Skip to main content
NCBI home page
The Journal of General Physiology logoLink to The Journal of General Physiology
. 1982 Jul 1;80(1):19–55. doi: 10.1085/jgp.80.1.19

Kinetics of oxygen consumption after a single flash of light in photoreceptors of the drone (Apis mellifera)

PMCID: PMC2228666  PMID: 6288837

Abstract

The time course of the rate of oxygen consumption (QO2) after a single flash of light has been measured in 300-micrometers slices of drone retina at 22 degrees C. To measure delta QO2(t), the change in QO2 from its level in darkness, the transients of the partial pressure of O2 (PO2) were recorded with O2 microelectrodes simultaneously in two sites in the slice and delta QO2 was calculated by a computer using Fourier transforms. After a 40-ms flash of intense light, delta QO2, reached a peak of 40 microliters O2/g.min and then declined exponentially to the baseline with a time constant tau 1 = 4.96 +/- 0.49 s (SD, n = 10). The rising phase was characterized by a time constant tau 2 = 1.90 +/- 0.35 s (SD, n = 10). The peak amplitude of delta QO2 increased linearly with the log of the light intensity. Replacement of Na+ by choline, known to decrease greatly the light-induced transmembrane current, caused a 63% decrease of delta QO2. With these changes, however, the kinetics of delta QO2 (t) were unchanged. This suggest that the recovery phase is rate-limited by a single reaction with apparent first-order kinetics. Evidence is provided that suggests that this reaction may be the working of the sodium pump. Exposure of the retina to high concentrations of ouabain or strophanthidin (inhibitors of the sodium pump) reduced the peak amplitude of delta QO2 by approximately 80% and increased tau 1. The increase of tau 1 was an exponential function of the time of exposure to the cardioactive steroids. Hence, it seems likely that the greatest part of delta QO2 is used for the working of the pump, whose activity is the mechanism underlying the rate constant of the descending limb of delta QO2 (t).

Full Text

The Full Text of this article is available as a PDF (2.0 MB).

Selected References

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

  1. Abeles A. L. Structure-activity relationships of several cardiotonic steroids with respect to inhibition of ion transport in frog muscle. J Gen Physiol. 1969 Aug;54(2):268–284. doi: 10.1085/jgp.54.2.268. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. 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]
  3. Baumann F., Mauro A. Effect of hypoxia on the change in membrane conductance evoked by illumination in arthropod photoreceptors. Nat New Biol. 1973 Aug 1;244(135):146–148. doi: 10.1038/newbio244146b0. [DOI] [PubMed] [Google Scholar]
  4. Baumann F. Slow and spike potentials recorded from retinula cells of the honeybee drone in response to light. J Gen Physiol. 1968 Dec;52(6):855–875. doi: 10.1085/jgp.52.6.855. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bertrand D., Fuortes G., Muri R. Pigment transformation and electrical responses in retinula cells of drone, Apis mellifera male. J Physiol. 1979 Nov;296:431–441. doi: 10.1113/jphysiol.1979.sp013014. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. 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]
  7. Brown J. E., Mote M. I. Ionic dependence of reversal voltage of the light response in Limulus ventral photoreceptors. J Gen Physiol. 1974 Mar;63(3):337–350. doi: 10.1085/jgp.63.3.337. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. 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]
  9. Coles J. A., Tsacopoulos M. Ionic and possible metabolic interactions between sensory neurones and glial cells in the retina of the honeybee drone. J Exp Biol. 1981 Dec;95:75–92. doi: 10.1242/jeb.95.1.75. [DOI] [PubMed] [Google Scholar]
  10. Coles J. A., Tsacopoulos M. Potassium activity in photoreceptors, glial cells and extracellular space in the drone retina: changes during photostimulation. J Physiol. 1979 May;290(2):525–549. doi: 10.1113/jphysiol.1979.sp012788. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Deitmer J. W., Ellis D. The intracellular sodium activity of cardiac Purkinje fibres during inhibition and re-activation of the Na-K pump. J Physiol. 1978 Nov;284:241–259. doi: 10.1113/jphysiol.1978.sp012539. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Erlij D., Elizalde A. Rapidly reversible inhibition of frog muscle sodium pump caused by cardiotonic steroids with modified lactone rings. Biochim Biophys Acta. 1974 Apr 12;345(1):49–54. doi: 10.1016/0005-2736(74)90244-2. [DOI] [PubMed] [Google Scholar]
  13. Fulpius B., Baumann F. Effects of sodium, potassium, and calcium ions on slow and spike potentials in single photoreceptor cells. J Gen Physiol. 1969 May;53(5):541–561. doi: 10.1085/jgp.53.5.541. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. 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]
  15. Gardner-Medwin A. R., Coles J. A., Tsacopoulos M. Clearance of extracellular potassium: evidence for spatial buffering by glial cells in the retina of the drone. Brain Res. 1981 Mar 30;209(2):452–457. doi: 10.1016/0006-8993(81)90169-4. [DOI] [PubMed] [Google Scholar]
  16. Glynn I. M., Karlish S. J. The sodium pump. Annu Rev Physiol. 1975;37:13–55. doi: 10.1146/annurev.ph.37.030175.000305. [DOI] [PubMed] [Google Scholar]
  17. 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]
  18. Hill D. K. Oxygen tension and the respiration of resting frog's muscle. J Physiol. 1948 Sep 30;107(4):479–495. doi: 10.1113/jphysiol.1948.sp004293. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Liebman P. A., Pugh E. N., Jr The control of phosphodiesterase in rod disk membranes: kinetics, possible mechanisms and significance for vision. Vision Res. 1979;19(4):375–380. doi: 10.1016/0042-6989(79)90097-x. [DOI] [PubMed] [Google Scholar]
  20. Mahler M. Diffusion and consumption of oxygen in the resting frog sartorius muscle. J Gen Physiol. 1978 May;71(5):533–557. doi: 10.1085/jgp.71.5.533. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Mahler M. Kinetics of oxygen consumption after a single isometric tetanus of frog sartorius muscle at 20 degrees C. J Gen Physiol. 1978 May;71(5):559–580. doi: 10.1085/jgp.71.5.559. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Mahler M. The relationship between initial creatine phosphate breakdown and recovery oxygen consumption for a single isometric tetanus of the frog sartorius muscle at 20 degrees C. J Gen Physiol. 1979 Feb;73(2):159–174. doi: 10.1085/jgp.73.2.159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Millecchia R., Mauro A. The ventral photoreceptor cells of Limulus. 3. A voltage-clamp study. J Gen Physiol. 1969 Sep;54(3):331–351. doi: 10.1085/jgp.54.3.331. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Nishiki K., Erecińska M., Wilson D. F. Effect of Amytal on metabolism of perfused rat heart: relationship between glycolysis and oxidative phosphorylation. Am J Physiol. 1979 Nov;237(5):C221–C230. doi: 10.1152/ajpcell.1979.237.5.C221. [DOI] [PubMed] [Google Scholar]
  25. Perrelet A. The fine structure of the retina of the honey bee drone. An electron microscopical study. Z Zellforsch Mikrosk Anat. 1970;108(4):530–562. doi: 10.1007/BF00339658. [DOI] [PubMed] [Google Scholar]
  26. Rang H. P., Ritchie J. M. The dependence on external cations of the oxygen consumption of mammalian non-myelinated fibres at rest and during activity. J Physiol. 1968 May;196(1):163–181. doi: 10.1113/jphysiol.1968.sp008501. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. 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]
  28. SKOU J. C. ENZYMATIC BASIS FOR ACTIVE TRANSPORT OF NA+ AND K+ ACROSS CELL MEMBRANE. Physiol Rev. 1965 Jul;45:596–617. doi: 10.1152/physrev.1965.45.3.596. [DOI] [PubMed] [Google Scholar]
  29. Schwartz A., Lindenmayer G. E., Allen J. C. The sodium-potassium adenosine triphosphatase: pharmacological, physiological and biochemical aspects. Pharmacol Rev. 1975 Mar;27(01):3–134. [PubMed] [Google Scholar]
  30. Sweadner K. J. Two molecular forms of (Na+ + K+)-stimulated ATPase in brain. Separation, and difference in affinity for strophanthidin. J Biol Chem. 1979 Jul 10;254(13):6060–6067. [PubMed] [Google Scholar]
  31. Thomas R. C. Electrogenic sodium pump in nerve and muscle cells. Physiol Rev. 1972 Jul;52(3):563–594. doi: 10.1152/physrev.1972.52.3.563. [DOI] [PubMed] [Google Scholar]
  32. 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]
  33. Tsacopoulos M., Lehmenkühler A. A double-barrelled Pt-microelectrode for simultaneous measurement of PO2 and bioelectrical activity in excitable tissues. Experientia. 1977 Oct 15;33(10):1337–1338. doi: 10.1007/BF01920167. [DOI] [PubMed] [Google Scholar]
  34. 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]

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

RESOURCES