Descending projections from the nucleus raphe obscurus to pudendal motoneurons in the male rat

Journal of Comparative Neurology

Volumn 397, Issue 4, 1998, Pages 458-474

  Hermann, Gerlinda E ^a   Bresnahan, Jacqueline C ^a   Holmes, Gregory M ^a   Rogers, Richard C ^a   Beattie, Michael S ^a,b  

^a OHIO STATE UNIVERSITY   (United States)

^b THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

Elimination; Pelvic floor reflexes; Sexual reflexes; Somatovisceral integration; Spinal cord

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN STEM; CONTROLLED STUDY; INTERNEURON; MALE; MOTONEURON; NERVE PROJECTION; NONHUMAN; PARASYMPATHETIC NERVE; PELVIS FLOOR; PRIORITY JOURNAL; PUDENDAL NERVE; RAPHE NUCLEUS; RAT; REFLEX; RETICULAR FORMATION; SEXUAL FUNCTION; SPINAL CORD;

ANIMALS; AUTONOMIC FIBERS, PREGANGLIONIC; DEXTRANS; EFFERENT PATHWAYS; FLUORESCENT DYES; INTERNEURONS; LUMBOSACRAL REGION; MALE; MOTOR NEURONS; PELVIS; RAPHE NUCLEI; RATS; RATS, INBRED STRAINS; REFLEX; RHODAMINES; SPINAL CORD; SYNAPTIC TRANSMISSION; THORAX;

EID: 0032504771     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19980810)397:4<458::AID-CNE2>3.0.CO;2-0     Document Type: Article

References (86)

1. Allen, G.V. and D.F. Cechetto (1994) Serotoninergic and nonserotoninergic neurons in the medullary raphe system have axon collateral projections to autonomic and somatic cell groups in the medulla and spinal cord. J. Comp. Neurol. 350:357-366.
2. Amendt, K., J. Czachurski, K. Dembowsky, and H. Seller (1979) Bulbospinal projections to the intermediolateral cell column; A neuroanatomical study. J. Autonom. Nerv. Syst. 1:103-117.
3. Andersson, K.-E. and G. Wagner (1995) Physiology of penile erection. Physiol. Rev. 75:191.
4. Arvidsson, U., S. Cullheim, B. Ulfhake, G.W. Bennett, K.C.F. Fone, C. Cuello, A.A.J. Verhofstad, T.J. Vissar, and T. Hökfelt (1990) 5-Hydroxytryptamine, substance P, and thyrotropin-releasing hormone in the adult cat spinal cord segment L-7: Immunohistochemical and chemical studies. Synapse 6:237-270.
5. Beattie, M.S., Q. Li, M.G. Leedy, and J.C. Bresnahan (1990) Motoneurons innervating the external anal and urethral sphincters of the female cat have different patterns of dendritic arborization. Neurosci. Lett. 111:69-74.
6. Beattie, M.S., G.M. Holmes, G.E. Hermann, R.C. Rogers, and J.C. Bresnahan (1996) Pudendal motoneuron function in intact and CNS injured rats: Alterations following brainstem lesions and spinal transection. Soc. Neurosci. Abstr. 22:722.4.
7. Beleslin, D.B., D. Jovanovic-Micic, R. Samardzic, and B. Terzic (1987) Studies of thyrotropin-releasing hormone (TRH)-induced defecation in cats. Pharmacol. Biochem. Behav. 26:639-641.
8. Bowker, R.M., K.N. Westlund, M.C. Sullivan, J.F. Wilber, and J.D. Coulter (1983) Descending serotonergic, peptidergic and cholinergic pathways from the raphe nuclei: A multiple transmitter complex. Brain Res. 288:33-48.
9. Breedlove, S.M. and A.P. Arnold (1980) Hormone accumulation in a sexually dimorphic motor nucleus of the rat spinal cord. Science 210:564-566.
10. Breedlove, S.M. and A.P. Arnold (1981) Sexually dimorphic motor nucleus in the rat lumbar spinal cord: Response to adult hormone manipulation, absence in androgen-insensitive rats. Brain Res. 225:297-307.
11. Chaouch, A., D. Menétrey, D. Binder, and J.M. Besson (1983) Neurons at the origin of the medial component of the bulbopontine spinoreticular tract in the rat: An anatomical study using horseradish peroxidase transport. J. Comp. Neurol. 214:309-320.
12. Christian, E.P. (1993) A retrograde labeling technique for the functional study of airway specific visceral afferent neurons. J. Neurosci. Methods 47:147-160.
13. Collins, W.F., III, J.T. Erichsen, and R.D. Rose (1991) Pudendal motor and premotor neurons in the male rat: A WGA transneuronal study. J. Comp. Neurol. 308:28-41.
14. Collins, W.F., III, D. Alspaugh, W. Hu, and J.T. Erichsen (1992a) Morphology of external urethral sphincter motoneurons and localization of putative sphincter interneurons in the rat spinal cord. Soc. Neurosci. Abstr. 18:1050.
15. Collins, W.F., III, A.W. Seymour, and S.W. Klugewicz (1992b) Differential effect of castration on the somal size of pudendal motoneurons in the adult male rat. Brain Res. 577:326-330.
16. De Groat, W.C., J.R. Roppolo, N. Yoshimura, and K. Sugaya (1994) Neural control of the urinary bladder and colon. In D.L. Wingate and T.F. Burks (eds): Innervation of the Gut: Pathophysiological Implications. Boca Raton, FL: CRC Press, pp. 167-190.
17. Ding, Y.-Q., M. Takada, H. Tokuno, and N. Mizuno (1995) Direct projections from the dorsolateral pontine tegmentum to pudendal motoneurons innervating the external urethral sphincter muscle in the rat. J. Comp. Neurol. 357:318-330.
18. Dubrovsky, B. and D. Filipini (1990) Neurobiological aspects of the pelvic floor muscles involved in defecation. Neurosci. Biobehav. Rev. 14:157-168.
19. Eskay, R., R. Long, and M. Palkovitz (1983) Localization of immunoreactive TRH in the lower brain stem of the rat. Brain Res. 277:159-162.
20. Faden, A.I., A. Gannon, and A.I. Basbaum (1988) Use of serotonin immunocytochemistry as a marker of injury severity after experimental spinal trauma in rats. Brain Res. 250:94-100.
