Skip to main content
NCBI home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1988 May;399:591–605. doi: 10.1113/jphysiol.1988.sp017098

Effects of raised extracellular potassium on the excitability of, and hormone release from, the isolated rat neurohypophysis.

G Leng 1, K Shibuki 1, S A Way 1
PMCID: PMC1191682  PMID: 3404469

Abstract

1. Single neurohypophyses from male rats were maintained in an in vitro perifusion chamber. Ion-sensitive microelectrodes were introduced into the tissue to measure changes in [K+]o and [Ca2+]o during electrical stimulation. 2. Electrical stimulation at 6 Hz for 1 min and 30 Hz for 12 s raised [K+]o by 5.4 +/- 0.4 and 13.5 +/- 0.5 mM (mean +/- S.E.M., n = 8) respectively. To investigate the effects of raised [K+]o on the excitability of the neurosecretory terminals, stimulations were repeated in media of altered K+ concentration. The increase in [K+]o evoked by 6 Hz stimulation was elevated in 10 mM-K+ medium (133% of that in 5 mM-K+ medium) and reduced in 0 mM-K+ medium and in 25 mM-K+ medium. Thus it appeared that stimulus-induced changes in [K+]o might enhance the excitability of the tissue during electrical activation. 3. To test this hypothesis, we measured the field potential responses evoked by 0.5 Hz stimulation in media of different K+ concentrations. The size of the field potential was enhanced in 10 mM-K+ medium and depressed in 0 mM-K+ medium and in 25 mM-K+ medium. 4. Electrical stimulation (6 Hz, 1 min) decreased [Ca2+]o by 10.9 +/- 1.8% (n = 6). This decrease was absent in the presence of 1 microM-tetrodotoxin or 1 mM-cadmium. Again, the [Ca2+] response to stimulation was enhanced in 10 mM-K+ medium and depressed in 0 mM-K+ medium or 25 mM-K+ medium. 5. The release of vasopressin and oxytocin evoked by stimulation at 6 or 30 Hz from isolated neurohypophyses was measured by radioimmunoassay in a separate series of experiments. Stimulation at 30 Hz for 1 min released 5- to 6-fold more hormone than stimulation at 6 Hz for 5 min. Release evoked by 6 Hz stimulation was enhanced in 15 mM-K+ medium and depressed in 25 mM-K+ medium. 6. We conclude that the rise in [K+]o that accompanies high-frequency activation of axons and terminals in the neurohypophysis contributes to the facilitation of hormone release with increasing frequencies of stimulation, and in particular to the efficiency of the milk-ejection burst discharge of oxytocin neurones for evoking oxytocin release.

Full text

PDF
591

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bicknell R. J., Brown D., Chapman C., Hancock P. D., Leng G. Reversible fatigue of stimulus-secretion coupling in the rat neurohypophysis. J Physiol. 1984 Mar;348:601–613. doi: 10.1113/jphysiol.1984.sp015128. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bicknell R. J., Chapman C., Leng G. A perifusion system for studying neurosecretion from the isolated rat neurohypophysis in vitro. J Neurosci Methods. 1982 Jan;5(1-2):95–101. doi: 10.1016/0165-0270(82)90056-5. [DOI] [PubMed] [Google Scholar]
  3. Bloom S. R., Edwards A. V., Ghatei M. A. Neuroendocrine responses to stimulation of the splanchnic nerves in bursts in the conscious adrenalectomized calf. J Physiol. 1984 Jan;346:519–531. doi: 10.1113/jphysiol.1984.sp015038. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Czéh G., Kríz N., Syková E. Extracellular potassium accumulation in the frog spinal cord induced by stimulation of the skin and ventrolateral columns. J Physiol. 1981 Nov;320:57–72. doi: 10.1113/jphysiol.1981.sp013934. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Dreifuss J. J., Tribollet E., Mühlethaler M. Temporal patterns of neural activity and their relation to the secretion of posterior pituitary hormones. Biol Reprod. 1981 Feb;24(1):51–72. doi: 10.1095/biolreprod24.1.51. [DOI] [PubMed] [Google Scholar]
  6. Dutton A., Dyball R. E. Phasic firing enhances vasopressin release from the rat neurohypophysis. J Physiol. 1979 May;290(2):433–440. doi: 10.1113/jphysiol.1979.sp012781. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. HODGKIN A. L., KEYNES R. D. The potassium permeability of a giant nerve fibre. J Physiol. 1955 Apr 28;128(1):61–88. doi: 10.1113/jphysiol.1955.sp005291. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Krnjević K., Morris M. E. Extracellular K + activity and slow potential changes in spinal cord and medulla. Can J Physiol Pharmacol. 1972 Dec;50(12):1214–1217. doi: 10.1139/y72-177. [DOI] [PubMed] [Google Scholar]
  9. Kuffler S. W., Nicholls J. G., Orkand R. K. Physiological properties of glial cells in the central nervous system of amphibia. J Neurophysiol. 1966 Jul;29(4):768–787. doi: 10.1152/jn.1966.29.4.768. [DOI] [PubMed] [Google Scholar]
  10. Leng G., Shibuki K. Extracellular potassium changes in the rat neurohypophysis during activation of the magnocellular neurosecretory system. J Physiol. 1987 Nov;392:97–111. doi: 10.1113/jphysiol.1987.sp016771. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Nicoll R. A. Dorsal root potentials and changes in extracellular potassium in the spinal cord of the frog. J Physiol. 1979 May;290(2):113–127. doi: 10.1113/jphysiol.1979.sp012763. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Nordmann J. J. Stimulus-secretion coupling. Prog Brain Res. 1983;60:281–304. doi: 10.1016/S0079-6123(08)64397-6. [DOI] [PubMed] [Google Scholar]
  13. Nordmann J. J., Stuenkel E. L. Electrical properties of axons and neurohypophysial nerve terminals and their relationship to secretion in the rat. J Physiol. 1986 Nov;380:521–539. doi: 10.1113/jphysiol.1986.sp016300. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Nordmann J. J. Ultrastructural morphometry of the rat neurohypophysis. J Anat. 1977 Feb;123(Pt 1):213–218. [PMC free article] [PubMed] [Google Scholar]
  15. Orkand R. K., Nicholls J. G., Kuffler S. W. Effect of nerve impulses on the membrane potential of glial cells in the central nervous system of amphibia. J Neurophysiol. 1966 Jul;29(4):788–806. doi: 10.1152/jn.1966.29.4.788. [DOI] [PubMed] [Google Scholar]
  16. Summerlee A. J. Extracellular recordings from oxytocin neurones during the expulsive phase of birth in unanaesthetized rats. J Physiol. 1981 Dec;321:1–9. doi: 10.1113/jphysiol.1981.sp013967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Wakerley J. B., Lincoln D. W. The milk-ejection reflex of the rat: a 20- to 40-fold acceleration in the firing of paraventricular neurones during oxytocin release. J Endocrinol. 1973 Jun;57(3):477–493. doi: 10.1677/joe.0.0570477. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Physiology are provided here courtesy of The Physiological Society

RESOURCES