Skip to main content
SpringerLink
Log in

Electrophysiological Studies of Oxytocin Neurons in Organotypic Slice Cultures

  • Chapter
Vasopressin and Oxytocin

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

Abstract

We have developed organotypic slice cultures derived from postnatal rat hypothalamus which contain well-differentiated oxytocin neurons. Intracellular recordings of identified neurons show that these cultured oxytocin cells exhibit basal electrical properties closely similar to those of magnocellular cells recorded in vivo and in acute in vitro preparations from adult animals. The cultures also include GABAergic and glutamatergic neurons making connections with the oxytocin cells, which strongly suggests that the rich GABAergic and glutamatergic innervations of adult oxytocin neurons in vivo derive largely from local hypothalamic sources. Pharmacological manipulations indicate that the cultured oxytocin neurons present functional GABAA (but not GABAB) receptors, and ionotropic non-NMDA and NMDA receptors, but no metabotropic receptors for glutamate. These synaptic inputs control to a great extent the electrical activity of oxytocin neurons. Of particular interest is our observation that the cultured oxytocin neurons display a recurrent bursting activity which does not appear to result from an endogenous regenerative activity, but from a patterned glutamatergic input. Our preliminary data show that oxytocin plays a facilitatory role in this bursting activity and suggest that such activity is generated within an hypothalamic circuitry.

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

Access this chapter

Log in via an institution
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.

Similar content being viewed by others

References

  1. Poulain DA, Wakerley JB 1982 Electrophysiology of hypothalamic magnocellular neurones secreting oxy­tocin and vasopressin. Neuroscience 7:773–808

    Article  PubMed  CAS  Google Scholar 

  2. Lincoln DW, Wakerley JB 1974 Electrophysiological evidence for the activation of supraoptic neurones during the release of oxytocin. J Physiol 242:533–554

    PubMed  CAS  Google Scholar 

  3. Armstrong WE, Smith BN, Tian M 1994 Electrophysiological characteristics of immunochemically identified rat oxytocin and vassopressin neurones in vitro J Physiol 475:115–128

    PubMed  CAS  Google Scholar 

  4. Stern JE, Armstrong WE 1995 Electrophysiological differences between oxytocin and vasopressin neurones recorded from female rats in vitro J Physiol 488:701–708

    PubMed  CAS  Google Scholar 

  5. Stern JE, Armstrong WE 1996 Changes in the electrical properties of supraoptic nucleus oxytocin and vasopressin neurons during lactation. J Neurosci 16:4861–4871

    PubMed  CAS  Google Scholar 

  6. Jourdain P, Poulain DA, Theodosis DT, Israel JM 1996 Electrical properties of oxytocin neurons in organotypic cultures from postnatal rat hypothalamus. J Neurophysiol 76:2772–2785

    PubMed  CAS  Google Scholar 

  7. Stern JE, Armstrong WE 1997 Sustained outward rectification of oxytocinergic neurones in the rat supraoptic nucleus: ionic dependence and pharmacology. J Physiol 500:497–508

    PubMed  CAS  Google Scholar 

  8. Gähwiler BH 1981 Organotypic monolayer cultures of nervous tissue. J Neurosci Methods 4:329–342

    Article  PubMed  Google Scholar 

  9. Sofroniew MV, Dreifuss JJ, Gähwiler BH 1988 Slice cultures of rat hypothalamus examined by immunohistochemical staining for neurohypophyseal peptides and GFAP. Brain Res Bull 20:669–674

    Article  PubMed  CAS  Google Scholar 

  10. Wray S, Kusano K, Gainer H 1991 Maintenance of LHRH and oxytocin neurons in slice explants cultured in serum-free media: effects of tetrodotoxin on gene expression. Neuroendocrinology 54:327–339

    Article  PubMed  CAS  Google Scholar 

  11. Herman JP, Marciano FF, Wiegand SJ, Gash DM 1987 Selective cell death of magnocellular vasopressin neurons in neurohypophysectomized rats following chronic administration of vasopressin. J Neurosci 7:2564–2575

