Skip to main content
NCBI home page
The Journal of General Physiology logoLink to The Journal of General Physiology
. 1982 Feb 1;79(2):211–232. doi: 10.1085/jgp.79.2.211

Functional significance of voltage-dependent conductances in Limulus ventral photoreceptors

PMCID: PMC2215499  PMID: 7057162

Abstract

The influence of voltage-dependent conductances on the receptor potential of Limulus ventral photoreceptors was investigated. During prolonged, bright illumination, the receptor potential consists of an initial transient phase followed by a smaller plateau phase. Generally, a spike appears on the rising edge of the transient phase, and often a dip occurs between the transient and plateau. Block of the rapidly inactivating outward current, iA, by 4-aminopyridine eliminates the dip under some conditions. Block of maintained outward current by internal tetraethylammonium increases the height of the plateau phase, but does not eliminate the dip. Block of the voltage-dependent Na+ and Ca2+ current by external Ni2+ eliminates the spike. The voltage-dependent Ca2+ conductance also influences the sensitivity of the photoreceptor to light as indicated by the following evidence: depolarizing voltage- clamp pulses reduce sensitivity to light. This reduction is blocked by removal of external Ca2+ or by block of inward Ca2+ current with Ni2+. The reduction of sensitivity depends on the amplitude of the pulse, reaching a maximum at or approximately +15 mV. The voltage dependence is consistent with the hypothesis that the desensitization results from passive Ca2+ entry through a voltage-dependent conductance.

Full Text

The Full Text of this article is available as a PDF (1.1 MB).

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. Measurement of calcium influx under voltage clamp in molluscan neurones using the metallochromic dye arsenazo III. J Physiol. 1979 Jan;286:61–82. doi: 10.1113/jphysiol.1979.sp012607. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Baker P. F., Hodgkin A. L., Ridgway E. B. Depolarization and calcium entry in squid giant axons. J Physiol. 1971 Nov;218(3):709–755. doi: 10.1113/jphysiol.1971.sp009641. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Baker P. F., Meves H., Ridgway E. B. Calcium entry in response to maintained depolarization of squid axons. J Physiol. 1973 Jun;231(3):527–548. doi: 10.1113/jphysiol.1973.sp010247. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Barlow R. B., Jr, Kaplan E. Limulus lateral eye: properties of receptor units in the unexcised eye. Science. 1971 Dec 3;174(4013):1027–1029. doi: 10.1126/science.174.4013.1027. [DOI] [PubMed] [Google Scholar]
  5. Bayer D. S., Barlow R. B., Jr Limulus ventral eye. Physiological properties of photoreceptor cells in an organ culture medium. J Gen Physiol. 1978 Oct;72(4):539–563. doi: 10.1085/jgp.72.4.539. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Borsellino A., Fuortes M. G., Smith T. G. Visual responses in Limulus. Cold Spring Harb Symp Quant Biol. 1965;30:429–443. doi: 10.1101/sqb.1965.030.01.042. [DOI] [PubMed] [Google Scholar]
  7. Brown H. M., Hagiwara S., Koike H., Meech R. M. Membrane properties of a barnacle photoreceptor examined by the voltage clamp technique. J Physiol. 1970 Jun;208(2):385–413. doi: 10.1113/jphysiol.1970.sp009127. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Brown J. E., Blinks J. R. Changes in intracellular free calcium concentration during illumination of invertebrate photoreceptors. Detection with aequorin. J Gen Physiol. 1974 Dec;64(6):643–665. doi: 10.1085/jgp.64.6.643. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Brown J. E., Brown P. K., Pinto L. H. Detection of light-induced changes of intracellular ionized calcium concentration in Limulus ventral photoreceptors using arsenazo III. J Physiol. 1977 May;267(2):299–320. doi: 10.1113/jphysiol.1977.sp011814. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. 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]
  11. Connor J. A., Stevens C. F. Voltage clamp studies of a transient outward membrane current in gastropod neural somata. J Physiol. 1971 Feb;213(1):21–30. doi: 10.1113/jphysiol.1971.sp009365. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Cornwall M. C., Gorman A. L. Contribution of calcium and potassium permeability changes to the off response of scallop hyperpolarizing photoreceptors. J Physiol. 1979 Jun;291:207–232. doi: 10.1113/jphysiol.1979.sp012808. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Dowling J. E. Discrete potentials in the dark-adapted ye of the crab Limulus. Nature. 1968 Jan 6;217(5123):28–31. doi: 10.1038/217028a0. [DOI] [PubMed] [Google Scholar]
  14. FUORTES M. G., HODGKIN A. L. CHANGES IN TIME SCALE AND SENSITIVITY IN THE OMMATIDIA OF LIMULUS. J Physiol. 1964 Aug;172:239–263. doi: 10.1113/jphysiol.1964.sp007415. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. FUORTES M. G., YEANDLE S. PROBABILITY OF OCCURRENCE OF DISCRETE POTENTIAL WAVES IN THE EYE OF LIMULUS. J Gen Physiol. 1964 Jan;47:443–463. doi: 10.1085/jgp.47.3.443. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Fein A., DeVoe R. D. Adaptation in the ventral eye of Limulus is functionally independent of the photochemical cycle, membrane potential, and membrane resistance. J Gen Physiol. 1973 Mar;61(3):273–289. doi: 10.1085/jgp.61.3.273. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Gorman A. L., Thomas M. V. Changes in the intracellular concentration of free calcium ions in a pace-maker neurone, measured with the metallochromic indicator dye arsenazo III. J Physiol. 1978 Feb;275:357–376. doi: 10.1113/jphysiol.1978.sp012194. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. HODGKIN A. L., HUXLEY A. F. Currents carried by sodium and potassium ions through the membrane of the giant axon of Loligo. J Physiol. 1952 Apr;116(4):449–472. doi: 10.1113/jphysiol.1952.sp004717. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hanani M., Shaw C. A potassium contribution to the response of the barnacle photoreceptor. J Physiol. 1977 Aug;270(1):151–163. doi: 10.1113/jphysiol.1977.sp011943. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Leonard R. J., Lisman J. E. Light modulates voltage-dependent potassium channels in limulus ventral photoreceptors. Science. 1981 Jun 12;212(4500):1273–1275. doi: 10.1126/science.212.4500.1273. [DOI] [PubMed] [Google Scholar]
  21. Lisman J. E., Brown J. E. Effects of intracellular injection of calcium buffers on light adaptation in Limulus ventral photoreceptors. J Gen Physiol. 1975 Oct;66(4):489–506. doi: 10.1085/jgp.66.4.489. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Lisman J. E., Brown J. E. Light-induced changes of sensitivity in Limulus ventral photoreceptors. J Gen Physiol. 1975 Oct;66(4):473–488. doi: 10.1085/jgp.66.4.473. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Lisman J. E., Brown J. E. The effects of intracellular iontophoretic injection of calcium and sodium ions on the light response of Limulus ventral photoreceptors. J Gen Physiol. 1972 Jun;59(6):701–719. doi: 10.1085/jgp.59.6.701. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Lisman J. E., Brown J. E. Two light-induced processes in the photoreceptor cells of Limulus ventral eye. J Gen Physiol. 1971 Nov;58(5):544–561. doi: 10.1085/jgp.58.5.544. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Lisman J. E. Effects of removing extracellular Ca2+ on excitation and adaptation in Limulus ventral photoreceptors. Biophys J. 1976 Nov;16(11):1331–1335. doi: 10.1016/S0006-3495(76)85777-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Lisman J. E., Fain G. L., O'Day P. M. Voltage-dependent conductances in Limulus ventral photoreceptors. J Gen Physiol. 1982 Feb;79(2):187–209. doi: 10.1085/jgp.79.2.187. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Lisman J. E., Strong J. A. The initiation of excitation and light adaptation in Limulus ventral photoreceptors. J Gen Physiol. 1979 Feb;73(2):219–243. doi: 10.1085/jgp.73.2.219. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. 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]
  29. 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]
  30. Pepose J. S., Lisman J. E. Voltage-sensitive potassium channels in Limulus ventral photoreceptors. J Gen Physiol. 1978 Jan;71(1):101–120. doi: 10.1085/jgp.71.1.101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Wulff V. J., Fahy J. L. Influence of calcium on the Limulus photoreceptor potential. Brain Res Bull. 1979 Nov-Dec;4(6):809–818. doi: 10.1016/0361-9230(79)90017-0. [DOI] [PubMed] [Google Scholar]

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

RESOURCES