Plasticity of lumbosacral propriospinal neurons is associated with the development of autonomic dysreflexia after thoracic spinal cord transection

Journal of Comparative Neurology

Volumn 509, Issue 4, 2008, Pages 382-399

  Hou, Shaoping ^a   Duale, Hanad ^a   Cameron, Adrian A ^a,b   Abshire, Sarah M ^a   Lyttle, Travis S ^a   Rabchevsky, Alexander G ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

c Fos; Colorectal distension; Dorsal commissural nucleus; Dorsal gray commissure; Hypertension; Neuronal tracers; Stereology

Indexed keywords

AMINE; BIOTINYLATED DEXTRAN AMINE; CHOLERA TOXIN; FAST BLUE; NERVE GROWTH FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; AUTONOMIC DYSREFLEXIA; CONTROLLED STUDY; DISEASE COURSE; FEMALE; GENE OVEREXPRESSION; GRAY MATTER; IMMUNOHISTOCHEMISTRY; NERVE CELL PLASTICITY; NERVE SPROUTING; NONHUMAN; ONCOGENE C FOS; PREGANGLIONIC NERVE CELL; PRIORITY JOURNAL; RAT; SPINAL CORD INJURY; SPINAL CORD NERVE CELL; SPINAL CORD TRANSSECTION; THORACIC SPINAL CORD;

AFFERENT PATHWAYS; ANIMALS; ANTIBODIES; AUTONOMIC DYSREFLEXIA; BIOTIN; CHOLINE O-ACETYLTRANSFERASE; DEXTRANS; DISEASE MODELS, ANIMAL; ENKEPHALINS; FEMALE; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; LUMBOSACRAL REGION; NERVE FIBERS; NEURONAL PLASTICITY; NEURONS; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, WISTAR; SPINAL CORD; SPINAL CORD INJURIES;

EID: 48249111069     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.21771     Document Type: Article

References (72)

1. Abercrombie M, Johnson ML. 1946. Quantitative histology of Wallerian degeneration: I. Nuclear population in rabbit sciatic nerve. J Anat 80:37-50.
2. Al-Chaer ED, Lawand NB, Westlund KN, Willis WD. 1996. Pelvic visceral input into the nucleus gracilis is largely mediated by the postsynaptic dorsal column pathway. J Neurophysiol 76:2675-2690.
3. Anderson CR, Edwards SL. 1994. Intraperitoneal injections of Fluorogold reliably labels all sympathetic preganglionic neurons in the rat. J Neurosci Methods 53:137-141.
4. Bacon SJ, Smith AD. 1988. Preganglionic sympathetic neurones innervating the rat adrenal medulla: immunocytochemical evidence of synaptic input from nerve terminals containing substance P, GABA or 5-hydroxytryptamine. J Auton Nerv Syst 24:97-122.
5. Brown A, Ricci MJ, Weaver LC. 2004. NGF message and protein distribution in the injured rat spinal cord. Exp Neurol 188:115-127.
6. Cameron AA, Smith GM, Randall DC, Brown DR, Rabchevsky AG. 2006. Genetic manipulation of intraspinal plasticity after spinal cord injury alters the severity of autonomic dysreflexia. J Neurosci 26:2923-2932.
7. Chau D, Johns DG, Schramm LP. 2000. Ongoing and stimulus-evoked activity of sympathetically correlated neurons in the intermediate zone and dorsal horn of acutely spinalized rats. J Neurophysiol 83:2699-2707.
8. Chung K, Coggeshall RE. 1983. Propriospinal fibers in the rat. J Comp Neurol 217:47-53.
9. Cuello AC, Milstein C, Couture R, Wright B, Priestley JV, Jarvis J. 1984. Characterization and immunocytochemical application of monoclonal antibodies against enkephalins. J Histochem Cytochem 32:947-957.
10. Dampney RA. 1994. Functional organization of central pathways regulating the cardiovascular system. Physiol Rev 74:323-364.
11. De Biasi S, Rustioni A. 1988. Glutamate and substance P coexist in primary afferent terminals in the superficial laminae of spinal cord. Proc Natl Acad Sci U S A 85:7820-7824.
12. Diaz-Ruiz A, Salgado-Ceballos H, Montes S, Maldonado V, Tristan L, Alcaraz-Zubeldia M, Rios C. 2007. Acute alterations of glutamate, glutamine, GABA, and other amino acids after spinal cord contusion in rats. Neurochem Res 32:57-63.
13. Dietz GW Jr, Salvaterra PM. 1980. Purification and peptide mapping of rat brain choline acetyltransferase. J Biol Chem 255:10612-10617.
14. Dragunow M, Faull R. 1989. The use of c-fos as a metabolic marker in neuronal pathway tracing. J Neurosci Methods 29:261-265.
15. Grider MH, Chen Q, Shine HD. 2006. Semi-automated quantification of axonal densities in labeled CNS tissue. J Neurosci Methods 155:172-179.
16. Guillery RW. 2002. On counting and counting errors. J Comp Neurol 447:1-7.
17. Hancock MB, Peveto CA. 1979. A preganglionic autonomic nucleus in the dorsal gray commissure of the lumbar spinal cord of the rat. J Comp Neurol 183:65-72.
18. Hirshberg RM, Al-Chaer ED, Lawand NB, Westlund KN, Willis WD. 1996. Is there a pathway in the posterior funiculus that signals visceral pain? Pain 67:291-305.
19. Holets V, Elde R. 1982. The differential distribution and relationship of serotoninergic and peptidergic fibers to sympathoadrenal neurons in the intermediolateral cell column of the rat: a combined retrograde axonal transport and immunofluorescence study. Neuroscience 7:1155-1174.
20. Hosoya Y, Nadelhaft I, Wang D, Kohno K. 1994. Thoracolumbar sympathetic preganglionic neurons in the dorsal commissural nucleus of the male rat: an immunohistochemical study using retrograde labeling of cholera toxin subunit B. Exp Brain Res 98:21-30.
21. Karlsson AK. 1999. Autonomic dysreflexia. Spinal Cord 37:383-391.
22. Krassioukov AV, Weaver LC. 1995. Episodic hypertension due to autonomic dysreflexia in acute and chronic spinal cord-injured rats. Am J Physiol 268:H2077-2083.
23. Krassioukov AV, Weaver LC. 1996. Morphological changes in sympathetic preganglionic neurons after spinal cord injury in rats. Neuroscience 70:211-225.
24. Krassioukov AV, Johns DG, Schramm LP. 2002. Sensitivity of sympathetically correlated spinal interneurons, renal sympathetic nerve activity, and arterial pressure to somatic and visceral stimuli after chronic spinal injury. J Neurotrauma 19:1521-1529.
25. Kratskin IL, Yu X, Doty RL. 1997. An easily constructed pipette for pressure microinjections into the brain. Brain Res Bull 44:199-203.
26. Krenz NR, Weaver LC. 1998a. Changes in the morphology of sympathetic preganglionic neurons parallel the development of autonomic dysreflexia after spinal cord injury in rats. Neurosci Lett 243:61-64.
27. Krenz NR, Weaver LC. 1998b. Sprouting of primary afferent fibers after spinal cord transection in the rat. Neuroscience 85:443-458.
28. Landrum LM, Jones SL, Blair RW. 2002. The expression of Fos-labeled spinal neurons in response to colorectal distension is enhanced after chronic spinal cord transection in the rat. Neuroscience 110:569-578.
29. Lindan R, Joiner E, Freehafer AA, Hazel C. 1980. Incidence and clinical features of autonomic dysreflexia in patients with spinal cord injury. Paraplegia 18:285-292.
30. Llewellyn-Smith IJ, Phend KD, Minson JB, Pilowsky PM, Chalmers JP. 1992. Glutamate-immunoreactive synapses on retrogradely labelled sympathetic preganglionic neurons in rat thoracic spinal cord. Brain Res 581:67-80.
31. Llewellyn-Smith IJ, Arnolda LF, Pilowsky PM, Chalmers JP, Minson JB. 1998. GABA- and glutamate-immunoreactive synapses on sympathetic preganglionic neurons projecting to the superior cervical ganglion. J Auton Nerv Syst 71:96-110.
32. Lu Y, Inokuchi H, McLachlan EM, Li JS, Higashi H. 2001. Correlation between electrophysiology and morphology of three groups of neuron in the dorsal commissural nucleus of lumbosacral spinal cord of mature rats studied in vitro. J Comp Neurol 437:156-169.
33. Marsh DR, Wong ST, Meakin SO, MacDonald JI, Hamilton EF, Weaver LC. 2002. Neutralizing intraspinal nerve growth factor with a trkA-IgG fusion protein blocks the development of autonomic dysreflexia in a clip-compression model of spinal cord injury. J Neurotrauma 19:1531-1541.
34. Masson RL Jr, Sparkes ML, Ritz LA. 1991. Descending projections to the rat sacrocaudal spinal cord. J Comp Neurol 307:120-130.
35. Matsushita M. 1998. Ascending propriospinal afferents to area X (substantia grisea centralis) of the spinal cord in the rat. Exp Brain Res 119:356-366.
36. Mayorov DN, Adams MA, Krassioukov AV. 2001. Telemetric blood pressure monitoring in conscious rats before and after compression injury of spinal cord. J Neurotrauma 18:727-736.
37. McCullers DL, Sullivan PG, Scheff SW, Herman JP. 2002. Mifepristone protects CA1 hippocampal neurons following traumatic brain injury in rat. Neuroscience 109:219-230.
38. Minson JB, Llewellyn-Smith IJ, Arnolda LF, Pilowsky PM, Oliver JR, Chalmers JP. 1994. Disinhibition of the rostral ventral medulla increases blood pressure and Fos expression in bulbospinal neurons. Brain Res 646:44-52.
39. Molander C, Xu Q, Grant G. 1984. The cytoarchitectonic organization of the spinal cord in the rat. I. The lower thoracic and lumbosacral cord. J Comp Neurol 230:133-141.
40. Molander C, Xu Q, Rivero-Melian C, Grant G. 1989. Cytoarchitectonic organization of the spinal cord in the rat: II. The cervical and upper thoracic cord. J Comp Neurol 289:375-385.
41. Morgan JI, Curran T. 1991. Stimulus-transcription coupling in the nervous system: involvement of the inducible protooncogenes fos and jun. Annu Rev Neurosci 14:421-451.
42. Ness TJ, Gebhart GF. 1987. Characterization of neuronal responses to noxious visceral and somatic stimuli in the medial lumbosacral spinal cord of the rat. J Neurophysiol 57:1867-1892.
43. Novikov LN. 2001. Labeling of central projections of primary afferents in adult rats: a comparison between biotinylated dextran amine, neurobiotin and Phaseolus vulgaris-leucoagglutinin. J Neurosci Methods 112:145-154.
44. Pan B, Kim EJ, Schramm LP. 2005. Increased close appositions between corticospinal tract axons and spinal sympathetic neurons after spinal cord injury in rats. J Neurotrauma 22:1399-1410.
45. Pan B, Zahner MR, Kulikowicz E, Schramm LP. 2007. Effects of corticospinal tract stimulation on renal sympathetic nerve activity in rats with intact and chronically lesioned spinal cords. Am J Physiol Regul Integr Comp Physiol 293:R178-R184.
46. Pandya JD, Pauly JR, Nukala VN, Sebastian AH, Day KM, Korde AS, Maragos WF, Hall ED, Sullivan PG. 2007. Post-injury administration of mitochondrial uncouplers increases tissue sparing and improves behavioral outcome following traumatic brain injury in rodents. J Neurotrauma 24:798-811.
47. Pascual JI, Insausti R, Gonzalo LM. 1993. Urinary bladder innervation in male rat: termination of primary afferents in the spinal cord as determined by transganglionic transport of WGA-HRP. J Urol 150:500-504.
48. Petkó M, Antal M. 2000. Propriospinal afferent and efferent connections of the lateral and medial areas of the dorsal horn (laminae I-IV) in the rat lumbar spinal cord. J Comp Neurol 422:312-325.