    PubMed  CAS  Google Scholar 

  12. Dohanics J, Hoffman GE, Verbalis JG 1996 Chronic hyponatremia reduces survival of magnocellular vasopressin and oxytocin neurons after axonal injury. J Neurosci 16:2373–2380

    PubMed  CAS  Google Scholar 

  13. Theodosis DT, Poulain DA 1996 Pulsatile neuronal activity and structural synaptic plasticity of the adult oxytocinergic system. Current Opinion in Endocrinology and Diabetes 3:164–170

    Article  Google Scholar 

  14. Gähwiler BH, Dreifuss JJ 1979 Phasically firing neurons in long-term cultures of the rat hypothalamic supraoptic area: pacemaker and follower cells. Brain Res 177:95–103

    Article  PubMed  Google Scholar 

  15. Gainer H, Kusano K, Wray S 1993 Hypothalamic slice-explant cultures as models for the long-term study of gene expression and cellular activity. Regulatory Peptides:5:25–29

    Article  Google Scholar 

  16. Dyball REJ, Tasker JG, Wuarin J-P, Dudek FE 1991 In vivo intracellular recording of neurons in the supraoptic nucleus of the rat hypothalamus. J Neuroendocrinol 3:383–386

    Article  PubMed  CAS  Google Scholar 

  17. Bourque CW, Renaud LP 1991 Membrane properties of rat magnocellular neuroendocrine cells in vivo. Brain Res 540:349–352

    Article  PubMed  CAS  Google Scholar 

  18. Mason WT 1983 Electrical properties of neurons recorded from the rat supraoptic nucleus in vitro. Proc R Soc Lond B 217:141–161

    Article  PubMed  CAS  Google Scholar 

  19. Oliet SHR, Bourque CW 1992 Properties of supraoptic magnocellular neurones isolated from the adult rat. J Physiol 455:291–306

    PubMed  CAS  Google Scholar 

  20. Andrew RD, Dudek FE 1984 Intrinsic inhibition in magnocellular neuroendocrine cells of rat hypothalamus. J Physiol 353:171–185

    PubMed  CAS  Google Scholar 

  21. Bourque CW, Renaud LP 1985 Calcium-dependent action potentials in rat supraoptic neurosecretory neurones recorded in vitro. J Physiol 363:419–428

    PubMed  CAS  Google Scholar 

  22. Erickson KR, Ronnekleiv OK, Kelly MJ 1993 Electrophysiology of guinea-pig supraoptic neurones: role of a hyperpolarization-activated cation current in phasic firing. J Physiol 460:407–425

    PubMed  CAS  Google Scholar 

  23. Andrew RD, Dudek FE 1984 Analysis of intracellularly recorded phasic bursting by mammalian neuroendocrine cells. J Neurophysiol 51:552–566

    PubMed  CAS  Google Scholar 

  24. Bourque CW 1988 Transient calcium-dependent potassium current in magnocellular neurosecretory cells of the rat supraoptic nucleus. J Physiol 397:331–347

    PubMed  CAS  Google Scholar 

  25. Bourque CW, Renaud LP 1985 Activity dependence of action potential duration in rat supraoptic neurosecretory neurones recorded in vitro. J Physiol 363:429–439

    PubMed  CAS  Google Scholar 

  26. Renaud LP, Bourque CW 1991 Neurophysiology and neuropharmacology of hypothalamic magnocellular neurons secreting vasopressin and oxytocin. Prog Neurobiol 36:131–169

    Article  PubMed  CAS  Google Scholar 

  27. Armstrong WE 1995 Morphological and electrophysiological classification of hypothalamic supraoptic neurons. Prog Neurobiol 47:291–339

    PubMed  CAS  Google Scholar 

  28. Randle JCR, Renaud LP 1987 Actions of gamma-aminobutyric acid on rat supraoptic nucleus neurosecretory neurones in vitro. J Physiol 387:629–647

