Skip to main content
The Journal of General Physiology logoLink to The Journal of General Physiology
. 1988 Apr 1;91(4):515–527. doi: 10.1085/jgp.91.4.515

Light-induced oxygen consumption in Limulus ventral photoreceptors does not result from a rise in the intracellular sodium concentration

PMCID: PMC2216144  PMID: 2455766

Abstract

Illumination of Limulus ventral photoreceptors leads to an increase in the intracellular concentration of sodium, [Na+]i, and to an increase in the consumption of O2 (delta QO2). After a 1-s light flash, it takes approximately 480 s for [Na+]i to return to within 10% of its preillumination level, whereas delta QO2 takes approximately 90 s. Thus, the delta QO2 is complete long before [Na+]i has returned to its resting level. Pressure injection of Na+ into the cell in order to elevate [Na+]i to the same levels as attained by illumination causes a rise in [Na+]i that returns to baseline with the same time course as the light-induced rise in [Na+]i. However, the injection of Na+ does not lead to an increase of the consumption of O2. We conclude that activation of the Na pump by a rise in [Na+]i is not a factor involved in the light-induced activation of O2 consumption in these cells.

Full Text

The Full Text of this article is available as a PDF (809.2 KB).

Selected References

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

  1. Baker P. F., Connelly C. M. Some properties of the external activation site of the sodium pump in crab nerve. J Physiol. 1966 Jul;185(2):270–297. doi: 10.1113/jphysiol.1966.sp007987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Baker P. F., Willis J. S. Binding of the cardiac glycoside ouabain to intact cells. J Physiol. 1972 Jul;224(2):441–462. doi: 10.1113/jphysiol.1972.sp009904. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Brown H. M., Cornwall M. C. Ionic mechanism of a quasi-stable depolarization in barnacle photoreceptor following red light. J Physiol. 1975 Jul;248(3):579–593. doi: 10.1113/jphysiol.1975.sp010989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Brown J. E., Lisman J. E. An electrogenic sodium pump in Limulus ventral photoreceptor cells. J Gen Physiol. 1972 Jun;59(6):720–733. doi: 10.1085/jgp.59.6.720. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. CHANCE B., CONNELLY C. M. A method for the estimation of the increase in concentration of adenosine diphosphate in muscle sarcosomes following a contraction. Nature. 1957 Jun 15;179(4572):1235–1237. doi: 10.1038/1791235a0. [DOI] [PubMed] [Google Scholar]
  6. Calman B. G., Chamberlain S. C. Distinct lobes of Limulus ventral photoreceptors. II. Structure and ultrastructure. J Gen Physiol. 1982 Dec;80(6):839–862. doi: 10.1085/jgp.80.6.839. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Coles J. A., Orkand R. K. Changes in sodium activity during light stimulation in photoreceptors, glia and extracellular space in drone retina. J Physiol. 1985 May;362:415–435. doi: 10.1113/jphysiol.1985.sp015686. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Corson D. W., Fein A. Quantitative pressure injection of picoliter volumes into Limulus ventral photoreceptors. Biophys J. 1983 Dec;44(3):299–304. doi: 10.1016/S0006-3495(83)84303-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Fain G. L., Lisman J. E. Membrane conductances of photoreceptors. Prog Biophys Mol Biol. 1981;37(2):91–147. doi: 10.1016/0079-6107(82)90021-9. [DOI] [PubMed] [Google Scholar]
  10. Fein A., Tsacopoulos M. Activation of mitochondrial oxidative metabolism by calcium ions in Limulus ventral photoreceptor. Nature. 1988 Feb 4;331(6155):437–440. doi: 10.1038/331437a0. [DOI] [PubMed] [Google Scholar]
  11. Gadsby D. C., Cranefield P. F. Direct measurement of changes in sodium pump current in canine cardiac Purkinje fibers. Proc Natl Acad Sci U S A. 1979 Apr;76(4):1783–1787. doi: 10.1073/pnas.76.4.1783. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Harris S. I., Balaban R. S., Mandel L. J. Oxygen consumption and cellular ion transport: evidence for adenosine triphosphate to O2 ratio near 6 in intact cell. Science. 1980 Jun 6;208(4448):1148–1150. doi: 10.1126/science.6246581. [DOI] [PubMed] [Google Scholar]
