Skip to main content

Vasopressin’s Depolarizing Action on Neonatal Rat Spinal Lateral Horn Neurons May Involve Multiple Conductances

  • Chapter
Vasopressin and Oxytocin

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 449))

Abstract

Vasopressin-immunoreactive fibers have been visualized in the area of spinal lateral horn cells, including spinal sympathetic preganglionic neurons (SPNs). The presence and nature of vasopressin receptors on 125 neurons in this area were addressed using whole-cell patch-clamp techniques in transverse spinal cord slice preparations from neonatal rat (11–21 days). Local pressure applications of Arg8-vasopressin (AVP, 1µM) induced a slow-onset membrane depolarization accompanied by spike discharges and membrane oscillations. In voltage-clamp, applications of AVP (10nM-1µM) induced a reversible, tetrodotoxin-resistant and dose-dependent inward current in 90% of tested cells. This effect was blocked by a V1 receptor antagonist [D- (CH2)5 Tyr (Me)-AVP], whereas a V2 receptor agonist [desamino-(D-Arg8)-vasopressin] was ineffective. Both the amplitude and duration of the AVP effect were significantly modified after intracellular dialysis of non-hydrolysable G-protein modulators. I-V relationships, examined in 75 cells, suggested two conductances. In 36 cells the net AVP current reversed ~-102mV, was associated with a decrease in membrane conductance and yielded linear I-V plots, suggesting mediation through closure of a resting potassium conductance. In a further 26 cells the I-V lines remained almost parallel in the voltage range used in this study (-130 to -40mV), while the membrane conductance was decreased in a majority of these cells. In the remaining 13 cells the net AVP current was estimated to reverse ~-30mV and was associated with a small increase in membrane conductance, suggesting mediation through opening of a non-selective cationic conductance. These data indicate that the majority of SPNs and other lateral horn cells possess functional G-protein-coupled V1-type vasopressin receptors in the neonatal spinal cord. In the adult spinal cord, some of these receptors are likely to participate in CNS regulation of autonomic nervous system function.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

eBook
USD 16.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 54.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. duVigneaud V, Gish DT, Katsoyannis PG 1954 A synthetic preparation possessing biological properties associated with arginine-vasopressin. J Am Chem Soc 76:4751–4752

    Article  CAS  Google Scholar 

  2. Acher R 1993 Neurohypophysial peptide systems: processing machinery, hydroosmotic regulation, adaptation and evolution. Reg Peptides 45:1–13

    Article  CAS  Google Scholar 

  3. Buijs RM 1987 Vasopressin localization and putative functions in the brain. In: Gash DM, Boer GJ (eds)Vasopressin: Principles and Properties. New York: Plenum Press

    Google Scholar 

  4. Ma RC, Dun NJ 1985 Vasopressin depolarizes lateral horn cells of the neonatal rat spinal cord in vitro. Brain Res 348:36–43

    Article  PubMed  CAS  Google Scholar 

  5. 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

    Article  PubMed  CAS  Google Scholar 

  6. Raggenbass M, Dubois-Dauphin M, Tribollet E, Dreifuss JJ 1988 Direct excitatory action of vasopressin in the lateral septum of the rat brain. Brain Res 459:60–69

    Article  PubMed  CAS  Google Scholar 

  7. 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

    PubMed  CAS  Google Scholar 

  8. Lowes VL, Sun K, Li Z, Ferguson AV 1995 Vasopressin actions on area postrema neurons in vitro. Am J Physiol 269:R463–R468

    PubMed  CAS  Google Scholar 

  9. Mo Z, Katafuchi T, Muratami H, Hori T 1992 Effects of vasopressin and angiotensin II on neurones in the rat dorsal motor nucleus of the vagus, in vitro. J Physiol (Lond) 458:561–577

    PubMed  CAS  Google Scholar 

  10. Sun M, Guyenet PG 1989 Effects of vasopressin and other neuropeptides on rostral medullary sympathoexcitatory neurons ‘in vitro’. Brain Res 492:261–270

