Identified motoneurons involved in sexual and eliminative functions in the rat are powerfully excited by vasopressin and tachykinins

Journal of Neuroscience

Volumn 26, Issue 42, 2006, Pages 10717-10726

  Ogier, Roch ^a   Tribollet, Eliane ^a   Suarez, Philippe ^a   Raggenbass, Mario ^a  

^a UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

Author keywords

Cationic conductance; Choline acetyltransferase; Oxytocin; Patch clamp; Pudendal motoneurons; Spinal cord

Indexed keywords

1,1' DILINOLEYL 3,3,3',3' TETRAMETHYLINDOCARBOCYANINE; 4 CHLOROBENZENESULFONATE; CARBOCYANINE; CHOLINE ACETYLTRANSFERASE; NEUROKININ 1 RECEPTOR; OXYTOCIN RECEPTOR; SULFONIC ACID DERIVATIVE; TACHYKININ; TETRODOTOXIN; UNCLASSIFIED DRUG; VASOPRESSIN; VASOPRESSIN DERIVATIVE; VASOPRESSIN RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING SITE; BLADDER FUNCTION; CONTROLLED STUDY; DEPOLARIZATION; DRUG MECHANISM; IMMUNOHISTOCHEMISTRY; MALE; MOTONEURON; NERVE CELL STIMULATION; NONHUMAN; PATCH CLAMP; PELVIS FLOOR; PRIORITY JOURNAL; PUDENDAL NERVE; RAT; SEXUAL BEHAVIOR; SKELETAL MUSCLE; SPINAL CORD; ANIMAL; ANIMAL BEHAVIOR; COMPARATIVE STUDY; DRUG EFFECT; DRUG POTENTIATION; NEWBORN; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; ANIMALS, NEWBORN; ELIMINATIVE BEHAVIOR, ANIMAL; MALE; MOTOR NEURONS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, VASOPRESSIN; SEXUAL BEHAVIOR, ANIMAL; TACHYKININS; VASOPRESSINS;

EID: 33750947015     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3364-06.2006     Document Type: Article

References (62)

