreactivity of cat lumbar motoneurons after chronic spinal cord transection. Brain Res. 489:1989;387-391.
2. Averill S., McMahon S. B., Clary D. O., Reichardt L. F., Priestley J. V. Immunocytochemical localization of trkA receptors in chemically identified subgroups of adult rat sensory neurons. Eur. J. Neurosci. 4:1995;1484-1494.
3. Bakhit C., Armanini M., Wong W. L. T., Bennett G. L., Wrathall J. R. Increase in nerve growth factor-like immunoreactivity and decrease in choline acetyltransferase following contusive spinal cord injury. Brain Res. 554:1991;264-271.
4. Barrett C. P., Donati E. J., Guth L. Differences between adult and neonatal rats in their astroglial response to spinal injury. Expl Neurol. 84:1984;374-385.
5. Barron K. D. (1983) Comparative observations on the cytologic reactions of central and peripheral nerve cells to axotomy. In Spinal Cord Reconstruction (eds Kao C. C., Bunge R. P. and Reier P. J.), pp. 7-40. Raven, New York.
6. Bovolenta P., Mason C. Growth cone morphology varies with position in the developing mouse visual pathway from retina to first targets. J. Neurosci. 7:1987;1447-1460.
7. Burke D. (1988) Spasticity as an adaptation to pyramidal tract injury. In Advances in Neurology: Functional Recovery in Neurological Disease (ed. Waxman S. G.), pp. 401-423. Raven, New York.
8. Christensen M. D., Hulsebosch C. E. Distribution of GAP-43 expression in the spinal cord following low thoracic hemisection. Soc. Neurosci. Abstr. 20:1994;660.
9. Chung K., Lee W. T., Carlton S. M. The effects of dorsal rhizotomy and spinal cord isolation on calcitonin gene-related peptide-labeled terminals in the rat lumbar dorsal horn. Neurosci. Lett. 90:1988;27-32.
10. Chung K., Lee W. T., Park M. J. Spinal projections of pelvic visceral afferents of the rat: a calcitonin gene-related peptide (CGRP) immunohistochemical study. J. comp. Neurol. 337:1993;63-69.
11. De Groat W. C. Mechanisms underlying the recovery of lower urinary tract function following spinal cord injury. Paraplegia. 33:1995;493-505.
12. El-Bohy A., LaMotte C. C. Deafferentation-induced changes in neuropeptides of the adult rat dorsal horn following pronase injection of the sciatic nerve. J. comp. Neurol. 336:1993;545-554.
13. Elwood H. (1980) Organization of the spinal cord and its reflexes. In Medical Physiology (ed. Mountcastle V. B.), pp. 762-786. C. V. Mosby, St Louis, MO.
14. Gibson S. J., Polak J. M., Bloom S. R., Sabate I. M., Mulderry P. M., Ghatei M. A., McGregor G. P., Morrison I. M., Kelly J. S., Evans R. M., Rosenfeld M. G. Calcitonin gene-related peptide immunoreactivity in the spinal cord of man and of eight other species. J. Neurosci. 4:1984;3101-3111.
15. Godement P., Vanselow J., Thanos S., Bonhoeffer F. A study in developing visual systems with a new method of staining neurones and their processes in fixed tissue. Development. 101:1987;697-713.
16. Goldberger M. E. The use of behavioral methods to predict spinal cord plasticity. J. restor. Neurol. Neurosci. 2:1991;339-350.
17. Goldberger M. E. and Murray M. (1988) Patterns of sprouting and implications for recovery of function. In Functional Recovery in Neurological Disease (ed. Waxman S. G.), pp. 361-385. Raven, New York.
18. Goldberger M. E., Murray M. and Tessler A. (1993) Sprouting and regeneration in the spinal cord. Their roles in recovery of function after spinal cord injury. In Neuroregeneration (ed. Gorio A.), pp. 241-264. Raven, New York.
19. Harburn K. L., Potter P. Spasticity and contractures. Phys. Med. Rehab. 7:1993;1-20.
20. Helgren M. E., Goldberger M. E. The recovery of postural reflexes and locomotion following low thoracic hemisection in adult cats involves compensation by undamaged primary afferent pathways. Expl Neurol. 123:1993;17-34.
21. Hory-Lee F., Russell M., Lindsay R. M., Frank E. Neurotrophin 3 supports the survival of developing muscle sensory neurons in culture. Proc. natn. Acad. Sci. U.S.A. 90:1993;2613-2617.
22. Hulsebosch C. E., Coggeshall R. E. A comparison of axonal numbers in dorsal roots following spinal cord hemisection in neonate and adult rats. Brain Res. 265:1983;187-197.
23. Inaishi Y., Kashihara Y., Sakaguchi M., Nawa H., Kuno M. Cooperative regulation of calcitonin-gene related peptide levels in rat sensory neurons via their central and peripheral processes. J. Neurosci. 12:1992;518-524.
24. Ju G., Hokfelt T., Brodin E., Fahrenkrug J., Fischer J. A., Frey P., Elde R. P., Brown J. C. Primary sensory neurons of the rat showing calcitonin gene-related peptide immunoreactivity and their relation to substance P-, somatostatin-, galanin-, vasoactive intestinal polypeptide- and cholecystokinin-immunoreactive ganglion cells. Cell Tiss. Res. 247:1987;417-431.
25. Krassioukov A. V., Weaver L. C. Episodic hypertension due to autonomic dysreflexia in acute and chronic spinal cord-injured rats. Am. J. Physiol. 268:1995;H2077-H2083.
26. Krassioukov A. V., Weaver L. C. Morphological changes in sympathetic preganglionic neurons after spinal cord injury in rats. Neuroscience. 70:1996;211-226.
27. Krenz N. R., Weaver L. C. CGRP expression increases in the ventral horn rostral to spinal cord transection. NeuroReport. 7:1996;2859-2862.
28. Krenz N. R., Weaver L. C. (1998) Changes in the morphology of sympathetic preganglionic neurons parallel the development of autonomic dysreflexia after spinal cord injury. Neurosci. Lett. (in press).
29. Kruse M. N., De Groat W. C. Changes in lower urinary tract function following spinal cord injury. J. Restor. Neurol. Neurosci. 5:1993;79-80.
30. Kuffler D. P. Long-term survival and sprouting in culture by motoneurons isolated from the spinal cord of adult frogs. J. comp. Neurol. 302:1990;729-738.
31. LaMotte C. C., Kapadia S. E. Deafferentation-induced terminal field expansion of myelinated saphenous afferents in the adult rat dorsal horn and nucleus gracilis following pronase injection of the sciatic nerve. J. comp. Neurol. 330:1993;83-94.
32. LaMotte C. C., Kapadia S. E., Shapiro C. M. Central projections of the sciatic, saphenous, median, and ulnar nerves of the rat demonstrated by transganglionic transport of choleragenoid-HRP (B-HRP) and wheat germ agglutinin-HRP (WGA-HRP). J. comp. Neurol. 311:1991;546-562.
33. Laskey W., Schondorf R., Polosa C. Intersegmental connections and interactions of myelinated somatic and visceral afferents with sympathetic preganglionic neurons in the unanaesthetized spinal cat. J. auton. nerv. Syst. 1:1979;69-76.
34. Lee B. Y., Karmakar M. G., Herz B. L., Sturgill R. A. Autonomic dysreflexia revisited. J. Spinal Cord Med. 18:1994;75-87.
35. Lindsay R. M., Harmar A. J. Nerve growth factor regulates expression of neuropeptide genes in adult sensory neurons. Nature. 337:1989;362-364.
36. 1 on scar production in the injured central nervous system of the rat. Eur. J. Neurosci. 6:1994;355-363.
37. Maiorov D. N., Krenz N. R., Krassioukov A. V., Weaver L. C. Role of spinal NMDA and AMPA receptors in episodic hypertension in conscious spinal rats. Am. J. Physiol. 273:1997;H1266-H1274.
38. Massari V. J., Tizabi T., Park C. H., Moody T. W., Helke C. J., O'Donohue T. L. Distribution and origin of bombesin, substance P and somatostatin in cat spinal cord. Peptides. 4:1983;673-681.
39. Mathias C. J., Frankel H. L. Cardiovascular control in spinal man. A. Rev. Physiol. 50:1988;577-592.
40. Mathias C. J. and Frankel H. L. (1992) The cardiovascular system in tetraplegia and paraplegia. In Handbook of Clinical Neurology (ed. Frankel H. L.), pp. 435-456. Elsevier Science, Amsterdam.
41. McMahon S. B., Kett-White R. Sprouting of peripherally regenerating primary sensory neurons in the adult central nervous system. J. comp. Neurol. 304:1991;307-315.
42. Molander C., Grant G. Laminar distribution and somatotopic organization of primary afferent fibres from hindlimb nerves in the dorsal horn. A study by transganglionic transport of horseradish peroxidase in the rat. Neuroscience. 19:1986;297-312.
43. Murray M. (1983) Axonal sprouting in response to dorsal rhizotomy. In Spinal Cord Reconstruction (eds Kao C. C., Bunge R. P. and Reier P. J.), pp. 445-453. Raven, New York.
44. Murray M., Goldberger M. E. Restitution of function and collateral sprouting in the cat spinal cord: the partially hemisected animal. J. comp. Neurol. 158:1974;19-36.
45. Nacimiento W., Mautes A., Töpper R., Oestreicher A. B., Gispen W. H., Nacimiento A. C., Noth J., Kreutzberg G. W. B-50 (GAP-43) in the spinal cord caudal to hemisection: indication for lack of intraspinal sprouting in dorsal root axons. J. Neurosci. Res. 35:1993;603-617.
46. Nacimiento W., Sappok T., Brook G. A., Toth L., Oestreicher A. B., Gispen W. H., Noth J., Kreutzberg G. W. B-50 (GAP-43) in the rat spinal cord caudal to hemisection: lack of intraspinal sprouting by dorsal root axons. Neurosci. Lett. 194:1995;13-16.
47. Naftchi N. E., Abrahams S. J., St. Paul H. M., Lowman E. W., Schlosser W. Localization and changes of substance P in spinal cord of paraplegic cats. Brain Res. 153:1978;507-513.
48. Nelson S. G., Mendell L. M. Enhancement in Ia-motoneuron synaptic transmission caudal to chronic spinal cord transection. J. Neurophysiol. 42:1979;624-654.
49. Neugebauer V., Rumenapp P., Schaible H.-G. Calcitonin gene-related peptide is involved in the spinal processing of mechanosensory input from the rat's knee joint and in the generation and maintenance of hyperexcitability of dorsal horn neurons during development of acute inflammation. Neuroscience. 71:1996;1095-1109.
50. Neumann S., Doubell T. P., Leslie T., Woolf C. J. Inflammatory pain hypersensitivity mediated by phenotypic switch in myelinated primary sensory neurons. Nature. 384:1996;360-364.
51. Ogawa T., Kanazawa I., Kimura S. Regional distribution of substance P, neurokinin alpha and neurokinin beta in rat spinal cord, nerve roots and dorsal root ganglia, and the effects of dorsal root section or spinal transection. Brain Res. 359:1985;152-157.
52. Osborn J. W., Taylor R. F., Schramm L. P. Chronic cervical spinal cord injury and autonomic hyperreflexia in rats. Am. J. Physiol. 258:1990;R169-R174.
53. Piehl F., Arvidsson U., Johnson H., Cullheim S., Villar M., Dagerlind A., Terenius L., Hokfelt T., Ulfhake B. Calcitonin gene-related peptide (CGRP)-like immunoreactivity and CGRP mRNA in rat spinal cord motoneurons after different types of lesions. Eur. J. Neurosci. 3:1991;737-757.
54. Rivero-Melian C., Grant G. Choleragenoid horseradish peroxidase used for studying projections of some hindlimb cutaneous nerves and plantar foot afferents to the dorsal horn and Clarke's column in the rat. Expl Brain Res. 84:1991;125-132.
