Bladder afferent pathway and spinal cord injury: Possible mechanisms inducing hyperreflexia of the urinary bladder

Progress in Neurobiology

Volumn 57, Issue 6, 1999, Pages 583-606

  Yoshimura, Naoki ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; AUTONOMIC HYPERREFLEXIA; AUTONOMIC NERVOUS SYSTEM; BLADDER EPITHELIUM; BLADDER FUNCTION; BLADDER INNERVATION; BLADDER SPHINCTER; ELECTROPHYSIOLOGY; HYPERREFLEXIA; MEMBRANE TRANSPORT; MICTURITION REFLEX; MOTOR COORDINATION; NEUROFILAMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REVIEW; SPINAL CORD INJURY;

AFFERENT PATHWAYS; ANIMALS; HUMANS; LUMBOSACRAL REGION; PHENOTYPE; REFLEX, ABNORMAL; SPINAL CORD INJURIES; URINARY BLADDER; URINATION;

EID: 0032977420     PISSN: 03010082     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0301-0082(98)00070-7     Document Type: Review

References (119)

1. Aguayo L. G., White G. Effects of nerve growth factor on TTX- and capsaicin-sensitivity in adult rat sensory neurons. Brain Res. 570:1992;61-67.
2. Akins P. T., McCleskey E. W. Characterization of potassium currents in adult rat sensory neurons and modulation by opioids and cyclic AMP. Neuroscience. 56:1993;759-769.
3. Akopian A. N., Sivilotti L., Wood J. N. A tetrodotoxin-resistant voltage-gated sodium channel expressed by sensory neurons. Nature. 379:1996;257-262.
4. Andersson K.-E. Pharmacology of lower urinary tract smooth muscles and penile erectile tissues. Pharmacol. Rev. 45:1993;253-308.
5. Araki I. Inhibitory postsynaptic currents and the effects of GABA on visually identified sacral parasympathetic preganglionic neurons in neonatal rats. J. Neurophysiol. 72:1995;2903-2910.
6. Araki I., de Groat W. C. Unitary excitatory synaptic currents in preganglionic neurons mediated by two distinct groups of interneurons in neonatal rat sacral parasympathetic nucleus. J. Neurophysiol. 76:1996;215-226.
7. Arbuckle J. B., Docherty R. J. Expression of tetrodotoxin-resistant sodium channels in capsaicin-sensitive dorsal root ganglion neurons of adult rats. Neurosci. Lett. 185:1995;70-73.
8. Bennett B. C., Roppolo J. R., Kruse M. N., de Groat W. C. Neural control of urethral smooth and striated muscle activity in vivo: role of nitric oxide. J. Urol. 153:1995;2004-2009.
9. Bennett D. L. H., Dmietrieva N., Priestley J. V., Clary D., McMahon S. B. trkA, CGRP and IB4 expression in retrogradely labelled cutaneous and visceral primary sensory neurones in the rat. Neurosci. Lett. 206:1996;33-36.
10. Bevan S., Winter J. Nerve growth factor (NGF) differentially regulates the chemosensitivity of adult rat cultured sensory neurons. J. Neurosci. 15:1995;4918-4926.
11. + channel III and SNS gene expression in spinal sensory neurons. NeuroReport. 8:1997;2331-2335.
12. Blok B. F., Holstege G. Direct projections from the periaqueductal gray to the pontine micturition center (M-region). An antegrade and retrograde tracing study in the cat. Neurosci. Lett. 166:1994;93-96.
13. Blok B. F., De Weerd H., Holstege G. Ultrastructural evidence for a paucity of projections from lumbosacral cord to the pontine micturition center or M-region in the cat: a new concept for the organization of the micturition reflex with the periaqueductal gray as central relay. J. Comp. Neurol. 359:1995;300-309.
14. Bors, E. and Comarr, A. E. (1971) Neurological Urology, Physiology of Micturition, its Neurological Disorders and Sequelae. University Park Press, Baltimore.
15. Buttyan R., Jacob B. Z., Blaivas J. G., Levin R. M. Early molecular response to rabbit bladder outlet obstruction. Neurourol. Urodyn. 11:1992;225-238.
16. 4 receptors couple positively to tetrodotoxin-insensitive sodium channels in a subpopulation of capsaicin-sensitive rat sensory neurons. J. Neurosci. 17:1997;7181-7189.
