Glutamatergic input governs periodicity and synchronization of bursting activity in oxytocin neurons in hypothalamic organotypic cultures

European Journal of Neuroscience

Volumn 17, Issue 12, 2003, Pages 2619-2629

  Israel, Jean Marc ^a   Le Masson, Gwendal ^a   Theodosis, Dionysia T ^a   Poulain, Dominique A ^a  

^a INSERM   (France)

Author keywords

Correlated firing; Intracellular recording; Organotypic slice cultures; Rat hypothalamus

Indexed keywords

6 CYANO 7 NITRO 2,3 QUINOXALINEDIONE; FLUORESCENT DYE; GLUTAMIC ACID; HALOTHANE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; OXYTOCIN; PROPIONIC ACID; VASOPRESSIN RECEPTOR;

ACTION POTENTIAL; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CELL POPULATION; CELL SYNCHRONIZATION; CONTROLLED STUDY; DEPOLARIZATION; EXCITATORY POSTSYNAPTIC POTENTIAL; HYPOTHALAMUS; IMMUNOCYTOCHEMISTRY; LACTATION; MEMBRANE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; RAT; RETROSPECTIVE STUDY; SUCKLING;

6-CYANO-7-NITROQUINOXALINE-2,3-DIONE; ACTION POTENTIALS; ANESTHETICS, INHALATION; ANIMALS; ANIMALS, NEWBORN; BICUCULLINE; BIOTIN; CALCIUM; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; ELECTRIC STIMULATION; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; GABA ANTAGONISTS; GLUTAMIC ACID; HALOTHANE; HYPOTHALAMUS; LYSINE; NEURONS; NEUROPHYSINS; ORGAN CULTURE TECHNIQUES; OXYTOCIN; PERIODICITY; PROPIONATES; RATS; RATS, WISTAR; VASOPRESSINS;

EID: 0038684216     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.2003.02705.x     Document Type: Article

References (39)