55. Rivero-Melian C., Rosario C., Grant G. Demonstration of transganglionically transported choleragenoid in rat spinal cord by immunofluorescence cytochemistry. Neurosci. Lett. 145:1992;114-117.
56. Robertson B., Perry M. J., Lawson S. N. Populations of rat spinal primary afferent neurons with choleragenoid binding compared with those labelled by markers for neurofilament and carbohydrate groups: a quantitative immunocytochemical study. J. Neurocytol. 20:1990;387-395.
57. Sakaguchi M., Inaishi Y., Kashihara Y., Kuno M. Degeneration of motor nerve fibers enhances the expression of calcitonin gene-related peptide in rat sensory neurons. Neurosci. Lett. 137:1992;61-64.
58. Sanner C. A., Cunningham T. J., Goldberger M. E. NMDA receptor blockade rescues Clarke's and red nucleus neurons after spinal hemisection. J. Neurosci. 14:1994;6472-6480.
59. Sanner C. A., Murray M., Goldberger M. E. Removal of dorsal root afferents prevents retrograde death of axotomized Clarke's nucleus neurons in the cat. Expl Neurol. 123:1993;81-90.
60. Sato A., Schmidt R. F. Somatosympathetic reflexes: afferent fibers, central pathways, discharge characteristics. Physiol. Rev. 53:1973;916-947.
61. Sharkey K. A., Sobrino J. A., Cervero F., Varro A., Dockray G. J. Visceral and somatic afferent origin of calcitonin gene-related peptide immunoreactivity in the lower thoracic spinal cord of the rat. Neuroscience. 32:1989;169-179.
62. Skofitsch G., Jacobowitz D. M. Calcitonin gene-related peptide: detailed immunohistochemical distribution in the central nervous system. Peptides. 6:1985;721-745.
63. Skofitsch G., Jacobowitz D. M. Quantitative distribution of calcitonin gene-related peptide in the rat central nervous system. Peptides. 6:1985;1069-1073.
64. Smith G. D., Seckl J. R., Harmar A. J. Distribution of neuropeptides in dorsal root ganglia of the rat; substance P, somatostatin and calcitonin gene-related peptide. Neurosci. Lett. 153:1993;5-8.
65. Sokol R. R. and Rohlf F. J. (1981) Biometry: The Principles and Practice of Statistics in Biological Research. W. H. Freeman, San Francisco.
66. Thor K., Kawatani M. and De Groat W. C. (1986) Plasticity in the reflex pathways to the lower urinary tract of the cat during postnatal development and following spinal cord injury. In Development and Plasticity of the Mammalian Spinal Cord (eds Goldberger M. E., Gorio A. and Murray M.), pp. 65-80. Liviana, Padova.
67. Tuszynski M. H., Gabriel K., Gage F. H., Suhr S., Meyer S., Rosetti A. Nerve growth factor delivery by gene transfer induces differential outgrowth of sensory, motor, and noradrenergic neurites after adult spinal cord injury. Expl Neurol. 137:1996;157-173.
68. Vita G., Hawkins E. F., Engel W. K. Effects of experimental spinal cord transection on substance P receptors: a quantitative autoradiography study. Neuropeptides. 17:1990;147-153.
69. Weaver L. C., Cassam A. K., Krassioukov A. V., Llewellyn-Smith I. J. Changes in immunoreactivity for growth associated protein-43 suggest reorganization of synapses on spinal sympathetic neurons after cord transection. Neuroscience. 81:1997;535-551.
70. Wilson P., Kitchener P. D. Plasticity of cutaneous primary afferent projections to the spinal dorsal horn. Prog. Neurobiol. 48:1996;105-129.
71. Woolf C. J., Fitzgerald M. Somatotopic organization of cutaneous afferent terminals and dorsal horn neuronal receptive fields in the superficial and deep laminae of the rat lumbar spinal cord. J. comp. Neurol. 251:1986;517-531.
72. Zhou X.-F., Rush R. A. Localization of neurotrophin-3-like immunoreactivity in peripheral tissues of the rat. Brain Res. 621:1993;189-199.