    Article  PubMed  CAS  Google Scholar 

  11. Muhlethaler M, Dreifuss JJ, Gahwiler BH 1982 Vasopressin excites hippocampal neurones. Nature 296:749–751

    Article  PubMed  CAS  Google Scholar 

  12. Lolait SJ, O’Carroll AM, McBride OW, Konig M, Morel A, Brownstein MJ 1992 Cloning and characterization of a vasopressin V2 receptor and possible link to nephrogenic diabetes insipidus. Nature 357:336–339

    Article  PubMed  CAS  Google Scholar 

  13. Morel A, O’Carroll AM, Brownstein MJ, Lolait SJ 1992 Molecular cloning and expression of a rat V1 a arginine vasopressin receptor. Nature 356:523–526

    Article  PubMed  CAS  Google Scholar 

  14. Lolait SJ, O’Carroll AM, Brownstein MJ 1995 Molecular biology of vasopressin receptors. Ann N Y Acad Sci 771:273–292

    Article  PubMed  CAS  Google Scholar 

  15. Barberis C, Tribollet E 1996 Vasopressin and oxytocin receptors in the central nervous system. Crit Rev Neurobiol 10:119–154

    Article  PubMed  CAS  Google Scholar 

  16. Jard S, Roy C, Burth T, Rajerison R, Bockaert J 1975 Antidiuretic hormone-sensitive kidney adenylate cyclase. Adv Cyclic Nucleotide Res 5:31–52

    PubMed  CAS  Google Scholar 

  17. Handler JS, Orloff J 1981 Antidiuretic hormone. Ann Rev Physiol 43:611–624

    Article  CAS  Google Scholar 

  18. Hofbauer KG, Studer W, Mah SC, Michel JB, Wood JM, Stadler R 1984 The significance of vasopressin as a pressor agent. J Cardiovasc Pharmac 6:S429–S438

    Article  Google Scholar 

  19. deWied D, Elands J, Kovacs G 1991 Interactive effects of neurohypophyseal neuropeptides with receptor antagonist on passive avoidance behavior: mediation by a cerebral neurohypophyseal hormone receptor? Proc Natl Acad Sci U S A 88:1494–1498

    Article  CAS  Google Scholar 

  20. Wilkinson MF, Kasting NW 1987 The antipyretic effect of centrally administered vasopressin at different ambient temperatures. Brain Res 415:275–280

    Article  PubMed  CAS  Google Scholar 

  21. Noszczyk B, Lon S, Sadowska S 1993 Central cardiovascular effects of AVP and AVP analogs with V1, V2 and ‘V3’ agonistic or antagonistic properties in conscious dog. Brain Res 610:115–126

    Article  PubMed  CAS  Google Scholar 

  22. Sawchenko PE, Swanson LW 1982 Immunohistochemical identification of neurons in the paraventricular nucleus of the hypothalamus that project to the medulla or to the spinal cord in the rat. J Comp Neurol 205:260–272

    Article  PubMed  CAS  Google Scholar 

  23. Saper CB, Loewy AD, Swanson LW, Cowan WM 1976 Direct hypothalamo-autonomic connections. Brain Res 117:305–312

    Article  PubMed  CAS  Google Scholar 

  24. Hosoya Y, Sugiura Y, Okado N, Loewy AD, Kohno K 1991 Descending input from the hypothalamic para-ventricular nucleus to sympathetic neurons in the rat. Exp Brain Res 85:10–20

    Article  PubMed  CAS  Google Scholar 

  25. Swanson LW 1977 Immunohistochemical evidence fora neurophysin-containing autonomic pathway arising in the paraventricular nucleus of the hypothalamus. Brain Res 128:346–353

    Article  PubMed  CAS  Google Scholar 

  26. Cechetto DF, Saper CB 1988 Neurochemical organization of the hypothalamic projection to the spinal cord in the rat. J Comp Neurol 272:579–604