21. Frenckner, B. (1975) Function of the anal sphincters in spinal man. Gut 16:638-644.
22. Glover, J.C., G. Petursdottir, and J.K.S. Jansen (1986) Fluorescent dextran-amines used as axonal tracers in the nervous system of the chicken embryo. J. Neurosci. Methods 18:255-268.
23. Goldstein, L.A., E.M. Kurz, and D.R. Sengelaub (1990) Androgen regulation of dendritic growth and retraction in the development of a sexually dimorphic spinal nucleus. J. Neurosci. 10:935-946.
24. Gonella, J., M. Bouvier, and F. Blanquet (1987) Extrinsic nervous control of motility of small and large intestines and related sphincters. Physiol. Rev. 67:902-961.
25. Hart, B.L. and P.Y. Melese-D'Hospital (1983) Penile mechanisms and the role of the striated penile muscles in penile reflexes. Physiol. Behav. 31:807-813.
26. Hermann, G.E., G.M. Holmes, R.C. Rogers, M.S. Beattie, and J.C. Bresnahan (1996) Descending projections of the lateral paragigantocellular nucleus (LPGi): Possible anatomical basis of role in lumbosacral reflexes. Soc. Neurosci. Abstr. 22:1835.
27. Hermann, G.E. and R.C. Rogers (1995) Tumor necrosis factor-alpha in the dorsal vagal complex suppresses gastric motility. Neuroimmunomodulation 2:74-81.
28. Hirsch, M.D. and C.J. Helke (1988) Bulbospinal thyrotropin-releasing hormone projections to the intermediolateral cell column: A double fluorescence immunohistochemical-retrograde tracing study in the rat. Neuroscience 25:625-637.
29. Holmes, G.M., J.C. Bresnahan, R.C. Rogers, G.E. Hermann, and M.S. Beattie (1994) Differential characteristics of rat dorsomedial motoneurons. Soc. Neurosci. Abstr. 20:791.
30. Holmes, G.M., R.C. Rogers, J.C. Bresnahan, and M.S. Beattie (1995) Thyrotropin-releasing hormone (TRH) and CNS regulation of anorectal motility in the rat. J. Autonom. Nerv. Syst. 56:8-14.
31. Holmes, G.M., J. Martau, G.E. Hermann, R.C. Rogers, J.C. Bresnahan, and M.S. Beattie (1997) Nucleus raphe obscurus (nRO) regulation of anorectal motility in rats. Brain Res. 759:197-204.
32. Holstege, G. (1987) Some anatomical observations on the projections from the hypothalamus to brainstem and spinal cord: An HRP and autoradiographic tracing study in the cat. J. Comp. Neurol. 260:98-126.
33. Holstege, G. and H.G.J.M. Kuypers (1982) The anatomy of brain stem pathways to the spinal cord in the cat. A labeled amino acid tracing study. Progr. Brain Res. 57:145-175.
34. Holstege, G. and J. Tan (1987) Supraspinal control of motoneurons innervating the striated muscles of the pelvic floor including urethral and anal sphincters in the cat. Brain 110:1323-1344.
35. Holstege, G., R. Bandler, and C.B. Saper (1996) The emotional motor system. Progr. Brain Res. 107:3-6.
36. Horita, A. and M.A. Carino (1982) Centrally administered thyrotropin-releasing hormone (TRH) stimulates colonic transit and diarrhea production by a vagally mediated serotonergic mechanism in the rabbit. J. Pharmacol. Exp. Ther. 222:367-371.
37. Hornby, P.J., C.D. Rossiter, R.L. White, W.P. Norman, D.H. Kuhn, and R.A. Gillis (1990) Medullary raphe: A new site for vagally mediated stimulation of gastric motility in cats. Am. J. Physiol. (Gastrointest. Liver Physiol.) 258:G637-G647.
38. Johnson, H., B. Ulfhake, Å. Dagerlind, G.W. Bennett, K.C.F. Fone, and T. Hökfelt (1993) The serotoninergic bulbospinal system and brainstemspinal cord content of serotonin-, TRH-, and substance P-like immunoreactivity in the aged rat with special reference to the spinal cord motor nucleus. Synapse 15:63-89.
39. Jordan, C.L., S.M. Breedlove, and A.P. Arnold (1982) Sexual dimorphism and the influence of neonatal androgen in the dorsolateral motor nucleus of the rat lumbar spinal cord. Brain Res. 249:309-314.
40. Kondo, Y., K. Yamanouchi, and Y. Sakuma (1996) Effects of the raphe obscurus lesion in the medulla on penile erection and copulatory behavior in the male rat [abstract]. Presented at the Conference on Reproductive Behavior, Concordia University, Montreal, Quebec, Canada.
41. Krowicki, Z.K. and P.J. Hornby (1994) TRH and substance P independently affect gastric motility in nucleus raphe obscurus of the rat. Am. J. Physiol. (Gastrointest. Liver Physiol.) 266:G870-G877.