1. Alonso, J.M., Usrey, W.M. & Reid, R.C. (1996) Precisely correlated firing in cells of the lateral geniculate nucleus. Nature, 383, 815-818.
2. Belin, V. & Moos, F. (1986) Paired recordings from supraoptic and paraventricular oxytocin cells in suckled rats: recruitment and synchronization. J. Physiol. (Lond.), 377, 369-390.
3. Belin, V., Moos, F. & Richard, P. (1984) Synchronization of oxytocin cells in the hypothalamic paraventricular and supraoptic nuclei in suckled rats: direct proof with paired extracellular recordings. Exp. Brain Res., 57, 201-203.
4. Ben-Barak, Y., Russell, J.T., Whitnall, M.H., Ozato, K. & Gainer, H. (1985) Neurophysin in the hypothalamo-neurohypophysial system: I. production and characterization of monoclonal antibodies. J. Neurosci., 5, 81-97.
5. Boudaba, C., Schrader, L.A. & Tasker, J.G. (1997) Physiological evidence for local excitatory synaptic circuits in the rat hypothalamus. J. Neurophysiol., 77, 3396-3400.
6. Brown, D. Fontanaud, P. & Moos, F. (2000) The variability of basal action potential firing is positively correlated with bursting in hypothalamic oxytocin neurones. J. Neuroendocrinol., 12, 506-520.
7. Brown, D. & Moos, F. (1997) Onset of bursting in oxytocin cells in suckled rats. J. Physiol. (Lond.), 503, 625-634.
8. Brussaard, A.B., Kits, K.S. & de Vlieger, T.A. (1996) Postsynaptic mechanism of depression of GABAergic synapses by oxytocin in the supraoptic nucleus of immature rat. J. Physiol. (Lond.), 497, 495-507.
9. Buchs, P.-A., Stoppini, L. & Muller, D. (1993) Structural modifications associated with synaptic development in area CA1 of rat hippocampal organotypic cultures. Dev. Brain Res., 71, 81-91.
10. Dan, Y., Alonso, J.-M., Usrey, W.M. & Reid, R.C. (1998) Coding of visual information by precisely correlated spikes in the lateral geniculate nucleus. Nature Neurosci., 1, 501-505.
11. El Majdoubi, M., Poulain, D.A. & Theodosis, D.T. (1996) The glutamatergic innervation of oxytocin- and vasopressin-secreting neurons in the rat supraoptic nucleus and its contribution to lactation-induced synaptic plasticity. Eur. J. Neurosci., 8, 1377-1389.
12. El Majdoubi, M., Poulain, D.A. & Theodosis, D.T. (1997) Lactation-induced plasticity in the supraoptic nucleus augments axodendritic and axosomatic gabaergic and glutamatergic synapses: an ultrastructural analysis using the disector method. Neuroscience, 80, 1137-1147.
13. Freund-Mercier, M.J. & Richard, P. (1984) Electrophysiological evidence for facilitatory control of oxytocin neurones by oxytocin during suckling in the rat. J. Physiol. (Lond.), 352, 447-466.
14. Freund-Mercier, M.J., Stoeckel, M.E. & Klein, M.J. (1994) Oxytocin receptors on oxytocin neurones: histoautoradiographic detection in the lactating rat. J. Physiol. (Lond.), 480, 155-161.
15. Gähwiler, B.H., Capogna, M., Debanne, D., McKinney, R.A. & Thompson, S.M. (1997) Organotypic slice cultures: a technique has come of age. Trends Neurosci., 20, 471-477.
16. Gainer, H., Kusano, K. & Wray, S. (1993) Hypothalamic slice-explant cultures as models for long-term study of gene expression and cellular activity. Regul. Pept., 45, 25-29.
17. Hatton, G.I. (1997) Function-related plasticity in hypothalamus. Ann. Rev. Neurosci., 20, 375-397.
18. Hatton, G.I. & Yang, Q.Z. (1994) Incidence of neuronal coupling in supraoptic nuclei of virgin and lactating rats: estimation by neurobiotin and lucifer yellow. Brain Res., 650, 63-69.
19. Hatton, G.I., Yang, Q.Z. & Cobbett, P. (1987) Dye coupling among immunocytochemically identified neurons in the supraoptic nucleus: increased incidence in lactating rats. Neuroscience, 21, 923-930.
20. Hirasawa, M., Kombian, S.B. & Pittman, Q.J. (2001) Oxytocin retrogradely inhibits evoked, but not miniature, EPSCs in the rat supraoptic nucleus: role of N- and P/Q-type calcium channels. J. Physiol. (Lond.), 532, 595-607.
21. Jourdain, P., Dupouy, B., Bonhomme, R., Poulain, D.A., Israel, J.M. & Theodosis, D.T. (1999) Visualization of local afferent inputs to magnocellular oxytocin neurons in vitro. Eur. J. Neurosci., 11, 1-13.
22. Jourdain, P., Israel, J.M., Dupouy, B., Oliet, S.H.R., Allard, M., Vitiello, S., Theodosis, D.T. & Poulain, D.A. (1998) Evidence for a hypothalamic oxytocin-sensitive pattern-generating network governing oxytocin neurons in vitro. J. Neurosci., 18, 6641-6649.
23. Jourdain, P., Poulain, D.A., Theodosis, D.T. & Israel, J.M. (1996) Electrical properties of oxytocin neurons in organotypic cultures from postnatal rat hypothalamus. J. Neurophysiol., 76, 2772-2785.
24. Lambert, R.C., Dayanithi, G., Moos, F.C. & Richard, P. (1994) A rise in the intracellular Ca2+ concentration of isolated rat supraoptic cells in response to oxytocin. J. Physiol. (Lond.), 478, 275-288.
25. Lambert, R.C., Moos, F.C. & Richard, P. (1993) Action of endogenous oxytocin within the paraventricular or supraoptic nuclei: a powerful link in the regulation of the bursting pattern of oxytocin neurons during the milk-ejection reflex in rats. Neuroscience, 57, 1027-1038.
26. Lincoln, D.W. & Wakerley, J.B. (1974) Electrophysiological evidence for the activation of supraoptic neurones during the release of oxytocin. J. Physiol. (Lond.), 242, 533-554.
27. Ludwig, M. (1998) Dendritic release of vasopressin and oxytocin. J. Neuroendocrinol., 10, 881-895.
28. Ludwig, M., Sabatier, N., Bull., P.M., Landgraf, R., Dayanithi, G. & Leng, G. (2002) Intracellular calcium stores regulate activity-dependent neuropeptide release from dendrites. Nature, 418, 85-89.
29. Moos, F. & Richard, P. (1989) Paraventricular and supraoptic bursting oxytocin cells in rat are locally regulated by oxytocin and functionally related. J. Physiol. (Lond.), 408, 1-18.
30. Perez-Velazquez, J.L., Valiante, T.A. & Carlen, P.L. (1994) Modulation of gap junctional mechanisms during calcium-free induced field burst activity: a possible role for electrotonic coupling in epileptogenesis. J. Neurosci., 14, 4308-4317.
31. Poulain, D.A. & Wakerley, J.B. (1982) Electrophysiology of hypothalamic magnocellular neurones secreting oxytocin and vasopressin. Neuroscience, 7, 773-808.
32. Richard, P., Moos, F. & Freund-Mercier, M.J. (1991) Central effects of oxytocin. Physiol. Rev., 71, 331-370.
33. Roberts, M.M., Robinson, A.G., Hoffman, G.E. & Fitzsimmons, M.D. (1991) Vasopressin transport regulation is coupled to synthesis rate. Neuroendocrinology, 53, 416-422.
34. Takano, S., Negoro, H., Honda, K. & Higuchi, T. (1992) Lesion and electrophysiological studies on the hypothalamic afferent pathway of the milk ejection reflex in the rat. Neuroscience, 50, 877-883.
35. Takuma, H., Sakurai, M. & Kanazawa, I. (2002) In vitro formation of corticospinal synapses in an organotypic slice co-culture. Neuroscience, 109, 359-370.
36. Teruyama, R. & Armstrong, W.E. (2002) Changes in the active membrane properties of rat supraoptic neurones during pregnancy and lactation. J. Neurosci., 14, 933-944.
37. Thellier, D., Moos, F.C., Richard, P. & Stoeckel, M.E. (1994) Evidence for connections between a discrete hypothalamic dorsochiasmatic area and the supraoptic and paraventricular nuclei. Brain Res. Bull., 34, 261-274.
38. Vutskits, L., Bartanusz, V., Schultz, M.-F. & Kiss, J.Z. (1998) Magnocellular vasopressinergic neurons in explant cultures are rescued from cell death by cilliary neurotrophic factor and leukemia inhibiting factor. Neuroscience, 87, 571-582.
39. Wakerley, J.B., Clarke, G. & Summerlee, A.J.S. (1994) Milk ejection and its control. In Knobil, E. & Neill, J.D. (eds), The Physiology of Reproduction, 2nd edn. Raven Press Ltd, New York, pp. 2283-2322.