    Article  PubMed  CAS  Google Scholar 

  27. Swanson LW, McKellar S 1979 The distribution of oxytocin-and neurophysin-stained fibers in the spinal cord of the rat and monkey. J Comp Neurol 188:87–106

    Article  PubMed  CAS  Google Scholar 

  28. Sofroniew MV 1985 Vasopressin, oxytocin and their related neurophysin. In: Bjorklund A, Hokfelt T (eds) Handbook of Chemical Neuroanatomy. GABA and Neuropeptides in the CNS, Amsterdam, Elsevier pp 93–165

    Google Scholar 

  29. Milian MJ, Milian MH, Czlonkowski A, Herz A 1984 Vasopressin and oxytocin in the rat spinal cord: distribution and origins in comparison to [Met]enkephalin, dynorphin and related opioids and their irresponsiveness to stimuli modulating neurohypophyseal secretion. Neuroscience 13:179–187

    Article  Google Scholar 

  30. Pretel S, Piekut DT 1989 Mediation of changes in paraventricular vasopressin and oxytocin mRNA content to the medullary vagal complex and spinal cord of the rat. J Chem Neuroanat 2:327–334

    PubMed  CAS  Google Scholar 

  31. Malpas SC, Coote JH 1994 Role of vasopressin in sympathetic response to paraventricular nucleus stimulation in anesthetized rats. Am J Physiol 266:Pt 2):R228–36

    PubMed  CAS  Google Scholar 

  32. Kolaj M, Shefchyk SJ, Renaud LP 1997 Two conductances mediate thyrotropin-releasing hormone-induced depolarization of neonatal rat spinal preganglionic and lateral horn neurons. J Neurophysiol 78:1726–1729

    PubMed  CAS  Google Scholar 

  33. Pickering AE, Spanswick D, Logan SD 1991 Whole-cell recordings from sympathetic preganglionic neurons in rat spinal cord slices. Neurosci Lett 130:237–242

    Article  PubMed  CAS  Google Scholar 

  34. Shen E, Wu SY, Dun NJ 1994 Spontaneous and transmitter-induced rhythmic activity in neonatal rat sympathetic preganglionic neurons in vitro. J Neurophysiol 71:1197–1205

    PubMed  CAS  Google Scholar 

  35. Logan SD, Pickering AE, Gibson IC, Nolan MF, Spanswick D 1996 Electrotonic coupling between rat sympathetic preganglionic neurones in vitro. J Physiol (Lond) 495:491–502

    PubMed  CAS  Google Scholar 

  36. Gilman AG 1984 G-proteins and dual control of adenylate cyclase. Cell 36:577–579

    Article  PubMed  CAS  Google Scholar 

  37. Benson DM, Blitzer RD, Landau EM 1988 An analysis of the depolarization produced in guinea-pig hippo-campus by cholinergie receptor stimulation. J Physiol (Lond) 404:479–496

    PubMed  CAS  Google Scholar 

  38. Bayliss DA, Viana F, Berger AJ 1992 Mechanisms underlying excitatory effects of thyrotropin-releasing hormone on rat hypoglossal motoneurons in vitro. J Neurophysiol 68:1733–1745

    PubMed  CAS  Google Scholar 

  39. Dong XW, Morin D, Feldman JL 1996 Multiple actions of 1S,3R-ACPD in modulating endogenous synaptic transmission to spinal respiratory motoneurons. J Neurosci 16:4971–4982

    PubMed  CAS  Google Scholar 

  40. Creba JA, Downes CP, Hawkins PT, Brewster G, Michell RH, Kirk CJ 1983 Rapid breakdown of phosphatidylinositol 4-phosphate and phosphatidylinositol 4,5-bisphosphate in rat hepatocytes stimulated by vasopressin and other Ca-mobilizing hormones. Biochem J 212:733–747

    PubMed  CAS  Google Scholar 

  41. Berridge MJ 1987 Inositol trisphosphate and diacylglycerol: two interacting second messengers. Ann Rev Biochem 56:159–193