17. Chai T. C., Steers W. C. Neurophysiology of micturition and continence. Urol. Clin. North. Am. 23:1996;221-236.
18. Chancellor, M. B. and Blaivas, J. G. (1996) Spinal cord injury. In: Practical Neuro-Urology: Genitourinary Complications of Neurologic Disease, pp. 99-118. Eds. M. B. Chancellor and J. G. Blaivas. Butterworth-Heinemann, Newton.
19. Cheng C.-L., Ma C.-P., de Groat W. C. The effects of capsaicin on micturition and associated reflexes in the rat. Am. J. Physiol. 265:1993;R132-R648.
20. Cheng C.-L., Ma C.-P., de Groat W. C. Effect of capsaicin on micturition and associated reflexes in chronic spinal rats. Brain Res. 678:1995;40-48.
21. Cruz F., Guimaraes M., Silva C., Rio M. E., Coimbra A., Reis M. Desensitization of bladder sensory fibers by intravesical capsaicin has long lasting clinical and urodynamic effects in patients with hyperactive or hypersensitive bladder dysfunction. J. Urol. 157:1997;585-589.
22. Cruz F., Guimaraes M., Silva C., Reis M. Suppression of bladder hyperreflexia by intravesical resiniferatoxin. Lancet. 350:1997;640-641.
23. 2 receptor-mediated facilitation of pudendal nerve reflexes in the anesthetized cats. Br. J. Pharmacol. 118:1996;150-154.
24. Dmitrieva N., McMahon S. B. Sensitization of visceral afferents by nerve growth factor in the adult rat. Pain. 66:1996;87-97.
25. Eglen R. M., Hegde S. S., Watson N. Muscarinic receptors subtypes and smooth muscle action. Pharmcol. Rev. 48:1996;531-565.
26. Elliott A. A., Elliott J. R. Characterization of TTX-sensitive and TTX-resistant sodium currents in small cells from adult rat dorsal root ganglia. J. Physiol. 463:1993;39-56.
27. Espey M. J., Dawnie J. W. Serotonergic modulation of cat bladder function before and after spinal transection. Eur. J. Pharmacol. 287:1995;173-177.
28. Fall M., Lindström S., Mazieres L. A bladder-to-bladder cooling reflex in the cat. J. Physiol. 427:1990;281-300.
29. Fam, B. A., Sarkarati, M. and Yalla, S. V. (1988) Spinal cord injury. In: Neurourology and Urodynamics, pp. 291-302. Eds S. V. Yalla, E. J. McGuire, A. Elbadawi and J. G. Blaivas. Macmillan Publishing Company, New York.
30. Fedirchuk B., Shefchyk S. J. Membrane potential changes in sphincter motoneurons during micturition in the decerebrate cat. J. Neurosci. 13:1993;3090-3094.
31. Geirsson G., Fall M., Lindström S. The ice-water test - a simple and valuable supplement to routine cystometry. Br. J. Urol. 71:1993;681-685.
32. Geirsson G., Lindström S., Fall M., Hermansson G. G., Hjalmas K. Positive bladder cooling test in neurologically normal young children. J. Urol. 151:1994;446-448.
33. Geirsson G., Fall M., Sullivan L. Clinical and urodynamic effects of intravesical capsaicin treatment in patients with chronic traumatic spinal detrusor hyperreflexia. J. Urol. 154:1995;1825-1829.
34. + currents in adult rat sensory neurons. J. Neurophysiol. 75:1996;2629-2646.
35. Gold M. S., Dastmalchi S., Levine J. D. Co-expression of nociceptor properties in dorsal root ganglion neurons from the adult rat in vitro. Neuroscience. 71:1996;265-275.
36. Goodness T. P., Albers K. M., Davis F. E., Davis B. M. Overexpression of nerve growth factor in skin increases sensory neuron size and modulates Trk receptor expression. Eur. J. Neurosci. 9:1997;1574-1585.
37. de Groat W. C. Spinal cord projections and neuropeptides in visceral afferent neurons. Prog. Brain. Res. 67:1986;165-187.
38. de Groat W. C. Mechanisms underlying the recovery of lower urinary tract function following spinal cord injury. Paraplegia. 33:1995;493-505.