  13. Koike H., Brown H. M., Hagiwara S. Hyperpolarization of a barnacle photoreceptor membrane following illumination. J Gen Physiol. 1971 Jun;57(6):723–737. doi: 10.1085/jgp.57.6.723. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Levy S., Fein A. Relationship between light sensitivity and intracellular free Ca concentration in Limulus ventral photoreceptors. A quantitative study using Ca-selective microelectrodes. J Gen Physiol. 1985 Jun;85(6):805–841. doi: 10.1085/jgp.85.6.805. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Millecchia R., Mauro A. The ventral photoreceptor cells of Limulus. II. The basic photoresponse. J Gen Physiol. 1969 Sep;54(3):310–330. doi: 10.1085/jgp.54.3.310. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Munoz J. L., Coles J. A. Quartz micropipettes for intracellular voltage microelectrodes and ion-selective microelectrodes. J Neurosci Methods. 1987 Nov;22(1):57–64. doi: 10.1016/0165-0270(87)90090-2. [DOI] [PubMed] [Google Scholar]
  17. Munoz J. L., Deyhimi F., Coles J. A. Silanization of glass in the making of ion-sensitive microelectrodes. J Neurosci Methods. 1983 Jul;8(3):231–247. doi: 10.1016/0165-0270(83)90037-7. [DOI] [PubMed] [Google Scholar]
  18. Ritchie J. M. Energetic aspects of nerve conduction: the relationships between heat production, electrical activity and metabolism. Prog Biophys Mol Biol. 1973;26:147–187. doi: 10.1016/0079-6107(73)90019-9. [DOI] [PubMed] [Google Scholar]
  19. Sheu S. S., Fozzard H. A. Transmembrane Na+ and Ca2+ electrochemical gradients in cardiac muscle and their relationship to force development. J Gen Physiol. 1982 Sep;80(3):325–351. doi: 10.1085/jgp.80.3.325. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Stern J., Chinn K., Bacigalupo J., Lisman J. Distinct lobes of Limulus ventral photoreceptors. I. Functional and anatomical properties of lobes revealed by removal of glial cells. J Gen Physiol. 1982 Dec;80(6):825–837. doi: 10.1085/jgp.80.6.825. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Taylor P. S., Thomas R. C. The effect of leakage on micro-electrode measurements of intracellular sodium activity in crab muscle fibres. J Physiol. 1984 Jul;352:539–550. doi: 10.1113/jphysiol.1984.sp015309. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Thomas R. C. Intracellular sodium activity and the sodium pump in snail neurones. J Physiol. 1972 Jan;220(1):55–71. doi: 10.1113/jphysiol.1972.sp009694. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Thomas R. C. Membrane current and intracellular sodium changes in a snail neurone during extrusion of injected sodium. J Physiol. 1969 Apr;201(2):495–514. doi: 10.1113/jphysiol.1969.sp008769. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Tsacopoulos M., Orkand R. K., Coles J. A., Levy S., Poitry S. Oxygen uptake occurs faster than sodium pumping in bee retina after a light flash. Nature. 1983 Feb 17;301(5901):604–606. doi: 10.1038/301604a0. [DOI] [PubMed] [Google Scholar]
  25. Tsacopoulos M., Poitry S., Borsellino A. Diffusion and consumption of oxygen in the superfused retina of the drone (Apis mellifera) in darkness. J Gen Physiol. 1981 Jun;77(6):601–628. doi: 10.1085/jgp.77.6.601. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Tsacopoulos M., Poitry S. Kinetics of oxygen consumption after a single flash of light in photoreceptors of the drone (Apis mellifera). J Gen Physiol. 1982 Jul;80(1):19–55. doi: 10.1085/jgp.80.1.19. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Vaughan-Jones R. D. The effect of lowering external sodium on the intracellular sodium activity of crab muscle fibres. J Physiol. 1977 Jan;264(1):239–265. doi: 10.1113/jphysiol.1977.sp011666. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Journal of General Physiology are provided here courtesy of The Rockefeller University Press

RESOURCES