1. Aghajanian GK, Rasmussen K (1989) Intracellular studies in the facial nucleus illustrating a simple new method for obtaining viable motoneurons in adult rat brain slices. Synapse 3:331-338.
2. Alberi S, Dubois-Dauphin M, Dreifuss JJ, Raggenbass M (1993) Modulation by divalent cations of the current generated by vasopressin in facial motoneurons. Brain Res 624:326-330.
3. 125I]Bolton Hunter-eledoisin binding sites in rat spinal cord by quantitative autoradiography. Neuroscience 46:225-232.
4. Breedlove SM, Arnold AP (1980) Hormone accumulation in a sexually dimorphic motor nucleus of the rat spinal cord. Science 210:564-566.
5. Breedlove SM, Arnold AP (1983) Hormonal control of a developing neuromuscular system. I. Complete demasculinization of the male rat spinal nucleus of the bulbocavernosus using the anti-androgen flutamide. J Neurosci 3:417-423.
6. Charlton CG, Helke CJ (1985) Autoradiographic localization and characterization of spinal cord substance P binding sites: high densities in sensory, autonomic, phrenic, and Onuf's motor nuclei. J Neurosci 5:1653-1661.
7. Derick S, Cheng LL, Voirol MJ, Stoev S, Giacomini M, Wo NC, Szeto HH, Ben Mimoun M, Andres M, Gaillard RC, Guillon G, Manning M (2002) [1-deamino-4-cyclohexylalanine] arginine vasopressin: a potent and specific agonist for vasopressin V1b receptors. Endocrinology 143:4655-4664.
8. Fedirchuk B, Shefchyk SJ (1993) Membrane potential changes in sphincter motoneurons during micturition in the decerebrate cat. J Neurosci 13:3090-3094.
9. Fedirchuk B, Downie JW, Shefchyk SJ (1994) Reduction of perineal evoked excitatory postsynaptic potentials in cat lumbar and sacral motoneurons during micturition. J Neurosci 14:6153-6159.
10. Fisher ND, Nistri A (1993) Substance P and TRH share a common effector pathway in rat spinal motoneurones: an in vitro electrophysiological investigation. Neurosci Lett 153:115-119.
11. Fisher ND, Baranauskas G, Nistri A (1994) Multiple types of tachykinin receptor mediate a slow excitation of rat spinal motoneurones in vitro. Neurosci Lett 165:84-88.
12. Grzonka Z, Lammek B, Kasprzykowski F, Gazis D, Schwartz IL (1983) Synthesis and some pharmacological properties of oxytocin and vasopressin analogues with sarcosine or N-methyl-L-alanine in position 7. J Med Chem 26:555-559.
13. Gueritaud JP, Seyfritz N (1992) An organotypic co-culture of embryonic rat brainstem and tongue or skeletal muscle. Eur J Neurosci 4:616-627.
14. Hallbeck M, Blomqvist A (1999) Spinal cord-projecting vasopressinergic neurons in the rat paraventricular hypothalamus. J Comp Neurol 411:201-211.
15. Hanson Jr MG, Shen S, Wiemelt AP, McMorris FA, Barres BA (1998) Cyclic AMP elevation is sufficient to promote the survival of spinal motor neurons in vitro. J Neurosci 18:7361-7371.
16. Holstege G, Tan J (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.
17. Hultborn H, Kiehn O (1992) Neuromodulation of vertebrate motor neuron membrane properties. Curr Opin Neurobiol 2:770-775.
18. Jordan CL, Breedlove SM, Arnold AP (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.
19. Jordan CL, Letinsky MS, Arnold AP (1989) The role of gonadal hormones in neuromuscular synapse elimination in rats. II. Multiple innervation persists in the adult levator ani muscle after juvenile androgen treatment. J Neurosci 9:239-247.
20. Jordan CL, Padgett B, Hershey J, Prins G, Arnold A (1997) Ontogeny of androgen receptor immunoreactivity in lumbar motoneurons and in the sexually dimorphic levator ani muscle of male rats. J Comp Neurol 379:88-98.
21. Kihira T, Yoshida S, Yoshimasu F, Wakayama I, Yase Y (1997) Involvement of Onuf's nucleus in amyotrophic lateral sclerosis. J Neurol Sci 147:81-88.
22. Kolaj M, Renaud LP (1998) Vasopressin-induced currents in rat neonatal spinal lateral horn neurons are G-protein mediated and involve two conductances. J Neurophysiol 80:1900-1910.
23. Koliatsos VE, Price DL, Clatterbuck RE (1994) Motor neurons in Onuf's nucleus and its rat homologues express the p75 nerve growth factor receptor: sexual dimorphism and regulation by axotomy. J Comp Neurol 345:510-527.
24. Konishi S, Otsuka M (1974) Excitatory action of hypothalamic substance P on spinal motoneurones of newborn rats. Nature 252:734-735.
25. Leong SK, Ling EA (1990) Labelling neurons with fluorescent dyes administered via intravenous, subcutaneous or intraperitoneal route. J Neurosci Methods 32:15-23.
26. Liu X, Tribollet E, Ogier R, Barberis C, Raggenbass M (2003) Presence of functional vasopressin receptors in spinal ventral horn neurons of young rats: a morphological and electrophysiological study. Eur J Neurosci 17:1833-1846.
27. Lowbridge J, Manning M, Haldar J, Sawyer WH (1977) Synthesis and some pharmacological properties of [4-threonine, 7- glycine]oxytocin, [1-(L-2-hydroxy-3-mercaptopropanoic acid), 4- threonine, 7-glycine]oxytocin (hydroxy[Thr4, Gly7]oxytocin), and [7-glycine]oxytocin, peptides with high oxytocic-antidiuretic selectivity. J Med Chem 20:120-123.
28. Manabe T, Araki I, Takahashi T, Kuno M (1991) Membrane currents recorded from sexually dimorphic motoneurones of the bulbocavernosus muscle in neonatal rats. J Physiol (Lond) 440:419-435.
29. Mannen T (2000) Neuropathological findings of Onuf's nucleus and its significance. Neuropathology [Suppl] 20:S30-S33.
30. Manning M, Bankowski K, Barberis C, Jard S, Elands J, Chan WY (1992) Novel approach to the design of synthetic radioiodinated linear V1A receptor antagonists of vasopressin. Int J Pept Protein Res 40:261-267.