39. de Groat, W. C. and Booth A. M. (1993) Synaptic transmission in pelvic ganglia. In: The Autonomic Nervous System, Vol. 3, Nervous Control of the Urogenital System, pp. 291-347. Ed C. A. Maggi. Harwood Academic Publishers, London.
40. de Groat W. C., Lalley P. M. Reflex firing in the lumbar sympathetic outflow to activation of vesical afferent fibers. J. Physiol. 226:1972;289-309.
41. de Groat W. C., Theobald R. J. Reflex activation of sympathetic pathways to vesical smooth muscle and parasympathetic ganglia by electrical stimulation of vesical afferents. J. Physiol. 259:1976;223-237.
42. de Groat W. C., Nadelhaft I., Milne R. J., Booth A. M., Morgan C., Thor K. Organization of the sacral parasympathetic reflex pathways to the urinary bladder and large intestine. J. Auton. Nerv. Syst. 3:1981;135-160.
43. de Groat W. C., Kawatani M., Hisamitsu T., Cheng C.-L., Ma C.-P., Thor K., Steers W. D., Roppolo J. R. Mechanisms underlying the recovery of urinary bladder function following spinal cord injury. J. Auton. Nerv. Syst. 30:1990;S71-78.
44. de Groat, W. C., Booth, A. M. and Yoshimura, N. (1993) Neurophysiology of micturition and its modification in animal models of human disease. In: The Autonomic Nervous System, Vol. 3, Nervous Control of the Urogenital System, pp. 227-290. Ed C. A. Maggi. Harwood Academic Publishers, London.
45. de Groat, W. C., Kruse, M. N., Vizzard, M. A., Cheng, C.-L., Araki, I. and Yoshimura, N. (1997) Modification of urinary bladder function after spinal cord injury. In: Advances in Neurology, Vol. 72, Neuronal Regeneration, Reorganization, and Repair, pp. 347-364. Ed. F. L. Seil. Lippincott-Raven Publishers, Philadelphia.
46. Häbler H. J., Jänig W., Koltzenburg M. Activation of unmyelinated afferent fibres by mechanical stimuli and inflammation of the urinary bladder in the cat. J. Physiol. 425:1990;545-562.
47. Hoffman P. N., Griffin J. W., Price D. L. Control of axonal caliber by neurofilament transport. J. Cell. Biol. 99:1984;705-714.
48. Hoffman P. N., Cleveland D. W., Griffin J. W., Landes P. W., Cowan N. J., Price D. L. Neurofilament gene expression: a major determinant of axonal caliber. Proc. Natl Acad. Sci. USA. 84:1987;3472-3476.
49. Holstege G., Griffiths D., de Wall H., Dalm E. Anatomical and physiological observations on supraspinal control of bladder and urethral sphincter muscles in cat. J. Comp. Neurol. 250:1986;449-461.
50. Hoyle, C. H. V. and Burnstock, G. P. (1993) Postganglionic efferent transmission in the bladder and urethra. In: The Autonomic Nervous System, Vol. 3, Nervous Control of the Urogenital System, pp. 349-382. Ed. C. A. Maggi. Harwood Academic Publishers, London.
51. Hulsebosch C. E., Coggeshall R. E. An analysis of the axon populations in the nerves to the viscera in the rat. J. Comp. Neurol. 211:1982;1-10.
52. Igawa Y., Mattiasson A., Andersson K.-E. Effects of GABA-receptor stimulation and blockade on micturition in normal rats and rats with bladder outlet obstruction. J. Urol. 150:1993;537-542.
53. Igawa Y., Mattiasson A., Andersson K.-E. Functional importance of cholinergic and purinergic neurotransmission for micturition contraction in the normal, un-anesthetized rat. Br. J. Pharmacol. 109:1993;473-479.
54. Igawa Y., Komiyama I., Nishizawa S., Ogawa A. Intravesical capsaicin inhibits autonomic dysreflexia in patients with spinal cord injury. Neurourol. Urodyn. 15:1996;374-376.
55. 2 adrenoceptors in micturition in normal conscious rats. J. Urol. 156:1996;1853-1857.
56. 1-adrenoceptors. Br. J. Pharmacol. 117:1996;962-966.
57. Jänig W., McLachlan E. M. Organization of lumber spinal outflow to distal colon and pelvic organs. Physiol. Rev. 67:1987;1332-1440.
58. Jänig W., Morrison J. F. B. Functional properties of spinal visceral afferents supplying abdominal and pelvic organs, with special emphasis on visceral nociception. Prog. Brain. Res. 67:1986;87-114.
59. Keast J. R., de Groat W. C. Segmental distribution and peptide content of primary afferent neurons innervating the urogenital organs and colon of male rats. J. Comp. Neurol. 319:1992;615-623.
60. Kohama T. Neuroanatomical studies on the urine storage facilitatory areas in the cat brain. Part I: input neuronal structures to the nucleus subcoeruleus and the nucleus reticularis pontis oralis. Jpn. J. Urol. 83:1992;1469-1477.
61. Kondo S., Morita T., Tashima Y. Muscarinic cholinergic receptor subtypes in human detrusor muscle studies by labelled and non-labelled pirenzepine, AF-DX116 and 4DAMP. Urol. Int. 54:1995;150-153.
62. Kornblum H. I., Johnson E. M. Time and dose dependencies of effects of nerve growth factor on sympathetic and sensory neurons in neonatal rats. Brain Res. 234:1982;41-51.
63. Kruse M. N., Noto H., Roppolo J. R., de Groat W. C. Pontine control of the urinary bladder and external urethral sphincter in the rat. Brain Res. 532:1990;182-190.
64. Kruse M. N., Belton A. L., de Groat W. C. Changes in bladder and external urethral sphincter function following spinal cord injury in the rat. Am. J. Physiol. 264:1993;R1157-1163.
65. Kruse M. N., Bray L. A., de Groat W. C. Influence of spinal cord injury on the morphology of bladder afferent and efferent neurons. J. Auton. Nerv. Syst. 54:1995;215-224.
66. Lawson S. N., Perry M. J., Prabhaker E., McCarthy P. W. Primary afferent neurones: neurofilament, neuropeptides, and conduction velocity. Brain Res. Bull. 30:1993;239-243.
67. Luheshi G. N., Zar A. Presence of non-cholinergic motor transmission in human isolated bladder. J. Pharm. Pharmacol. 42:1990;223-224.
68. Lundberg J. M. Pharmacology of cotransmission in the autonomic nervous system: integrative aspects on amines neuropeptides, adenosine triphosphate, amine acids and nitric oxide. Pharmacol. Rev. 48:1996;113-178.
69. Maggi C. A. The role of peptides in the regulation of the micturition reflex: an update. J. Gen. Pharmacol. 22:1991;1-24.
70. Maggi, C. A. (1993) The dual, sensory and efferent function of the capsaicin-sensitive primary sensory nerves in the bladder and urethra. In: The Autonomic Nervous System, Vol. 3, Nervous Control of Urogenital System, pp. 383-422. Ed. C. A. Maggi. Harwood Academic Publishers, London.
71. Mallory B., Steers W. D., de Groat W. C. Electrophysiological study of micturition reflexes in rats. Am. J. Physiol. 257:1989;R410-421.
72. Mallory B. S., Roppolo J. R., de Groat W. C. Pharmacological modulation of the pontine micturition center. Brain Res. 546:1991;310-320.
73. Matsumoto G., Hisamitsu T., de Groat W. C. Role of glutamate and NMDA receptors in the descending limb of the spinobulbospinal micturition reflex pathway of the rat. Neurosci. Lett. 183:1995;58-61.
74. Matsumoto G., Hisamitsu T., de Groat W. C. Non-NMDA glutamatergic excitatory transmission in the descending limb of the spinobulbospinal micturition reflex pathway in the rat. Brain Res. 693:1995;246-250.
75. McFarlane S., Cooper E. Kinetics and voltage dependence of A-type currents on neonatal rat sensory neurons. J. Neurophysiol. 66:1991;1380-1391.
76. Nishizawa O., Sugaya K., Noto H., Harada T., Tsuchida S. Pontine micturition center in the dog. J. Urol. 140:1988;872-874.
77. Noto H., Roppolo J. R., Steers W. D., de Groat W. C. Excitatory and inhibitory influences on bladder activity elicited by electrical stimulation in the pontine micturition center in rat. Brain Res. 492:1989;99-115.
78. Noto H., Roppolo J. R., de Groat W. C., Nishizawa O., Sugaya K., Tsuchida S. Opioid modulation of the micturition reflex at the level of the pontine micturition center. Urol. Int. 47:1991;19-22.
79. Noto H., Roppolo J. R., Steers W. D., de Groat W. C. Electrophysiological analysis of ascending and descending components of the micturition reflex pathway in the rat. Brain Res. 549:1991;95-105.
80. Novakovic S. D., Tzoumaka E., McGivern J. G., Haraguchi M., Sangameswaran L., Gogas K. R., Eglen R. M., Hunter J. C. Distribution of the tetrodotoxin-resistant sodium channel PN3 in rat sensory neurons in normal and neuropathic conditions. J. Neurosci. 18:1998;2174-2187.
81. + channels in rat dorsal root ganglia. J. Physiol. 466:1993;9-37.
82. A-receptor-mediated conductance and sodium currents in cutaneous afferent neurons. J. Neurophysiol. 78:1997;31-42.
83. Persson K., Alm P., Johansson K., Larsson B., Andersson K.-E. Nitric oxide synthase in pig lower urinary tract: immunohistochemistry, NADPH diaphorase histochemistry, and functional effects. Br. J. Pharmacol. 110:1993;521-530.
84. Roy M. L., Narahashi T. Differential properties of tetrodotoxin-sensitive and tetrodotoxin-resistant sodium channels in rat dorsal root ganglion neurons. J. Neurosci. 12:1992;2104-2111.
85. Sangameswaran L., Delgado S. G., Fish L. M., Koch B. D., Jakeman L. B., Stewart G. R., Sze P., Hunter J. C., Eglen R. M., Herman R. C. Structure and function of a novel voltage-gated, tetrodotoxin-resistant sodium channel specific to sensory neurons. J. Biol. Chem. 271:1996;5953-5956.
86. Sengupta J. N., Gebhart G. F. Mechanosensitive properties of pelvic nerve afferent fibres innervating the urinary bladder of the rat. J. Neurophysiol. 72:1994;2420-2430.
87. Shimoda N., Takakusaki K., Nishizawa O., Tsuchida S., Mori S. The changes in the activity of pudendal motoneurons in relation to reflex micturition evoked in decerebrated cats. Neurosci. Lett. 135:1992;175-178.
88. Somogyi G. T., de Groat W. C. Evidence for inhibitory nicotinic and facilitatory muscarinic receptors in cholinergic nerve terminals of the rat urinary bladder. J. Auton. Nerv. Syst. 37:1992;89-97.
89. Somogyi G. T., Tanowitz M., de Groat W. C. M-1 muscarinic receptor mediated facilitation of acetylcholine release in the rat urinary bladder but not in the heart. J. Physiol. 80:1994;81-89.
90. Steers W. D., Ciambotti J., Etzel B., Erdman S., de Groat W. C. Alterations in afferent pathways from the urinary bladder of the rat in response to partial urethral obstruction. J. Comp. Neurol. 310:1991;401-410.
91. Steers W. D., Kolbeck S., Creedon D., Tuttle J. B. Nerve growth factor in the urinary bladder of the adult regulates neuronal form and function. J. Clin. Invest. 88:1991;1709-1715.
92. Steers W. D., Meythaler J. M., Haworth C., Herrell D., Park T. S. Effects of acute bolus and chronic continuous intrathecal baclofen on genitourinary dysfunction due to spinal cord pathology. J. Urol. 148:1992;1849-1855.
93. Steers W. D., Albo M., van Asselt E. Effects of serotonergic agonists on micturition and sexual function in the rat. J. Drug. Dev. Res. 27:1992;361-375.
94. Steers W. D., Creedon D. J., Tuttle J. B. Immunity to nerve growth factor prevents afferent plasticity following urinary bladder hypertrophy. J. Urol. 155:1996;379-385.
95. Sugaya K., de Groat W. C. Effects of MK-801 and CNQX, glutamate receptor antagonists on bladder activity in neonatal rats. Brain Res. 640:1994;1-10.
96. Sugaya K., Matsuyama K., Takakusaki K., Mori S. Electrical and chemical stimulations of the pontine micturition center. Neurosci. Lett. 80:1987;197-201.
97. Takeda M., Lepor H. Nitric oxide synthase in the dog urethra: a histochemical and pharmacological analysis. Br. J. Pharmacol. 116:1995;2517-2523.
98. Thor K. B., Hisamitsu T., de Groat W. C. Unmasking of a neonatal somatovesical reflex in adult cats by the serotonin autoreceptor agonist 5-methoxy-N,N dimethyltryptamine. Dev. Brain. Res. 54:1990;35-42.
99. Thornbury K. D., Hollywood M. A., McHale N. G. Mediation by nitric oxide of neurogenic relaxation of the urinary bladder neck muscle in sheep. J. Physiol. 451:1992;133-144.
100. Tran L. V., Somogyi G. T., de Groat W. C. Inhibitory effects of neuropeptide Y on cholinergic and adrenergic transmission in the rat urinary bladder and urethra. Am. J. Physiol. 266:1994;R1411-1417.
101. Vera P. L., Nadelhaft I. Conduction velocity distribution of afferent fibers innervating the rat urinary bladder. Brain Res. 520:1990;83-89.
102. Verge V. M. K., Tetzlaff W., Bisby M. A., Richardson P. M. Influence of nerve growth factor on neurofilament gene expression in mature primary sensory neurons. J. Neurosci. 10:1990;2018-2025.
103. Waddell P. J., Lawson S. N. Electrophysiological properties of subpopulations of rat dorsal root ganglion neurons in vitro. Neuroscience. 36:1990;811-822.
104. Wang P., Luthin G. R., Ruggieri M. R. Muscarinic acetylcholine receptor subtypes mediating urinary bladder contractility and coupling to GTP proteins. J. Pharmacol. Exp. Ther. 273:1995;959-966.
105. Winter J., Forbes C. A., Sternberg J., Linsay R. M. Nerve growth factor (NGF) regulates adult rat cultured dorsal root ganglion neuron responses to the excitotoxin capsaicin. Neuron. 1:1988;973-981.
106. Yamaguchi O., Shishido K., Tamura K., Ogawa T., Fujimura T., Otsuka A. Evaluation of mRNAs encoding muscarinic receptor subtypes in human detrusor muscle. J. Urol. 156:1996;1208-1213.
107. + channels in afferent neurons innervating rat urinary bladder following spinal cord injury. J. Physiol. 503:1997;269-276.
108. Yoshimura N., de Groat W. C. Neural control of the lower urinary tract. Int. J. Urol. 4:1997;111-125.
109. Yoshimura N., Sasa M., Yoshida O., Takaori S. Mediation of micturition reflex by central norepinephrine from the locus coeruleus in the cat. J. Urol. 143:1990;840-843.
110. 1-Adrenergic receptor-mediated excitation from the locus coeruleus of the sacral parasympathetic preganglionic neuron. Life Sci. 47:1990;789-797.
111. Yoshimura N., Mizuta E., Kuno S., Sasa M., Yoshida O. The dopamine D1 receptor agonist SKF 38393 suppresses detrusor hyperreflexia in the monkey with parkinsonism induced by 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP). Neuropharmacology. 32:1993;315-321.
112. Yoshimura N., White G., Weight F. F., de Groat W. C. Patch-clamp recordings from subpopulations of autonomic and afferent neurons identified by axonal tracing techniques. J. Auton. Nerv. Syst. 49:1994;86-92.
113. + currents in rat dorsal root ganglion neurons innervating the urinary bladder. J. Physiol. 494:1996;1-16.
114. Yoshimura N., Erdman S. L., Snider M. W., de Groat W. C. 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.
115. 2 receptor agonists on detrusor hyperreflexia in 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-lesioned parkinsonian cynomolgus monkeys. J. Pharmacol. Exp. Ther. 286, 228-233.
116. Yoshiyama M., Roppolo J. R., de Groat W. C. The effects of MK801 on the micturition reflex in the rat: possible sites of action. J. Pharmacol. Exp. Ther. 265:1993;844-850.
117. Yoshiyama M., Roppolo J. R., de Groat W. C. Interactions between NMDA and AMPA/kainate receptors in the control of micturition in the rat. Eur. J. Pharmacol. 287:1995;73-78.
118. Yoshiyama M., Roppolo J. R., de Groat W. C. Effects of LY215490, a competitive α-amino-3-hydroxy-5-methylisoxazole-4-propionic acid (AMPA) receptor antagonist, on the micturition reflex in the rat. J. Pharmacol. Exp. Ther. 280:1997;894-904.
119. Zhong H. J., Nurse C. Basic fibroblast growth factor regulates ionic currents and excitability of fetal rat carotid body chemoreceptors. Neurosci. Lett. 202:1995;41-44.