Pflügers Archiv

, Volume 450, Issue 2, pp 96–110 | Cite as

Frequency-dependent potentiation of voltage-activated responses only in the intact neurohypophysis of the rat

Ion Channels, Transporters
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Abstract

The loose-patch-clamp technique was used with multiple-pulse protocols to study the frequency dependence of currents from the surface of the intact rat neurohypophysis (NH) and hypothalamus. In the NH, but not in the corresponding supraoptic nucleus of the hypothalamus, an initial, single pulse of 3–8 ms duration (long pulse) potentiated a secondary pulse response starting 20–50 ms after the initial pulse. Potentiation was abolished by 4-aminopyridine (4-AP), but not by tetraethylammonium (TEA) chloride or tetrandrine, indicating the participation of A-type potassium currents. Potentiation was also abolished by CdCl2, CoCl2 or 1 µM nicardipine, indicating the participation of calcium currents. The potentiation was reduced significantly in the presence of 4–6 mM extracellular CaCl2, indicating that the potentiation is not due to calcium influx. An initial train with as few as two pulses, each of 0.3–0.7 ms duration (short pulses) at 64–1,100 Hz also potentiated the secondary short pulse response significantly. We conclude that voltage-gated channels underlie this potentiation, which is due to interstitial calcium and potassium homeostasis changes induced by action potential activity and occurs only in the intact NH. A model is proposed for the participation of calcium and potassium channels in the burst patterning that is optimal for secretion from the NH.

Keywords

A-Type current Ca2+ currents Na current Nerve terminals Loose-patch 
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References