    Article  PubMed  CAS  Google Scholar 

  42. Jurzak M, Müller AR, Gerstberger R 1995 Characterization of vasopressin receptors in cultured cells derived from the region of rat brain circumventricular organs. Neuroscience 65:1145–1159

    Article  PubMed  CAS  Google Scholar 

  43. Fisher SK, Heacock AM, Agranoff BW 1992 Inositol lipids and signal transduction in the nervous system: an update. J Neurochem 58:18–38

    Article  PubMed  CAS  Google Scholar 

  44. Wickman K, Clapham DE 1995 Ion channel regulation by G proteins. Physiol Rev 75:865–885

    PubMed  CAS  Google Scholar 

  45. Lidofsky SD, Xie MH, Sostman A, Scharschmidt BF, Fitz JG 1993 Vasopressin increases cytosolic sodium concentration in hepatocytes and activates calcium influx through cation-selective channels. J Biol Chem 268:14632–14636

    PubMed  CAS  Google Scholar 

  46. Zhang S, Hirano Y, Hiraoka M 1995 Arginine vasopressin-induced potentiation of unitary L-type Ca2+ channel current in guinea pig ventricular myocytes. Cire Res 76:592–599

    Article  CAS  Google Scholar 

  47. Thorn P, Petersen OH 1991 Activation of voltage-sensitive Ca2+ currents by vasopressin in an insulin-secreting cell line. J Membr Biol 124:63–71

    Article  PubMed  CAS  Google Scholar 

  48. Thibonnier M, Bayer AL, Simonson MS, Kester M 1991 Multiple signaling pathways of V1-vascular vasopressin receptors of A7r5 cells. Endocrinology 129:2845–2856

    Article  PubMed  CAS  Google Scholar 

  49. Byron KL, Taylor CW 1995 Vasopressin stimulation of Ca2+ mobilization, two bivalent cation entry pathways and Ca2+ efflux in A7r5 rat smooth muscle cells. J Physiol (Lond) 485:455–468

    PubMed  CAS  Google Scholar 

  50. VanRenterghem C, Romey G, Lazdunski M 1988 Vasopressin modulates the spontaneous electrical activity in aortic cells (line A7r5) by acting on three different types of ionic channels. Proc Natl Acad Sci U S A 85:9365–9369

    Article  CAS  Google Scholar 

  51. Riphagen CL, Pittman QJ 1985 Vasopressin influences renal function via a spinal action. Brain Res 336:346–349

    Article  PubMed  CAS  Google Scholar 

  52. Riphagen CL, Pittman QJ 1985 Cardiovascular responses to intrathecal administration of arginine vasopressin in rats. Reg Peptides 10:293–298

    Article  CAS  Google Scholar 

  53. Riphagen CL, Pittman QJ 1989 Mechanisms underlying the cardiovascular responses to intrathecal vasopressin administration in rats. Can J Physiol Pharmacol 67:269–275

    Article  PubMed  CAS  Google Scholar 

  54. 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 U S A 91:9636–9640

    Article  PubMed  CAS  Google Scholar 

  55. Iwasaki Y, Kinoshita M, Ikeda K, Shiojima T, Kurihara T, Appel SH 1991 Trophic effect of angiotensin II, vasopressin and other peptides on the cultured ventral spinal cord of rat embryo. J Neurol Sci 103:151–155

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 1998 Springer Science+Business Media New York

About this chapter

Cite this chapter

Kolaj, M., Renaud, L.P. (1998). Vasopressin’s Depolarizing Action on Neonatal Rat Spinal Lateral Horn Neurons May Involve Multiple Conductances. In: Zingg, H.H., Bourque, C.W., Bichet, D.G. (eds) Vasopressin and Oxytocin. Advances in Experimental Medicine and Biology, vol 449. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-4871-3_26

Download citation

  • DOI: https://doi.org/10.1007/978-1-4615-4871-3_26

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4613-7210-3

  • Online ISBN: 978-1-4615-4871-3

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics