Skip to main content
PMC home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1994 Nov 15;481(Pt 1):1–5. doi: 10.1113/jphysiol.1994.sp020413

Evidence that glial cells modulate extracellular pH transients induced by neuronal activity in the leech central nervous system.

C R Rose 1, J W Deitmer 1
PMCID: PMC1155860  PMID: 7853232

Abstract

1. The role of the giant neuropile glial cells in the buffering of activity-related extracellular pH changes was studied in segmental ganglia of the leech Hirudo medicinalis L. using pH-sensitive microelectrodes and a slow, two-electrode voltage-clamp system. Neuronal activity was induced by electrical stimulation of a ganglionic side nerve (20 Hz, 1 min). 2. In CO2-HCO3(-)-buffered saline the glial cells were depolarized by 6.5 +/- 2.3 mV and alkalinized by 0.024 +/- 0.006 pH units (mean +/- SD) during the stimulation. The stimulation induced an acidification of 0.032 +/- 0.006 pH units in the extracellular spaces (ECS). 3. Voltage clamping the glial cells suppressed the stimulus-induced glial depolarization and turned the intraglial alkalinization into an acidification of 0.045 +/- 0.021 pH units (n = 6) that closely resembled the acidification observed in the presence of the anion transport blocker DIDS (4,4'-diisothiocyanatostilbene-2,2'-disulphonic acid, 0.5 mM), and in CO2-HCO(3-)-free saline. 4. Voltage clamping the glial cell resulted in the appearance of a distinct stimulus-induced extracellular alkalinization of 0.024 +/- 0.013 pH units at the onset of the stimulation, as also observed during DIDS application and in the absence of CO2-HCO3-. 5. The results suggest that glial uptake of bicarbonate is mediated by depolarization-induced activation of the electrogenic Na(+)-HCO3- cotransport, which suppresses the profound alkalinization of the ECS during neuronal activity. This is the first direct evidence the glial cells actively modulate extracellular pH changes in a voltage-dependent manner.

Full text

PDF
3

Selected References

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

  1. Ahmed Z., Connor J. A. Intracellular pH changes induced by calcium influx during electrical activity in molluscan neurons. J Gen Physiol. 1980 Apr;75(4):403–426. doi: 10.1085/jgp.75.4.403. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Aram J. A., Lodge D. Epileptiform activity induced by alkalosis in rat neocortical slices: block by antagonists of N-methyl-D-aspartate. Neurosci Lett. 1987 Dec 29;83(3):345–350. doi: 10.1016/0304-3940(87)90112-1. [DOI] [PubMed] [Google Scholar]
  3. Balestrino M., Somjen G. G. Concentration of carbon dioxide, interstitial pH and synaptic transmission in hippocampal formation of the rat. J Physiol. 1988 Feb;396:247–266. doi: 10.1113/jphysiol.1988.sp016961. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Chesler M., Kaila K. Modulation of pH by neuronal activity. Trends Neurosci. 1992 Oct;15(10):396–402. doi: 10.1016/0166-2236(92)90191-a. [DOI] [PubMed] [Google Scholar]
  5. Chesler M., Kraig R. P. Intracellular pH transients of mammalian astrocytes. J Neurosci. 1989 Jun;9(6):2011–2019. doi: 10.1523/JNEUROSCI.09-06-02011.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Chesler M. The regulation and modulation of pH in the nervous system. Prog Neurobiol. 1990;34(5):401–427. doi: 10.1016/0301-0082(90)90034-e. [DOI] [PubMed] [Google Scholar]
  7. Coles J. A. Functions of glial cells in the retina of the honeybee drone. Glia. 1989;2(1):1–9. doi: 10.1002/glia.440020102. [DOI] [PubMed] [Google Scholar]
  8. Deitmer J. W. Electrogenic sodium-dependent bicarbonate secretion by glial cells of the leech central nervous system. J Gen Physiol. 1991 Sep;98(3):637–655. doi: 10.1085/jgp.98.3.637. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Deitmer J. W. Evidence for glial control of extracellular pH in the leech central nervous system. Glia. 1992;5(1):43–47. doi: 10.1002/glia.440050107. [DOI] [PubMed] [Google Scholar]
  10. Deitmer J. W., Schlue W. R. An inwardly directed electrogenic sodium-bicarbonate co-transport in leech glial cells. J Physiol. 1989 Apr;411:179–194. doi: 10.1113/jphysiol.1989.sp017567. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Deitmer J. W., Szatkowski M. Membrane potential dependence of intracellular pH regulation by identified glial cells in the leech central nervous system. J Physiol. 1990 Feb;421:617–631. doi: 10.1113/jphysiol.1990.sp017965. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Jarolimek W., Misgeld U., Lux H. D. Activity dependent alkaline and acid transients in guinea pig hippocampal slices. Brain Res. 1989 Dec 29;505(2):225–232. doi: 10.1016/0006-8993(89)91447-9. [DOI] [PubMed] [Google Scholar]
  13. Munsch T., Deitmer J. W. Sodium-bicarbonate cotransport current in identified leech glial cells. J Physiol. 1994 Jan 1;474(1):43–53. doi: 10.1113/jphysiol.1994.sp020001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Newman E. A., Astion M. L. Localization and stoichiometry of electrogenic sodium bicarbonate cotransport in retinal glial cells. Glia. 1991;4(4):424–428. doi: 10.1002/glia.440040411. [DOI] [PubMed] [Google Scholar]
  15. Ransom B. R., Carlini W. G., Connors B. W. Brain extracellular space: developmental studies in rat optic nerve. Ann N Y Acad Sci. 1986;481:87–105. doi: 10.1111/j.1749-6632.1986.tb27141.x. [DOI] [PubMed] [Google Scholar]
  16. Ransom B. R. Glial modulation of neural excitability mediated by extracellular pH: a hypothesis. Prog Brain Res. 1992;94:37–46. doi: 10.1016/s0079-6123(08)61737-9. [DOI] [PubMed] [Google Scholar]
  17. Syková E., Jendelová P., Simonová Z., Chvátal A. K+ and pH homeostasis in the developing rat spinal cord is impaired by early postnatal X-irradiation. Brain Res. 1992 Oct 23;594(1):19–30. doi: 10.1016/0006-8993(92)91025-a. [DOI] [PubMed] [Google Scholar]
  18. Voipio J., Kaila K. Interstitial PCO2 and pH in rat hippocampal slices measured by means of a novel fast CO2/H(+)-sensitive microelectrode based on a PVC-gelled membrane. Pflugers Arch. 1993 May;423(3-4):193–201. doi: 10.1007/BF00374394. [DOI] [PubMed] [Google Scholar]

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

RESOURCES