42. Kurz, E., D. Senegelaub, and A. Arnold (1986) Androgens regulate the dendritic length of mammalian motoneurons in adulthood. Science 232:395-398.
43. LaHann, T.R. and A. Horita (1982) Thyrotropin-releasing hormone: Centrally mediated effects on gastrointestinal motor activity. J. Pharmacol. Exp. Ther. 222:66-70.
44. Leah, J., D. Menétrey, and J. de Pommery (1988) Neuropeptides in long ascending spinal tract cells in the rat: Evidence for parallel processing of ascending information. Neuroscience 24:195-207.
45. Leedy, M.G., M.S. Beattie, and J.C. Bresnahan (1987) Testosterone-induced plasticity of synaptic inputs to adult mammalian motoneurons. Brain Res. 424:386-390.
46. Lenz, H.J. and TA. Silverman (1995) Effects of cerebral TRH on intestinal water transport: Role of vagal, muscarinic, and VIP pathways. Am. J. Physiol. (Gastrointest. Liver Physiol.) 269:G138-G143.
47. Loewy, A.D. (1981) Raphe pallidus and raphe obscurus projections to the intermediolateral cell column in the rat. Brain Res. 222:129-133.
48. Longo, W.E., G.H. Ballantyne, and I.M. Modlin (1989) The colon, anorectum and spinal cord patient: A review of the functional alterations of the denervated gut. Dis. Colon Rectum 32:261-267.
49. Lynn, R.B., M.S. Kreider, and R.R. Miselis (1991) Thyrotropin-releasing hormone-immunoreactive projections to the dorsal motor nucleus and the nucleus of the solitary tract of the rat. J. Comp. Neurol. 311:271-288.
50. MacDonagh, R., W.M. Sun, D.G. Thomas, R. Smallwood, and N.W. Read (1992) Anorectal function in patients with complete supraconal spinal cord lesions. Gut 33:1532-1538.
51. Marson, L. and K.E. McKenna (1990) The identification of a brainstem site controlling spinal sexual reflexes in male rats. Brain Res. 515:303-308.
52. Marson, L. and K.E. McKenna (1992) A role for 5-hydroxytryptamine in descending inhibition of spinal sexual reflexes. Exp. Brain Res. 88:313-320.
53. Martin, G.F., T. Cabana, F.J. Ditirro, R.H. Ho, and A.O. Humbertson, Jr. (1982) Raphespinal projections in the North American opossum: Evidence for connectional heterogeneity. J. Comp. Neurol. 208:67-84.
54. Martin, GF. R. Waltzer, and R.P. Vertes (1985) Major projections of the reticular formation. In G. Paxinos (ed): The Rat Nervous System. Orlando, FL: Academic Press, Inc., pp. 29-42.
55. McCann, M.J., G.E. Hermann, and R.C. Rogers (1989) Nucleus raphe obscurus (nRO) influences vagal control of gastric motility in rats. Brain Res. 486:181-184.
56. McKenna, K.E. and I.R. Nadelhaft (1986) The organization of the pudendal nerve in the male and female rat. J. Comp. Neurol. 248:532-549.
57. Meisel, R.L. and B.D. Sachs (1993) The physiology of male sexual behavior. In E. Knobil and J. Neill (eds): The Physiology of Reproduction. New York: Raven Press, pp. 3-105.
58. Menétrey, D., F. Roudier, and J.M. Besson (1983) Spinal neurons reaching the lateral reticular nucleus as studied in the rat by retrograde transport of horseradish peroxidase. J. Comp. Neurol. 220:439-452.
59. Menétrey, D., J. de Pommery, and J.M. Besson (1984) Electrophysiological characteristics of lumbar spinal cord neurons backfired from lateral reticular nucleus in the rat. J. Neurophysiol. 52:595-611.
60. Miyata, K., T. Kamato, A. Nishida, H. Ito, H. Yuki, M. Yamano, R. Tsutsumi, Y. Katsuyama, and K. Honda (1992) Role of serotonin-3 receptor in stress-induced defecation. J. Pharmacol. Exp. Ther. 261:297-303.
61. Monaghan, E.P. and S.M. Breedlove (1991) Brain sites projecting to the spinal nucleus of the bulbocavernosus. J. Comp. Neurol. 307:370-374.
62. Morrison, S.F. and G.L. Gebber (1985) Axonal branching patterns and funicular trajectories of raphespinal sympathoinhibitory neurons. J. Physiol. (London) 53:759-772.
63. Parkman, H.P., J.C. Reynolds. C.P. Ogorek, and M.S. Kreider (1993) TRH: An inhibitory, regulatory peptide of feline lower esophageal sphincter. Am. J. Physiol. (Gastrointest. Liver Physiol.) 264:G522-G527.
64. Paxinos, G. and C. Watson (1986) The Rat Brain in Stereotaxic Coordinates. New York: Academic Press.