    PubMed  CAS  Google Scholar 

  29. Voisin DL, Herbison AE, Poulain DA 1995 Central inhibitory effects of muscimol and bicuculline on the milk ejection reflex in the anaesthetized rat. J Physiol 483:211–224

    PubMed  CAS  Google Scholar 

  30. Moos FC 1995 GABA-induced facilitation of the periodic bursting activity of oxytocin neurones in suckled rats. J Physiol 488:103–114

    PubMed  CAS  Google Scholar 

  31. Voisin DL, Herbison AE, Chapman C, Poulain DA 1996 Effects of central GABA-B receptor modulation upon the milk ejection reflex in the rat. Neuroendocrinology 63:368–376

    Article  PubMed  CAS  Google Scholar 

  32. Hu B, Bourque CW 1991 Functional N-Methyl-D-Aspartate and non-N-Methyl-D-Aspartate receptors are expressed by rat supraoptic neurosecretory cells in vitro. J Neuroendocrinol 3:509–514

    Article  PubMed  CAS  Google Scholar 

  33. Meeker RB, Greenwood RS, Hayward JN 1994 Glutamate receptors in the rat hypothalamus and pituitary. Endocrinology 134:621–629

    Article  PubMed  CAS  Google Scholar 

  34. Petralia RS, Yokotani N, Wenthold RJ 1994 Light and electron microscope distribution of the NMDA receptor subunit NMDARI in the rat nervous system using selective anti-peptide antibody. J Neurosci 14:667–696

    PubMed  CAS  Google Scholar 

  35. Van Den Pol AN, Wuarin J-P, Dudek FE 1990 Glutamate, the dominant excitatory transmitter in neuroendocrine regulation. Science 250:1276–1278

    Article  PubMed  Google Scholar 

  36. Parker SL, Crowley WR 1993 Stimulation of oxytocin release in the lactating rat by central exitatory amino acid mechanisms: evidence for specific involvement of R,S-alpha-amino-3-hydroxy-5-methylisoxazole-4-propionic acid-sensitive glutamate receptors. Endocrinology 133:2847--2854

    Article  PubMed  CAS  Google Scholar 

  37. Hu B. Bourque CW 1992 NMDA receptor-mediated rhythmic bursting activity in rat supraoptic nucleus neurones in vitro J Physiol 458:667–687

    PubMed  CAS  Google Scholar 

  38. Moos FC, Rossi K, Richard P 1997 Activation of N-Methyl-D-Aspartate receptors regulates basal electrical activity of oxytocin and vasopressin neurons in lactating rats. Neuroscience 77:993–1002

    Article  PubMed  CAS  Google Scholar 

  39. Richard P, Moos F, Freund-Mercier M.I 1991 Central effects of oxytocin. Physiol Rev 71:331–370

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institut François Magendie, INSERM U. 378, 1 Rue Camille Saint Saens, F33077, Bordeaux, France

    P. Jourdain, B. Dupouy, R. Bonhomme, D. T. Theodosis, D. A. Poulain & J. M. Israel

Authors
  1. P. Jourdain
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. B. Dupouy
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. R. Bonhomme
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. D. T. Theodosis
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. D. A. Poulain
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. J. M. Israel
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. McGill University, Montreal, Quebec, Canada

    Hans H. Zingg  & Charles W. Bourque  & 

  2. University of Montreal, Montreal, Quebec, Canada

    Daniel G. Bichet

Rights and permissions

Reprints and permissions

Copyright information

© 1998 Springer Science+Business Media New York

About this chapter

Cite this chapter

Jourdain, P., Dupouy, B., Bonhomme, R., Theodosis, D.T., Poulain, D.A., Israel, J.M. (1998). Electrophysiological Studies of Oxytocin Neurons in Organotypic Slice Cultures. 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_16

Download citation

  • DOI: https://doi.org/10.1007/978-1-4615-4871-3_16

  • 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

Search

Navigation