Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Stimulus-induced changes in extracellular Na+ and Cl concentration in relation to changes in the size of the extracellular space

  • 117 Accesses

  • 154 Citations

Summary

Extracellular Na+- and Cl-concentrations ([Na+]o, [Cl]o) were recorded with ion-selective microelectrodes during repetitive stimulation and stimulus-induced self-sustained neuronal afterdischarges (SAD) in the sensorimotor cortex of cats. In all cortical layers [Na+]o initially decreased by 4–7 mM. In depths of more than 600 μm below the cortical surface such decreases usually turned into increases of 2–6 mM during the course of the SADs, whereas in superficial layers [Na+]o never rose above its resting level. [Cl]o always showed an increase in the course of the SADs often preceded by an initial small decrease. The average increase at a depth of 1,000 μm was about 7 mM. [Cl]o reached peak values at about the end of the ictal period, whereas [Na+]o reached its maximum shortly after the end of the SAD, at times when [K+]o was still elevated above the baseline concentration.

These data indicate that the extracellular osmolarity can increase during SAD by up to 30 mM. Such an increase in osmolarity can be explained by an increase in the number of intracellular particles, caused by cleavage of larger molecules during enhanced metabolism. This could lead to cell-swelling due to passive water influx from the extracellular space (ES). However, the resulting reduction of the size of the ES is calculated to be less than 10% for an increase in intracellular osmolarity by 30 mOsm. This value is too small as compared to previously measured ES-reductions under similar conditions (i.e., 30% reduction at 1,000 μm; Dietzel et al. 1980). Reductions of the size of the ES that accompany the observed changes in the ionic environment, are quantitatively explained on the basis of the extended glial buffering mechanism described in the preceding paper.

This is a preview of subscription content, log in to check access.

References

  1. Ames A, Sakanoue M, Endo S (1964) Na, K, Ca, Mg, and Cl concentrations in choroid plexus fluid and cisternal fluid compared with plasma ultrafiltrate. J Neurophysiol 27: 672–681.

  2. Bührle Ph, Sonnhof U (1981) Intracellular activities of K+, Na+, Ca2+, and Cl in motoneurons and glial cells of the frog spinal cord. Pflügers Arch [Suppl] 389: R24.

  3. Crank J (1956) The mathematics of diffusion. Oxford University Press, London.

  4. Deisz RA, Lux HD (1978) Intracellular chloride concentration and postsynaptic inhibition in crayfish stretch receptor neurons. Arzneim Forsch 28: 870–871.

  5. Dietzel I, Heinemann U, Hofmeier G, Lux HD (1980) Transient changes in the size of the extracellular space in the sensorimotor cortex of cats in relation to stimulus induced changes in potassium concentration. Exp Brain Res 40: 432–439.

  6. Dietzel I, Heinemann U, Hofmeier G, Lux HD (1982) Changes in the extracellular volume in the cerebral cortex of cats in relation to stimulus induced epileptiform afterdischarges. In: Klee MR, Lux HD, Speckmann EJ (eds) Pharmacology and physiology of epileptogenic phenomena. Raven Press, New York (in press).

  7. Freygang WH, Landau WM (1955) Some relations between resistivity and electrical activity in the cerebral cortex of the cat. J Cell Physiol 45: 377–392.

  8. Gardner-Medwin AR (1980) Membrane transport and solute migration affecting the brain cell microenvironment. In: Nicholson C (ed) Dynamics of the brain cell microenvironment. MIT Press, Cambridge (Neurosci Res Program Bull, vol 18, p 220).

  9. Gardner-Medwin AR, Coles JA, Tsacopoulos M (1981) Clearance of extracellular potassium: Evidence for spatial buffering by glial cells in the retina of the drone. Brain Res 209: 452–457.

  10. Gutnick MJ, Heinemann U, Lux HD (1979) Stimulus-induced and seizure-related changes in extracellular potassium concentration in cat thalamus (VPL). Electroencephalogr Clin Neurophysiol 47: 329–344.

  11. Hand P, Greenberg J, Goochee C, Sylvestro A, Weller L, Reivich M (1979) A normal and developmentally altered cortical column: A laminar analysis of local glucose utilization with natural stimulation of a single receptor organ. Acta Neurol Scand [Suppl 72] 60: 46–47.

  12. Hansen AJ, Olsen CE (1980) Brain extracellular space during spreading depression and ischemia. Acta Physiol Scand 108: 355–365.

  13. Harreveld A van, Schadé JP (1959) Chloride movements in cerebral cortex after circulatory arrest and during spreading depression. J Cell Comp Physiol 54: 65–77.

  14. Harreveld A van, Khattab FI (1967) Changes in cortical extracellular space during spreading depression investigated with the electron microscope. J Neurophysiol 30: 911–929.

  15. Heinemann U, Konnerth A, Lux HD (1981) Stimulation induced changes in extracellular free calcium in normal and chronic alumina cream foci of cats. Brain Res 213: 246–250.

  16. Heinemann U, Lux HD (1975) Undershoots following stimulus induced rises of extracellular potassium concentration in cerebral cortex of cat. Brain Res 93: 63–76.

  17. Heinemann U, Lux HD (1977) Ceiling of stimulus induced rises in extracellular potassium concentration in the cerebral cortex of cats. Brain Res 120: 231–249.

  18. Heinemann U, Lux HD, Gutnick MJ (1977) Extracellular free calcium and potassium during paroxysmal activity in cerebral cortex of the cat. Exp Brain Res 27: 237–243.

  19. House CR (1974) Water transport in cells and tissues. Arnold, London.

  20. House CR (1980) cited by Nicholson C (1980).

  21. Howse DC, Caronna JJ, Duffy TE, Plum F (1974) Cerebral energy metabolism, pH, and blood flow during seizures in the cat. Am J Physiol 227: 1444–1450.

  22. Janus J, Lehmenkühler A (1981) Changes of extracellular chloride, sodium and calcium activities during stimulus-induced DC-potential shifts in the CNS. Pflügers Arch [Suppl] 389: R18.

  23. King LJ, Carl JL, Lao L (1973) Carbohydrate metabolism in brain during convulsions and its modification by phenobarbitone. J Neurochem 20: 477–485.

  24. Kraig RP, Nicholson C (1978) Extracellular ionic variations during spreading depression. Neuroscience 3: 1045–1059.

  25. Lehmenkühler A, Zidek W, Caspers H (1982) Changes of extracellular Na+, and Cl activity in the brain cortex during seizure discharges. In: Klee MR, Lux HD, Speckmann EJ (eds) Pharmacology and physiology of epileptogenic phenomena. Raven Press, New York (in press).

  26. Lux HD (1974) Kinetics of extracellular potassium. Relation to epileptogenesis. Epilepsia 15: 375–393.

  27. Lux HD, Neher E (1973) The equilibration time course of [K+]o in cat cortex. Exp Brain Res 17: 190–205.

  28. Moody W, Futamachi KJ, Prince DA (1974) Extracellular potassium activity during epileptogenesis. Exp Neurol 42: 248–263.

  29. Neher E, Lux HD (1973) Rapid changes of potassium concentration at the outer surface of exposed single neurons during membrane current flow. J Gen Physiol 61: 385–399.

  30. Nicholson C (1980) Dynamics of the brain cell microenvironment. MIT Press, Cambridge (Neurosci Res Program Bull, vol. 18).

  31. Orkand RK, Nicholls JG, Kuffler SW (1966) Effect of nerve impulses on the membrane potential of glial cells in the central nervous system of amphibia. J Neurophysiol 29: 788–806.

  32. Phillips JM, Nicholson C (1978) Tetra-alkyl ammonium ions as probes of brain cell microenvironment. Soc Neurosci Abstr 4: 236.

  33. Phillips JM, Nicholson C (1979) Anion permeability in spreading depression investigated with ion-sensitive microelectrodes. Brain Res 173: 567–571.

  34. Siesjö BK (1978) Brain energy metabolism. Wiley, New York.

  35. Steiner RA, Oehme M, Ammann D, Simon W (1979) Neutral carrier sodium ion-selective microelectrode for intracellular studies. Anal Chem 51: 351–353.

  36. Somjen GG (1975) Electrophysiology of neuroglia. Ann Rev Physiol 37: 163–190.

  37. Sypert GW, Ward AA, Jr (1974) Changes in extracellular potassium activity during neocortical propagated seizures. Exp Neurol 45: 19–41.

  38. Trachtenberg MC, Pollen DA (1970) Neuroglia: Biophysical properties and physiologic function. Science 167: 1248–1253.

Download references

Author information

Correspondence to I. Dietzel.

Additional information

Supported by the Deutsche Forschungsgemeinschaft, grant no. He 1128/2-2

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Dietzel, I., Heinemann, U., Hofmeier, G. et al. Stimulus-induced changes in extracellular Na+ and Cl concentration in relation to changes in the size of the extracellular space. Exp Brain Res 46, 73–84 (1982). https://doi.org/10.1007/BF00238100

Download citation

Key words

  • Extracellular space
  • Na+ and Cl concentration
  • Effects of metabolism on osmolarity
  • Epilepsy
  • Cerebral cortex