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Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1977 Mar;74(3):1287–1290. doi: 10.1073/pnas.74.3.1287

Calcium modulation in brain extracellular microenvironment demonstrated with ion-selective micropipette.

C Nicholson, G T Bruggencate, R Steinberg, H Stöckle
PMCID: PMC430669  PMID: 265573

Abstract

Changes in extracellular Ca2+ concentration were directly measured in the rat cerebellum, using an ion-selective micropipette. Extracellular K+ was measured simultaneously with a second ion-selective micropipette. The potential reference barrels of the ion electrodes also provided fast field and slow potentials. During repetitive stimulation of the parallel fiber--Purkinje cell cerebellar circuit, extracellular Ca2+ fell to about 80% of base line concentration. During the spreading depression of Leão, extracellular Ca2+ fell to about 10% of base line; decreases of this magnitude also occurred during terminal anoxia. In all cases extracellular K+ increased substantially. These results show that extracellular Ca2+ is modulated during neuronal activity in the central nervous system and that under some conditions the Ca2+ change can be extreme. Given the well-established and antagonistic effects of reduce extracellular Ca2+ on axonal excitability and synaptic transmission, these results suggest that Ca2+ modulation in the brain cell microenvironment may be a significant parameter in the behavior of neuronal ensembles.

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Selected References

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

  1. Adey W. R. Evidence for cerebral membrane effects of calcium, derived from direct-current gradient, impedance, and intracellular records. Exp Neurol. 1971 Jan;30(1):78–102. doi: 10.1016/0014-4886(71)90224-x. [DOI] [PubMed] [Google Scholar]
  2. Bawin S. M., Adey W. R. Sensitivity of calcium binding in cerebral tissue to weak environmental electric fields oscillating at low frequency. Proc Natl Acad Sci U S A. 1976 Jun;73(6):1999–2003. doi: 10.1073/pnas.73.6.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. FIFKOVA E., BURES J., KOSHTOYANTS O. K., KRIVANEK J., WEISS T. Leao's spreading depression in the cerebellum of rat. Experientia. 1961 Dec 15;17:572–573. doi: 10.1007/BF02156433. [DOI] [PubMed] [Google Scholar]
  4. FRANKENHAEUSER B., HODGKIN A. L. The action of calcium on the electrical properties of squid axons. J Physiol. 1957 Jul 11;137(2):218–244. doi: 10.1113/jphysiol.1957.sp005808. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. GRAFSTEIN B. Mechanism of spreading cortical depression. J Neurophysiol. 1956 Mar;19(2):154–171. doi: 10.1152/jn.1956.19.2.154. [DOI] [PubMed] [Google Scholar]
  6. Heinemann U., Lux H. D. Undershoots following stimulus-induced rises of extracellular potassium concentration in cerebral cortex of cat. Brain Res. 1975 Jul 25;93(1):63–76. doi: 10.1016/0006-8993(75)90286-3. [DOI] [PubMed] [Google Scholar]
  7. Heyer C. B., Lux H. D. Control of the delayed outward potassium currents in bursting pace-maker neurones of the snail, Helix pomatia. J Physiol. 1976 Nov;262(2):349–382. doi: 10.1113/jphysiol.1976.sp011599. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Katz B., Miledi R. Further study of the role of calcium in synaptic transmission. J Physiol. 1970 May;207(3):789–801. doi: 10.1113/jphysiol.1970.sp009095. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Kraig R. P., Nicholson C. Sodium liquid ion exchanger microelectrode used to measure large extracellular sodium transients. Science. 1976 Nov 12;194(4266):725–726. doi: 10.1126/science.982036. [DOI] [PubMed] [Google Scholar]
  10. Kusano K., Miledi R., Stinnakre J. Postsynaptic entry of calcium induced by transmitter action. Proc R Soc Lond B Biol Sci. 1975 Apr 29;189(1094):49–56. doi: 10.1098/rspb.1975.0040. [DOI] [PubMed] [Google Scholar]
  11. Llinás R., Hess R. Tetrodotoxin-resistant dendritic spikes in avian Purkinje cells. Proc Natl Acad Sci U S A. 1976 Jul;73(7):2520–2523. doi: 10.1073/pnas.73.7.2520. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Llinás R., Nicholson C. Calcium role in depolarization-secretion coupling: an aequorin study in squid giant synapse. Proc Natl Acad Sci U S A. 1975 Jan;72(1):187–190. doi: 10.1073/pnas.72.1.187. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Lux H. D. Fast recording ion specific microelectrodes: their use in pharmacological studies in the CNS. Neuropharmacology. 1974 Jun;13(6):509–517. doi: 10.1016/0028-3908(74)90140-3. [DOI] [PubMed] [Google Scholar]
  14. Meech R. W., Standen N. B. Potassium activation in Helix aspersa neurones under voltage clamp: a component mediated by calcium influx. J Physiol. 1975 Jul;249(2):211–239. doi: 10.1113/jphysiol.1975.sp011012. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Mori S., Miller W. H., Tomita T. Müller cell function during spreading depression in frog retina. Proc Natl Acad Sci U S A. 1976 Apr;73(4):1351–1354. doi: 10.1073/pnas.73.4.1351. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Nicholson C., Kraig R. P. Chloride and potassium changes measured during spreading depression in catfish cerebellum. Brain Res. 1975 Oct 17;96(2):384–389. doi: 10.1016/0006-8993(75)90752-0. [DOI] [PubMed] [Google Scholar]
  17. Pedley T. A., Fisher R. S., Futamachi K. J., Prince D. A. Regulation of extracellular potassium concentration in epileptogenesis. Fed Proc. 1976 May 1;35(6):1254–1259. [PubMed] [Google Scholar]
  18. Prince D. A., Lux H. D., Neher E. Measurement of extracellular potassium activity in cat cortex. Brain Res. 1973 Feb 28;50(2):489–495. doi: 10.1016/0006-8993(73)90758-0. [DOI] [PubMed] [Google Scholar]
  19. VAN HARREVELD A. Compounds in brain extracts causing spreading depression of cerebral cortical activity and contraction of crustacean muscle. J Neurochem. 1959 Feb;3(4):300–315. doi: 10.1111/j.1471-4159.1959.tb12636.x. [DOI] [PubMed] [Google Scholar]
  20. Vyskocil F., Kritz N., Bures J. Potassium-selective microelectrodes used for measuring the extracellular brain potassium during spreading depression and anoxic depolarization in rats. Brain Res. 1972 Apr 14;39(1):255–259. doi: 10.1016/0006-8993(72)90802-5. [DOI] [PubMed] [Google Scholar]
  21. ten Bruggencate G., Lux H. D., Liebl L. Possible relationships between extracellular potassium activity and presynaptic inhibition in the spinal cord of the cat. Pflugers Arch. 1974;349(4):301–317. doi: 10.1007/BF00588416. [DOI] [PubMed] [Google Scholar]

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