  1. 1.
    Andrew RD, Dudek FE (1983) Burst discharge in mammalian neuroendocrine cells involves an intrinsic regenerative mechanism. Science 221:1050–1052Google Scholar
  2. 2.
    Bourke CW, Kirkpatrick K, Jarvis CR (1998) Extrinsic modulation of spike afterpotentials in rat hypothalamoneurohypophysial neurons. Cell Mol Neurobiol 18:3–12CrossRefGoogle Scholar
  3. 3.
    Bouron A, Reuter H (1996) A role of intracellular Na+ in the regulation of synaptic transmission and turnover of the vesicular pool in cultured hippocampal cells. Neuron 17:969–978CrossRefGoogle Scholar
  4. 4.
    Cazalis M, Dayanithi G, Nordman JJ (1985) The role of pattern burst and interburst interval on the excitation-coupling mechanism in the isolated rat neural lobe. J Physiol (Lond) 369:45–60Google Scholar
  5. 5.
    Egelman DM, Montague PR (1998) Computational properties of peri-dendritic calcium fluctuations. J Neurosci 18:8580–8589Google Scholar
  6. 6.
    Egelman DM, Montague PR (1999) Calcium dynamics in the extracellular space of mammalian neural tissue. Biophys J 76:1856–1867Google Scholar
  7. 7.
    Fonnum F, Johsen A, Bjørnar H (1997) Use of fluoroacetate in the study of brain metabolism. Glia 21:106–113Google Scholar
  8. 8.
    Gainer H, Wolfe SA Jr, Obaid AL, Salzberg BM (1986) Action potentials and frequency-dependent secretion in the mouse neurohypophysis. Neuroendocrinology. 43:557–563Google Scholar
  9. 9.
    Hanck DA, Sheets MF (1992) Extracellular divalent and trivalent cation effects on sodium current kinetics in single canine cardiac Purkinje cells. J Physiol (Lond) 454:267–298Google Scholar
  10. 10.
    Lemos JR (2001) Magnocellular neurons. Encyclopedia of Life Sciences A176:1–5Google Scholar
  11. 11.
    Lemos JR, Nowycky MC (1989) Two types of calcium channels coexist in peptide-releasing vertebrate nerve terminals. Neuron 2:1419–1426CrossRefGoogle Scholar
  12. 12.
    Leng G, Shibuki K (1987) Extracellular potassium changes in the rat neurohypophysis during activation of the magnocellular neurosecretory system. J Physiol (Lond) 392:97–111Google Scholar
  13. 13.
    Leng G, Shibuki K, Way SA (1988) Effects of raised extracellular potassium on the excitability of, and hormone release from, the isolated rat neurohypophysis. J Physiol (Lond) 399:591–605Google Scholar
  14. 14.
    Leng G, Brown CH, Russell JA (1999) Physiological pathways regulating the activity of magnocellular neurosecretory cells. Prog Neurobiol 57:625–655CrossRefGoogle Scholar
  15. 15.
    Marrero HG, Lemos JR (2001) Calcium and potassium currents affect the frequency-dependence of voltage-activated responses from the rat neurohypophysis (abstract). Biophys J 80:242AGoogle Scholar
  16. 16.
    Marrero HG, Lemos JR (2003) Loose-patch clamp currents from the hypothalamo-neurohypophysial system of the rat. Pflugers Arch 446:702–713CrossRefGoogle Scholar
  17. 17.
    Muschol M, Salzberg BM (2000) Dependence of transient and residual calcium dynamics on action-potential patterning during neuropeptide secretion. J Neurosci 20:6773–6780Google Scholar
  18. 18.
    Paulsen RE, Contestabile A, Villani L, Fonnum F (1987) An in vivo model for studying function of brain tissue temporarily devoid of glial cell metabolism: the use of fluorocitrate. J Neurochem 48:1377–1385Google Scholar
  19. 19.
    Poulain DA, Wakerley JB (1982) Electrophysiology of hypothalamic magnocellular neurones secreting oxytocin and vasopressin. Neuroscience 7:773–808CrossRefGoogle Scholar
  20. 20.
    Seward EP, Chernevskaya NI, Nowicky MC (1995) Exocytosis in peptidergic nerve terminals exhibits two calcium-sensitive phases during pulsatile calcium entry. J Neurosci 15:3390–3399Google Scholar
  21. 21.
    Sheets MF, Hanck DA (1992) Mechanisms of extracellular divalent and trivalent cation block of the sodium current in canine cardiac Purkinje cells. J Physiol (Lond) 454:299–320Google Scholar
  22. 22.
    Shibuki K (1990) Activation of neurohypophysial vasopressin release by Ca2+ influx and intracellular Ca2+ accumulation in the rat. J Physiol (Lond) 422:321–331Google Scholar
  23. 23.
    Stuenkel EL, Nordman JJ (1993) Sodium-evoked, calcium-independent vasopressin release from rat isolated neurohypophysial nerve endings. J Physiol (Lond) 468:357–378Google Scholar
  24. 24.
    Thirion S, Troadec J-D, Pivovarova NB, Pagnotts S, Andrews SB, Leapman RD, Nicaise G (1999) Stimulus-secretion coupling in neurohypophysial nerve endings: a role for intravesicular calcium? Proc Natl Acad Sci USA 96:3206–3210CrossRefGoogle Scholar
  25. 25.
    Thorn PJ, Wang X, Lemos JR (1991) A fast, transient K+ current in neurohypophysial nerve terminals. J Physiol (Lond) 432:313–326Google Scholar
  26. 26.
    Turner D, Stuenkel EL (1998) Effects of depolarization-evoked Na+ influx on intracellular Na+ concentration at neurosecretory nerve endings. Neuroscience 86:547–556CrossRefGoogle Scholar
  27. 27.
    Wang G, Lemos JR (1992) Tetrandrine blocks a slow, large-conductance, Ca+2-activated potassium channels besides inhibiting a non-inactivating Ca+2 current in isolated nerve terminals of the rat neurohypophysis. Pflugers Arch 421:558–565CrossRefGoogle Scholar
  28. 28.
    Wang G, Dayanithi G, Kim S, Hom D, Nadasdi L, Kristipati R, Rmachandran J, Stuenkel EL, Nordman JJ, Newcomb R, Lemos JR (1997) Role of Q-type Ca2+ channel in vasopressin secretion from neurohypophysial terminals of the rat. J Physiol (Lond) 502.2:351–363Google Scholar
  29. 29.
    Wang G, Dayanithi G, Newcomb R, Lemos, JR (1999) An R-type Ca2+ current in neurohypophysial terminals preferentially regulates oxytocin secretion. J Neurosci 19:9235–9241Google Scholar
  30. 30.
    Wang X, Treistman SN, Lemos JR (1992) Two types of high-threshold calcium currents inhibited by ω-conotoxin in nerve terminals of rat neurohypophysis. J Physiol (Lond) 445:181–199Google Scholar
  31. 31.
    Wang X, Treistman SN, Lemos JR (1993) Single channel recordings of Nt- and L-type Ca2+ currents in rat neurohypophysial terminals. J Neurophysiol 70:1617–1628Google Scholar
  32. 32.
    Woodhull AM (1973) Ionic blockage of sodium channels in nerve. J Gen Physiol 61:687–708CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag  2005

Authors and Affiliations

  1. 1.Department of Physiology & Neuroscience ProgramUniversity of Massachusetts Medical SchoolWorcesterUSA

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