Plasticity in the injured spinal cord: Can we use it to advantage to reestablish effective bladder voiding and continence?

Progress in Brain Research

Volumn 152, Issue , 2006, Pages 147-162

  Zinck, Natasha D T ^a   Downie, John W ^a  

^a DALHOUSIE UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

4 (1 AMINOETHYL) N (4 PYRIDYL)CYCLOHEXANECARBOXAMIDE; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; CAPSAICIN; CELL ADHESION MOLECULE; MUSCARINIC RECEPTOR BLOCKING AGENT; NERVE CELL ADHESION MOLECULE; NERVE GROWTH FACTOR; NEUROTROPHIC FACTOR; NEUROTROPHIN; PROTEIN NOGO; PROTEIN P75; PROTEIN TYROSINE KINASE A; RHO KINASE; SODIUM CHANNEL;

AREFLEXIA; AUTONOMIC DYSREFLEXIA; BLADDER CONTRACTION; BLADDER DYSFUNCTION; BLADDER EMPTYING; BLADDER FUNCTION; BLADDER INNERVATION; BLADDER SPHINCTER; BRAIN STEM; CELL DIFFERENTIATION; CELL FUNCTION; CELL SURVIVAL; CONFERENCE PAPER; CONTINENCE; EFFERENT NERVE; HUMAN; LUMBOSACRAL SPINE; MICTURITION; MICTURITION REFLEX; MYELINATED NERVE; NERVE CELL PLASTICITY; NERVE FIBER C; NERVE FIBER GROWTH; NERVE REGENERATION; NEUROPATHIC PAIN; NONHUMAN; PATHOPHYSIOLOGY; PHENOTYPE; PREGANGLIONIC NERVE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SENSORY NERVE; SENSORY NERVE CELL; SPINAL CORD; SPINAL CORD INJURY; SPINAL CORD NERVE CELL; STEM CELL TRANSPLANTATION; SYNAPSE; UPREGULATION;

EID: 25844448719     PISSN: 00796123     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0079-6123(05)52010-7     Document Type: Conference Paper

References (104)

1. S.C. Apfel, D.E. Wright, A.M. Wiideman, C. Dormia, W.D. Snider, and J.A. Kessler Nerve growth factor regulates the expression of brain-derived neurotrophic factor mRNA in the peripheral nervous system Mol. Cell. Neurosci. 7 1996 134 142
2. J. Aubert, J. Ridet, M. Schachner, G. Rougon, and F. Gage Expression of L1 and PSA during sprouting and regeneration in adult hippocampal formation J. Comp. Neurol. 399 1998 1 19
3. F. Barrington The nervous mechanism of micturition Quart. J. Exp. Physiol. 8 1915 33 71
4. I.A. Belyantseva, and G.R. Lewin Stability and plasticity of primary afferent projections following nerve regeneration and central degeneration Eur. J. Neurosci. 11 1999 457 468
5. A.L. Bishop, and A. Hall Rho GTPases and their effector proteins Biochem. J. 348 Part 2 2000 241 255
6. Boggs, J.W., Wenzel, B.J., Gustafson, K.J., and Grill, W.M. (2004) A spinal micturition reflex mediated by afferents in the deep perineal nerve. J. Neurophysiol., in press.
7. L. Bonfanti, A. Merighi, and D.T. Theodosis Dorsal rhizotomy induces transient expression of the highly sialylated isoform of the neural cell adhesion molecule in neurons and astrocytes of the adult rat spinal cord Neuroscience 74 1996 619 623
8. J.F. Borisoff, C.C. Chan, G.W. Hiebert, L. Oschipok, G.S. Robertson, R. Zamboni, J.D. Steeves, and W. Tetzlaff Suppression of Rho-kinase activity promotes axonal growth on inhibitory CNS substrates Mol. Cell. Neurosci. 22 2003 405 416
9. P. Bovolenta, and I. Fernaud-Espinosa Nervous system proteoglycans as modulators of neurite outgrowth Prog. Neurobiol. 61 2000 113 132
10. W.R. Bowles, M. Sabino, C. Harding-Rose, and K.M. Hargreaves Nerve growth factor treatment enhances release of immunoreactive calcitonin gene-related peptide but not substance P from spinal dorsal horn slices in rats Neurosci. Lett. 363 2004 239 242
11. J.L. Bruses, N. Chauvet, M.E. Rubio, and U. Rutishauser Polysialic acid and the formation of oculomotor synapses on chick ciliary neurons J. Comp. Neurol. 446 2002 244 256
12. O. Bukalo, N. Fentrop, A.Y. Lee, B. Salmen, J.W. Law, C.T. Wotjak, M. Schweizer, A. Dityatev, and M. Schachner Conditional ablation of the neural cell adhesion molecule reduces precision of spatial learning, long-term potentiation, and depression in the CA1 subfield of mouse hippocampus J. Neurosci. 24 2004 1565 1577
13. D. Cai, J. Qiu, Z. Cao, M. McAtee, B.S. Bregman, and M.T. Filbin Neuronal cyclic AMP controls the developmental loss in ability of axons to regenerate J. Neurosci. 21 2001 4731 4739
14. D. Cai, Y. Shen, M. De Bellard, S. Tang, and M.T. Filbin Prior exposure to neurotrophins blocks inhibition of axonal regeneration by MAG and myelin via a cAMP-dependent mechanism Neuron 22 1999 89 101
15. C.L. Cheng, and W.C. de Groat The role of capsaicin-sensitive afferent fibers in the lower urinary tract dysfunction induced by chronic spinal cord injury in rats Exp. Neurol. 187 2004 445 454
16. H. Cheng, K.K. Liao, S.F. Liao, T.Y. Chuang, and Y.H. Shih Spinal cord repair with acidic fibroblast growth factor as a treatment for a patient with chronic paraplegia Spine 29 2004 E284 E288
17. M.D. Christensen, and C.E. Hulsebosch Spinal cord injury and anti-NGF treatment results in changes in CGRP density and distribution in the dorsal horn in the rat Exp. Neurol. 147 1997 463 475
18. E.M. Coonan, J.W. Downie, and H.-J. Du Sacral spinal cord neurons responsive to bladder pelvic and perineal inputs in cats Neurosci. Lett. 260 1999 137 140
19. H. Cremer, R. Lange, A. Christoph, M. Plomann, G. Vopper, J. Roes, R. Brown, S. Baldwin, P. Kraemer, and S. Scheff Inactivation of the N-CAM gene in mice results in size reduction of the olfactory bulb and deficits in spatial learning Nature 367 1994 455 459
20. C. Crowley, S.D. Spencer, M.C. Nishimura, K.S. Chen, S. Pitts-Meek, M.P. Armanini, L.H. Ling, S.B. MacMahon, D.L. Shelton, and A.D. Levinson Mice lacking nerve growth factor display perinatal loss of sensory and sympathetic neurons yet develop basal forebrain cholinergic neurons Cell 76 1994 1001 1011
21. M.M. Daston, M. Bastmeyer, U. Rutishauser, and D.D. O'Leary Spatially restricted increase in polysialic acid enhances corticospinal axon branching related to target recognition and innervation J. Neurosci. 16 1996 5488 5497
22. W. de Groat Plasticity of bladder reflex pathways during postnatal development Physiol. Behav. 77 2002 689 692
23. W. de Groat, M. Kawatani, T. Hisamitsu, C. Cheng, C. Ma, K. Thor, W. Steers, and J. Roppolo Mechanisms underlying the recovery of urinary bladder function following spinal cord injury J. Auton. Nerv. Sys. 30 1990 S71 S78
24. W.C. de Groat, I. Araki, M.A. Vizzard, M. Yoshiyama, N. Yoshimura, K. Sugaya, C. Tai, and J.R. Roppolo Developmental and injury induced plasticity in the micturition reflex pathway Behav. Brain Res. 92 1998 127 140
25. B.J. Dickson, and K.A. Senti Axon guidance: growth cones make an unexpected turn Curr. Biol. 12 2002 R218 R220
26. Y.-Q. Ding, B.-Z. Qin, J.-S. Li, and N. Mizuno Induction of c-fos-like protein in the spinoparabrachial tract-neurons locating within the sacral parasympathetic nucleus in the rat Brain Res. 659 1994 283 286
27. U. Drescher, A. Faissner, R. Klein, F.G. Rathjen, and C. Sturmer Axonal growth and pathfinding: from phenomena to molecules Cell. Tissue Res. 290 1997 187 188
28. C. Franz, U. Rutishauser, and V. Rafuse Polysialyated neural cell adhesion molecule (PSA-NCAM) is necessary for selective targeting of regenerating motor neurons J. Neurosci. 25 2005 2081 2091
29. G. Gallo, and P.C. Letourneau Regulation of growth cone actin filaments by guidance cues J. Neurobiol. 58 2004 92 102
30. W.F. Goins, N. Yoshimura, M.W. Phelan, T. Yokoyama, M.O. Fraser, H. Ozawa, N.J. Bennett, W.C. de Groat, J.C. Glorioso, and M.B. Chancellor Herpes simplex virus mediated nerve growth factor expression in bladder and afferent neurons: potential treatment for diabetic bladder dysfunction J. Urol. 165 2001 1748 1754
31. P.R. Gordon-Weeks Microtubules and growth cone function J. Neurobiol. 58 2004 70 83
32. E.M. Grados-Munro, and A.E. Fournier Myelin-associated inhibitors of axon regeneration J. Neurosci. Res. 74 2003 479 485
33. T. GrandPre, S. Li, and S.M. Strittmatter Nogo-66 receptor antagonist peptide promotes axonal regeneration Nature 417 2002 547 551
34. R. Grasso, Y.P. Ivanenko, M. Zago, M. Molinari, G. Scivoletto, V. Castellano, V. Macellari, and F. Lacquaniti Distributed plasticity of locomotor pattern generators in spinal cord injured patients Brain 127 2004 1019 1034
35. W. Grill, B. Wang, S. Hadziefendie, and M. Haxhiu Identification of the spinal neural network involved in coordination of micturition in the male cat Brain Res. 796 1998 150 160
36. C.N. Honda Visceral and somatic afferent convergence onto neurons near the central canal in the sacral spinal cord of the cat J. Neurophysiol. 53 1985 1059 1078
37. Z. Hoyk, A. Parducz, and D.T. Theodosis The highly sialylated isoform of the neural cell adhesion molecule is required for estradiol-induced morphological synaptic plasticity in the adult arcuate nucleus Eur. J. Neurosci. 13 2001 649 656
38. D.W. Huang, L. McKerracher, P.E. Braun, and S. David A therapeutic vaccine approach to stimulate axon regeneration in the adult mammalian spinal cord Neuron 24 1999 639 647
39. W. Janig, and J.F. Morrison Functional properties of spinal visceral afferents supplying abdominal and pelvic organs, with special emphasis on visceral nociception Prog. Brain Res. 67 1986 87 114
40. H. Kakizaki, and W.C. de Groat Reorganization of somato-urethral reflexes following spinal cord injury in the rat J. Urol. 158 1997 1562 1567
41. D. Kiryushko, V. Berezin, and E. Bock Regulators of neurite outgrowth: role of cell adhesion molecules Ann. NY Acad. Sci. 1014 2004 140 154
42. J.Z. Kiss, and D. Muller Contribution of the neural cell adhesion molecule to neuronal and synaptic plasticity Rev. Neurosci. 12 2001 297 310
43. N.R. Krenz, S.O. Meakin, A.V. Krassioukov, and L.C. Weaver Neutralizing intraspinal nerve growth factor blocks autonomic dysreflexia caused by spinal cord injury J. Neurosci. 19 1999 7405 7414
44. N.R. Krenz, and L.C. Weaver Nerve growth factor in glia and inflammatory cells of the injured rat spinal cord J. Neurochem. 74 2000 730 739
45. M.N. Kruse, A.L. Belton, and W.C. de Groat Changes in bladder and externalurethral sphincter function after spinal cord injury in the rat Am. J. Physiol. 264 1993 R1157 R1163
46. M.N. Kruse, L.A. Bray, and W.C. de Groat Influence of spinal cord injury on the morphology of bladder afferent and efferent neurons J. Auton. Nerv. Syst. 54 1995 215 224
47. K. Lamb, G.F. Gebhart, and K. Bielefeldt Increased nerve growth factor expression triggers bladder overactivity J. Pain. 5 2004 150 156
48. L. Li, and X.F. Zhou Pericellular Griffonia simplicifolia I isolectin B4-binding ring structures in the dorsal root ganglia following peripheral nerve injury in rats J. Comp. Neurol. 439 2001 259 274
49. X.G. Luo, R.A. Rush, and X.F. Zhou Ultrastructural localization of brain-derived neurotrophic factor in rat primary sensory neurons Neurosci. Res. 39 2001 377 384
50. C.A. Maggi, P. Santicioli, and A. Meli Postnatal development of micturition reflex in rats Am. J. Physiol. 250 1986 R926 R931
51. D.L. Maier, S. Mani, S.L. Donovan, D. Soppet, L. Tessarollo, J.S. McCasland, and K.F. Meiri Disrupted cortical map and absence of cortical barrels in growth-associated protein (GAP)-43 knockout mice Proc. Natl. Acad. Sci. USA 96 1999 9397 9402
52. L. Marson Identification of central nervous system neurons that innervate the bladder body, bladder base, or external urethral sphincter of female rats: a transneuronal tracing study using pseudorabies virus J. Comp. Neurol. 389 1997 584 602
53. J.W. McDonald, X.Z. Liu, Y. Qu, S. Liu, S.K. Mickey, D. Turetsky, D.I. Gottlieb, and D.W. Choi Transplanted embryonic stem cells survive, differentiate and promote recovery in injured rat spinal cord Nat. Med. 5 1999 1410 1412
54. S. McMahon, and J. Morrison Two groups of spinal interneurons that respond to stimulation of the viscera of the cat J. Physiol. 322 1982 21 34
55. S.B. McMahon, and J.F.B. Morrison Spinal neurones with long projections activated from the abdominal viscera of the cat J. Physiol. 322 1982 1 20
56. R.J. Milne, R.D. Foreman, and W.D. Willis Responses of primate spinothalamic neurons located in the sacral intermediomedial gray (Stilling's nucleus) to proprioceptive input from the tail Brain Res. 234 1982 227 236
57. T. Mitsui, H. Kakizaki, H. Tanaka, T. Shibata, I. Matsuoka, and T. Koyanagi Immortalized neural stem cells transplanted into the injured spinal cord promote recovery of voiding function in the rat J. Urol. 170 2003 1421 1425
58. P.P. Monnier, S.G. Beck, J. Bolz, and S. Henke-Fahle The polysialic acid moiety of the neural cell adhesion molecule is involved in intraretinal guidance of retinal ganglion cell axons Dev. Biol. 229 2001 1 14
59. C. Morgan, I. Nadelhaft, and W.C. de Groat The distribution of visceral primary afferents from the pelvic nerve to Lissauer's tract and the spinal gray matter and its relationship to the sacral parasympathetic nucleus J. Comp. Neurol. 201 1981 415 440
60. D. Muller, Z. Djebbara-Hannas, P. Jourdain, L. Vutskits, P. Durbec, G. Rougon, and J.Z. Kiss Brain-derived neurotrophic factor restores long-term potentiation in polysialic acid-neural cell adhesion molecule-deficient hippocampus Proc. Natl. Acad. Sci. USA 97 2000 4315 4320
61. I. Nadelhaft, and A.M. Booth The location and morphology of preganglionic neurons and the distribution of visceral afferents from the rat pelvic nerve: a horseradish peroxidase study J. Comp. Neurol. 226 1984 238 245
62. I. Nadelhaft, and P.L. Vera Neurons in the rat brain and spinal cord labeled after pseudorabies virus injected into the external urethral sphincter J. Comp. Neurol. 375 1996 502 517
63. I. Nadelhaft, P.L. Vera, J.P. Card, and R.R. Miselis Central nervous system neurons labelled following the injection of pseudorabies virus into the rat urinary bladder Neurosci. Lett. 143 1992 271 274
64. S. Neumann, F. Bradke, M. Tessier-Lavigne, and A.I. Basbaum Regeneration of sensory axons within the injured spinal cord induced by intraganglionic cAMP elevation Neuron 34 2002 885 893
65. J. Nishiguchi, K. Sasaki, S. Seki, M.B. Chancellor, K.A. Erickson, W.C. de Groat, H. Kumon, and N. Yoshimura Effects of isolectin B4-conjugated saporin, a targeting cytotoxin, on bladder overactivity induced by bladder irritation Eur. J. Neurosci. 20 2004 474 482
66. K. Obata, H. Yamanaka, Y. Dai, T. Tachibana, T. Fukuoka, A. Tokunaga, H. Yoshikawa, and K. Noguchi Differential activation of extracellular signal-regulated protein kinase in primary afferent neurons regulates brain-derived neurotrophic factor expression after peripheral inflammation and nerve injury J. Neurosci. 23 2003 4117 4126
67. J. Pannek, H.J. Sommerfeld, U. Botel, and T. Senge Combined intravesical and oral oxybutynin chloride in adult patients with spinal cord injury Urology 55 2000 358 362
68. G. Paratcha, F. Ledda, and C.F. Ibanez The neural cell adhesion molecule NCAM is an alternative signaling receptor for GDNF family ligands Cell 113 2003 867 879
69. J.I. Pascual, G. Gudino-Cabrera, R. Insausti, and M. Nieto-Sampedro Spinal implants of olfactory ensheathing cells promote axon regeneration and bladder activity after bilateral lumbosacral dorsal rhizotomy in the adult rat J. Urol. 167 2002 1522 1526
70. L. Qiao, and M.A. Vizzard Up-regulation of tyrosine kinase (Trka, Trkb) receptor expression and phosphorylation in lumbosacral dorsal root ganglia after chronic spinal cord (T8-T10) injury J. Comp. Neurol. 449 2002 217 230
71. M. Renganathan, T.R. Cummins, and S.G. Waxman Contribution of Na(v)1.8 sodium channels to action potential electrogenesis in DRG neurons J. Neurophysiol. 86 2001 629 640
72. M. Renganathan, M. Gelderblom, J.A. Black, and S.G. Waxman Expression of Nav1.8 sodium channels perturbs the firing patterns of cerebellar Purkinje cells Brain Res. 959 2003 235 242
73. J.M. Reynard, J. Vass, M.E. Sullivan, and M. Mamas Sphincterotomy and the treatment of detrusor-sphincter dyssynergia: current status, future prospects Spinal Cord 41 2003 1 11
74. K. Sakamoto, B. Uvelius, T. Khan, and M.S. Damaser Preliminary study of a genetically engineered spinal cord implant on urinary bladder after experimental spinal cord injury in rats J. Rehabil. Res. Dev. 39 2002 347 357
75. S. Schumacher, S. Bross, J.R. Scheepe, P. Alken, and K.P. Junemann Sacral anterior root stimulation and posterior rhizotomy in spastic neuropathic bladder Restor. Neurol. Neurosci. 14 1999 195 199
76. A. Sculptoreanu, N. Yoshimura, and W. de Groat KW-7158 [(2S)-(+)-3,3,3-trifluoro-2-hydroxy-2-methyl-N-(5,5,10-trioxo-4, 10-dihydrothieno[3,2-c][1]benzothiepin-9-yl)propanamide] enhances A-type K+ currents in neurons of the dorsal root ganglion of the adult rat J. Pharmacol. Exp. Ther. 310 2004 159 168
77. S. Seki, K. Sasaki, M.O. Fraser, Y. Igawa, O. Nishizawa, M.B. Chancellor, W.C. de Groat, and N. Yoshimura Immunoneutralization of nerve growth factor in lumbosacral spinal cord reduces bladder hyperreflexia in spinal cord injured rats J. Urol. 168 2002 2269 2274
78. S. Seki, K. Sasaki, Y. Igawa, O. Nishizawa, M.B. Chancellor, W.C. De Groat, and N. Yoshimura Suppression of detrusor-sphincter dyssynergia by immunoneutralization of nerve growth factor in lumbosacral spinal cord in spinal cord injured rats J. Urol. 171 2004 478 482
79. S. Shefchyk, and R. Buss Urethral pudendal afferent-evoked bladder and sphincter reflexes in decerabrate and acute spinal cats Neurosci. Lett. 244 1998 137 140
80. S.J. Shefchyk Sacral spinal interneurones and the control of urinary bladder and urethral striated sphincter muscle function J. Physiol. 533 2001 57 63
81. S.J. Shefchyk, and R.R. Buss Urethral pudendal afferent-evoked bladder and sphincter reflexes in decerebrate and acute spinal cats Neurosci. Lett. 244 1998 137 140
82. C.L. Stucky, and G.R. Lewin Isolectin B(4)-positive and -negative nociceptors are functionally distinct J. Neurosci. 19 1999 6497 6505
83. J. Tang, and L. Landmesser Reduction of intramuscular nerve branching and synaptogenesis is correlated with decreased motoneuron survival J. Neurosci. 13 1993 3095 3103
84. J.W. Tarpley, M.G. Kohler, and W.J. Martin The behavioral and neuroanatomical effects of IB(4)-saporin treatment in rat models of nociceptive and neuropathic pain Brain Res. 1029 2004 65 76