49. Preston GA, Lyon TT, Yin Y, Lang JE, Solomon G, Annab L, Srinivasan DG, Alcorta DA, Barrett JC. 1996. Induction of apoptosis by c-Fos protein. Mol Cell Biol 16:211-218.
50. Rabchevsky AG. 2006. Segmental organization of spinal reflexes mediating autonomic dysreflexia after spinal cord injury. Prog Brain Res 152:265-274.
51. Rabchevsky AG, Sullivan PG, Scheff SW. 2007. Temporal-spatial dynamics in oligodendrocyte and glial progenitor cell numbers throughout ventrolateral white matter following contusion spinal cord injury. Glia 55:831-843.
52. Rodriguez MJ, Robledo P, Andrade C, Mahy N. 2005. In vivo co-ordinated interactions between inhibitory systems to control glutamate-mediated hippocampal excitability. J Neurochem 95:651-661.
53. Romagnano MA, Braiman J, Loomis M, Hamill RW. 1987. Enkephalin fibers in autonomic nuclear regions: intraspinal vs. supraspinal origin. J Comp Neurol 266:319-331.
54. Sagar SM, Sharp FR, Curran T. 1988. Expression of c-fos protein in brain: metabolic mapping at the cellular level. Science 240:1328-1331.
55. Schwartz-Bloom RD, Sah R. 2001. Gamma-aminobutyric acid(A) neurotransmission and cerebral ischemia. J Neurochem 77:353-371.
56. Seki Y, Kanzaki R. 2008. Comprehensive morphological identification and GABA immunocytochemistry of antennal lobe local interneurons in Bombyx mori. J Comp Neurol 506:93-107.
57. Snow JC, Sideropoulos HP, Kripke BJ, Freed MM, Shah NK, Schlesinger RM. 1978. Autonomic hyperreflexia during cystoscopy in patients with high spinal cord injuries. Paraplegia 15:327-332.
58. Steward O, Zheng B, Banos K, Yee KM. 2007. Response to: Kim et al., "Axon regeneration in young adult mice lacking Nogo-A/B. Neuron 38:187-199." Neuron 54:191-195.
59. Sun D, Vingrys AJ, Kalloniatis M. 2007. Metabolic and functional profiling of the normal rat retina. J Comp Neurol 505:92-113.
60. Tang X, Neckel ND, Schramm LP. 2003. Locations and morphologies of sympathetically correlated neurons in the T(10) spinal segment of the rat. Brain Res 976:185-193.
61. Thor KB, Roppolo JR, Kawatani M, Erdman S, deGroat WC. 1994. Plasticity in spinal opioid control of lower urinary tract function in paraplegic cats. Neuroreport 5:1673-1678.
62. Todd AJ, McKenzie J. 1989. GABA-immunoreactive neurons in the dorsal horn of the rat spinal cord. Neuroscience 31:799-806.
63. Vizzard MA. 2000. Increased expression of spinal cord Fos protein induced by bladder stimulation after spinal cord injury. Am J Physiol Regul Integr Comp Physiol 279:R295-R305.
64. Wang CC, Willis WD, Westlund KN. 1999. Ascending projections from the area around the spinal cord central canal: a Phaseolus vulgaris leucoagglutinin study in rats. J Comp Neurol 415:341-367.
65. Weaver LC, Cassam AK, Krassioukov AV, Llewellyn-Smith IJ. 1997. Changes in immunoreactivity for growth associated protein-43 suggest reorganization of synapses on spinal sympathetic neurons after cord transection. Neuroscience 81:535-551.
66. Weaver LC, Verghese P, Bruce JC, Fehlings MG, Krenz NR, Marsh DR. 2001. Autonomic dysreflexia and primary afferent sprouting after clip-compression injury of the rat spinal cord. J Neurotrauma 18:1107-1119.
67. West MJ, Slomianka L, Gundersen HJ. 1991. Unbiased stereological estimation of the total number of neurons in thesubdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231:482-497.
68. Whisler RL, Chen M, Beiqing L, Carle KW. 1997. Impaired induction of c-fos/c-jun genes and of transcriptional regulatory proteins binding distinct c-fos/c-jun promoter elements in activated human T cells during aging. Cell Immunol 175:41-50.
69. Xu Y, Zheng Z, Ho KP, Qian Z. 2006. Effects of spinal cord injury on c-fos expression in hypothalamic paraventricular nucleus and supraoptic nucleus in rats. Brain Res 1087:175-179.
70. Yaici ED, Rampin O, Calas A, Jestin A, McKenna KE, Leclerc P, Benoit G, Giuliano F. 2002a. Alpha(2a) and alpha(2c) adrenoceptors on spinal neurons controlling penile erection. Neuroscience 114:945-960.
71. Yaici ED, Rampin O, Tang Y, Calas A, Jestin A, Leclerc P, Benoit G, Giuliano F. 2002b. Catecholaminergic projections onto spinal neurons destined to the pelvis including the penis in rat. Int J Impot Res 14:151-166.
72. Ye Y, Machado DG, Kim DO. 2000. Projection of the marginal shell of the anteroventral cochlear nucleus to olivocochlear neurons in the cat. J Comp Neurol 420:127-138.