31. McKenna KE, Nadelhaft I (1986) The organization of the pudendal nerve in the male and female rat. J Comp Neurol 248:532-549.
32. Monaghan EP, Arjomand J, Breedlove SM (1993) Brain lesions affect penile reflexes. Horm Behav 27:122-131.
33. Nacimiento W, Topper R, Fischer A, Mobius E, Oestreicher AB, Gispen WH, Nacimiento AC, Noth J, Kreutzberg GW (1993) B-50 (GAP-43) in Onuf's nucleus of the adult cat. Brain Res 613:80-87.
34. Nordeen EJ, Nordeen KW, Sengelaub DR, Arnold AP (1985) Androgens prevent normally occurring cell death in a sexually dimorphic spinal nucleus. Science 229:671-673.
35. Otsuka M, Yanagisawa M (1980) The effects of substance P and baclofen on motoneurones of isolated spinal cord of the newborn rat. J Exp Biol 89:201-214.
36. Oz M, Kolaj M, Renaud LP (2001) Electrophysiological evidence for vasopressin V(1) receptors on neonatal motoneurons, premotor and other ventral horn neurons. J Neurophysiol 86:1202-1210.
37. Palouzier-Paulignan B, Dubois-Dauphin M, Tribollet E, Dreifuss JJ, Raggenbass M (1994) Action of vasopressin on hypoglossal motoneurones of the rat: presynaptic and postsynaptic effects. Brain Res 650:117-126.
38. Peshori KR, Erichsen JT, Collins III WF (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.
39. Pierson P, Tribollet E, Raggenbass M (2001) Effect of vasopressin on the input-output properties of rat facial motoneurons. Eur J Neurosci 14:957-967.
40. Ptak K, Konrad M, Di Pasquale E, Tell F, Hilaire G, Monteau R (2000) Cellular and synaptic effect of substance P on neonatal phrenic motoneurons. Eur J Neurosci 12:126-138.
41. Pullen AH, Tucker D, Martin JE (1997) Morphological and morphometric characterisation of Onuf's nucleus in the spinal cord in man. J Anat 191:201-213.
42. Quirion R, Dam TV (1986) Ontogeny of substance P receptor binding sites in rat brain. J Neurosci 6:2187-2199.
43. Raggenbass M, Goumaz M, Sermasi E, Tribollet E, Dreifuss JJ (1991) Vasopressin generates a persistent voltage-dependent sodium current in a mammalian motoneuron. J Neurosci 11:1609-1616.
44. Regoli D, Drapeau G, Dion S, Couture R (1988) New selective agonists for neurokinin receptors: pharmacological tools for receptor characterization. Trends Pharmacol Sci 9:290-295.
45. Regoli D, Boudon A, Fauchere JL (1994) Receptors and antagonists for substance P and related peptides. Pharmacol Rev 46:551-599.
46. Rekling JC, Funk GD, Bayliss DA, Dong XW, Feldman JL (2000) Synaptic control of motoneuronal excitability. Physiol Rev 80:767-852.
47. Reymond-Marron I, Raggenbass M, Zaninetti M (2005) Vasopressin facilitates glycinergic and GABAergic synaptic transmission in developing hypoglossal motoneurons. Eur J Neurosci 21:1601-1609.
48. Roppolo JR, Nadelhaft I, de Groat WC (1985) The organization of pudendal motoneurons and primary afferent projections in the spinal cord of the rhesus monkey revealed by horseradish peroxidase. J Comp Neurol 234:475-488.
49. Sachs BD (1982) Role of striated penile muscles in penile reflexes, copulation, and induction of pregnancy in the rat. J Reprod Fertil 66:433-443.
50. Sasaki M (1991) Membrane properties of external urethral and external anal sphincter motoneurones in the cat. J Physiol (Lond) 440:345-366.
51. Sawyer WH, Grzonka Z, Manning M (1981) Neurohypophysial peptides. Design of tissue-specific agonists and antagonists. Mol Cell Endocrinol 22:117-134.
52. Schroder HD (1980) Organization of the motoneurons innervating the pelvic muscles of the male rat. J Comp Neurol 192:567-587.
53. + channel, is modulated by multiple neurotransmitters in motoneurons. Neuron 25:399-410.
54. Tashiro T, Satoda T, Matsushima R, Mizuno N (1989a) Convergence of serotonin-, enkephalin- and substance P-like immunoreactive afferent fibers on single pudendal motoneurons in Onuf's nucleus of the cat: a light microscope study combining the triple immunocytochemical staining technique with the retrograde HRP-tracing method. Brain Res 481:392-398.
55. Tashiro T, Satoda T, Matsushima R, Mizuno N (1989b) Possible origins of substance P-like immunoreactive axons within Onuf's nucleus of the cat. Brain Res 497:177-182.
56. Tribollet E, Goumaz M, Raggenbass M, Dubois-Dauphin M, Dreifuss JJ (1991) Early appearance and transient expression of vasopressin receptors in the brain of rat fetus and infant. An autoradiographical and electrophysiological study. Brain Res Dev Brain Res 58:13-24.
57. Tribollet E, Arsenijevic Y, Marguerat A, Barberis C, Dreifuss JJ (1994) Axotomy induces the expression of vasopressin receptors in cranial and spinal motor nuclei in the adult rat. Proc Natl Acad Sci USA 91:9636-9640.
58. Tribollet E, Barberis C, Arsenijevic Y (1997) Distribution of vasopressin and oxytocin receptors in the rat spinal cord: sex-related differences and effect of castration in pudendal motor nuclei. Neuroscience 78:499-509.
59. Ueyama T, Mizuno N, Nomura S, Konishi A, Itoh K, Arakawa H (1984) Central distribution of afferent and efferent components of the pudendal nerve in cat. J Comp Neurol 222:38-46.
60. Wagner CK, Clemens LG (1991) Projections of the paraventricular nucleus of the hypothalamus to the sexually dimorphic lumbosacral region of the spinal cord. Brain Res 539:254-262.
61. Wagner CK, Clemens LG (1993) Neurophysin-containing pathway from the paraventricular nucleus of the hypothalamus to a sexually dimorphic motor nucleus in lumbar spinal cord. J Comp Neurol 336:106-116.
62. Yasuda K, Robinson DM, Selvaratnam SR, Walsh CW, McMorland AJ, Funk GD (2001) Modulation of hypoglossal motoneuron excitability by NK1 receptor activation in neonatal mice in vitro. J Physiol (Lond) 534:447-464.