65. Peshori, K.R., J.T. Erichsen, and W.F. Collins, III (1995) Differences in the connectivity of rat pudendal motor nuclei as revealed by retrograde transneuronal transport of wheat germ agglutinin. J. Comp. Neurol. 353:119-128.
66. Reddy, V.K., P. Cassini, R.H. Ho, and G.F. Martin (1990) Origins and terminations of bulbospinal axons that contain serotonin and either enkephalin or substance-P in the North American opossum. J. Comp. Neurol. 294:96-108.
67. Richmond, R., R. Gladdy, J.L. Creasy, S. Kitamura, E. Smits, and D.B. Thomson (1994) Efficacy of seven retrograde tracers compared in multiple-labeling studies of feline motoneurons. J. Neurosci. Methods 53:35-46.
68. Rinaman, L. and R.R. Miselis (1990) Thyrotropin-releasing hormone immunoreactive nerve terminals synapse on the dendrites of gastric vagal motoneurons in the rat. J. Comp. Neurol. 294:235-251.
69. Rogers, R.C. and G. Hermann (1987) Oxytocin, oxytocin antagonist, TRH, and hypothalamic paraventricular nucleus stimulation effects on gastric motility. Peptides 8:505-513.
70. Rogers, R.C., H. Kita, L.L. Butcher, and D. Novin (1980) Afferent projections to the dorsal motor nucleus of the vagus. Brain Res. Bull. 5:365-373.
71. Rose, R.D. and W.F. Collins, III (1985) Crossing dendrites may be a substrate for synchronized activation of penile motoneurons. Brain Res. 337:373-377.
72. Sachs, B.D. (1982) Role of striated penile muscles in penile reflexes, and induction of pregnancy in the rat. J. Reprod. Fertil. 66:433-443.
73. Sasaki, M. (1994) Morphological analysis of external urethral and external anal sphincter motoneurones of cat. J. Comp. Neurol. 349:269-287.
74. Sasek, C.A., M.W. Wessendorf, and C.J. Heike (1990) Evidence for coexistence of thyrotropin-releasing hormone, substance P and serotonin in ventral medullary neurons that project to the intermediolateral cell column in the rat. Neuroscience 35:105-119.
75. Schmued, L., K. Kyriakidis, and L. Heimer (1990) In vivo anterograde and retrograde axonal transport of the fluorescent rhodamine-dextranamine, Fluoro-Ruby, within the CNS. Brain Res. 526:127-134.
76. Schroder, H.D. (1985) Anatomical and pathoanatomical studies on the spinal efferent systems innervating pelvic structures. J. Autonom. Nerv. Syst. 14:23-48.
77. Shapiro, S., M. Kubek, E. Siemers, E. Daly, J. Callahan, and T. Putty (1995) Quantification of thyrotropin-releasing hormone changes and serotonin content changes following graded spinal cord injury. J. Surg. Res. 59:393-398.
78. Shen, P., A.P. Arnold, and P.E. Micevych (1990) Supraspinal projections to the ventromedial lumbar spinal cord in adult male rats. J. Comp. Neurol. 300:263-272.
79. Skagerberg, G. and A. Björklund (1985) Topographic principles in the spinal projections of serotonergic and non-serotonergic brainstem neurons in the rat. Neuroscience 15:445-480.
80. Smith, J.R., T.R. LaHann, R.M. Chesnut, M.A. Carino, and A. Horita (1977) Thyrotropin-releasing hormone: Stimulation of colonic activity following intracerebroventricular administration. Science 196:660-662.
81. Tache, Y., H. Yang, and M. Yoneda (1993) Vagal regulation of gastric function involves TRH in the medullary raphe nuclei and dorsal vagal complex. Digestion 54:65-72.
82. Tache, Y., H. Yang, and H. Kaneko (1995) Caudal raphe-dorsal vagal complex peptidergic projections: Role in gastric vagal control. Peptides 16:431-435.
83. Tork, I. (1985) Raphe nuclei and serotonin containing systems. In G. Paxinos (ed): The Rat Nervous System. Orlando, FL: Academic Press, pp. 43-78.
84. Watkins, L.R., G. Griffin, G.R. Leichnetz, and D.J. Mayer (1980) The somatotopic organization of the nucleus raphe magnus and surrounding brainstem structures as revealed by HRP slow-release gels. Brain Res. 181:1-15.
85. Wessendorf, M.W. (1991) Fluoro-Gold: Composition and mechanism of uptake. Brain Res. 553:135-148.
86. Yamanouchi, K. and M. Kakeyama (1992) Effect of medullary raphe lesions on sexual behavior in male rats with or without treatments of p chlorophenylalanine. Physiol. Behav. 51:575-579.