85. M. Theodosiou, R.A. Rush, X.F. Zhou, D. Hu, J.S. Walker, and D.J. Tracey Hyperalgesia due to nerve damage: role of nerve growth factor Pain 81 1999 245 255
86. K.B. Thor, D.P. Blais, and W.C. de Groat Behavioral analysis of the postnatal development of micturition in kittens Brain Res. Dev. Brain Res. 46 1989 137 144
87. P.L. Vera, and I. Nadelhaft Anatomical evidence for two spinal 'afferent-interneuron-efferent' reflex pathways involved in micturition in the rat: a 'pelvic nerve' reflex pathway and a 'sacrolumbar intersegmental' reflex pathway Brain Res. 883 2000 107 118
88. M.A. Vizzard Changes in urinary bladder neurotrophic factor mRNA and NGF protein following urinary bladder dysfunction Exp. Neurol. 161 2000 273 284
89. M.A. Vizzard, and M.M. Boyle Increased expression of growth-associated protein (GAP-43) in lower urinary tract pathways following cyclophosphamide (CYP)-induced cystitis Brain Res. 844 1999 174 187
90. L. Vulchanova, T.H. Olson, L.S. Stone, M.S. Riedl, R. Elde, and C.N. Honda Cytotoxic targeting of isolectin IB4-binding sensory neurons Neuroscience 108 2001 143 155
91. L. Vutskits, Z. Djebbara-Hannas, H. Zhang, J.P. Paccaud, P. Durbec, G. Rougon, D. Muller, and J.Z. Kiss PSA-NCAM modulates BDNF-dependent survival and differentiation of cortical neurons Eur. J. Neurosci, 13 2001 1391 1402
92. H.F. Wang, P. Shortland, M.J. Park, and G. Grant Retrograde and transganglionic transport of horseradish peroxidase-conjugated cholera toxin B subunit, wheatgerm agglutinin and isolectin B4 from Griffonia simplicifolia I in primary afferent neurons innervating the rat urinary bladder Neuroscience 87 1998 275 288
93. K.C. Wang, J.A. Kim, R. Sivasankaran, R. Segal, and Z. He P75 interacts with the Nogo receptor as a co-receptor for Nogo, MAG and OMgp Nature 420 2002 74 78
94. S.G. Waxman, T.R. Cummins, S. Dib-Hajj, J. Fjell, and J.A. Black Sodium channels, excitability of primary sensory neurons, and the molecular basis of pain Muscle Nerve 22 1999 1177 1187
95. K.J. Weld, and R.R. Dmochowski Association of level of injury and bladder behavior in patients with post-traumatic spinal cord injury Urology 55 2000 490 494
96. T. Yamashita, and M. Tohyama The p75 receptor acts as a displacement factor that releases Rho from Rho-GDI Nat. Neurosci. 6 2003 461 467
97. N. Yoshimura, and W.C. de Groat Plasticity of Na+ channels in afferent neurones innervating rat urinary bladder following spinal cord injury J. Physiol. 503 Part 2 1997 269 276
98. N. Yoshimura, S.L. Erdman, M.W. Snider, and W.C. de Groat Effects of spinal cord injury on neurofilament immunoreactivity and capsaicin sensitivity in rat dorsal root ganglion neurons innervating the urinary bladder Neuroscience 83 1998 633 643
99. N. Yoshimura, M.E. Franks, K. Sasaki, W.F. Goins, J. Goss, T. Yokoyama, M.O. Fraser, S. Seki, J. Fink, J. Glorioso, W.C. de Groat, and M.B. Chancellor Gene therapy of bladder pain with herpes simplex virus (HSV) vectors expressing preproenkephalin (PPE) Urology 57 2001 116
100. N. Yoshimura, S. Seki, K.A. Erickson, V.L. Erickson, M.B. Chancellor, and W.C. de Groat Histological and electrical properties of rat dorsal root ganglion neurons innervating the lower urinary tract J. Neurosci. 23 2003 4355 4361
101. M. Yoshiyama, F.M. Nezu, O. Yokoyama, W.C. de Groat, and M.B. Chancellor Changes in micturition after spinal cord injury in conscious rats Urology 54 1999 929 933
102. X. Yu, L. Xu, X.D. Zhang, and F.Z. Cui Effect of spinal cord injury on urinary bladder spinal neural pathway: a retrograde transneuronal tracing study with pseudorabies virus Urology 62 2003 755 759
103. F.Q. Zhou, J. Zhong, and W.D. Snider Extracellular crosstalk: when GDNF meets N-CAM Cell 113 2003 814 815
104. K. Zvarova, E. Murray, and M.A. Vizzard Changes in galanin immunoreactivity in rat lumbosacral spinal cord and dorsal root ganglia after spinal cord injury J. Comp. Neurol. 475 2004 590 603