Skip to main content
NCBI home page
The Journal of General Physiology logoLink to The Journal of General Physiology
. 1986 Mar 1;87(3):391–405. doi: 10.1085/jgp.87.3.391

Spatial properties of the prolonged depolarizing afterpotential in barnacle photoreceptors. I. The induction process

PMCID: PMC2217611  PMID: 3958692

Abstract

In invertebrate photoreceptors, when the light stimulus results in substantial net transfer of the visual pigment from the rhodopsin (R) to the metarhodopsin (M) state, the ordinary late receptor potential (LRP) is followed by a prolonged depolarizing afterpotential (PDA). The dependence of the amplitude of the PDA on the amount of pigment conversion is strongly supralinear, and the PDA duration also depends on this amount. These observations indicate an interaction among the elements of the PDA induction process and also make possible a test of the range of this interaction. The test consists of a comparison of the PDA after localized pigment conversion, obtained by strong spot illumination, to that after weaker diffuse illumination converting a comparable total amount of pigment. The experiment was performed on the barnacle lateral eye. The effective spot size was measured by the early receptor potential (ERP), in seawater saturated with CO2, which considerably reduced the electrical coupling between the photoreceptors. The ERP was also used to determine whether there is diffusion of R molecules into the illuminated spot. The spot illumination induced a PDA with small amplitude and long duration, while no detectable PDA was induced by the diffuse light. This indicates that the range of the PDA interaction is much smaller than the entire cell. In addition, the ERP results showed that there was no detectable diffusion of R molecules into the illuminated spot area over 30 min. This measurement, with a calculated correction for the microvillar geometry of the photoreceptor, enabled us to put an upper limit on the diffusion coefficient of the pigment molecules in the inact, unfixed barnacle photoreceptor of D less than 6 X 10(-9) cm2 s-1.

Full Text

The Full Text of this article is available as a PDF (960.7 KB).

Selected References

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

  1. Blumenfeld A., Erusalimsky J., Heichal O., Selinger Z., Minke B. Light-activated guanosinetriphosphatase in Musca eye membranes resembles the prolonged depolarizing afterpotential in photoreceptor cells. Proc Natl Acad Sci U S A. 1985 Oct;82(20):7116–7120. doi: 10.1073/pnas.82.20.7116. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. 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]
  3. 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]
  4. Giaume C., Spira M. E., Korn H. Uncoupling of invertebrate electrotonic synapses by carbon dioxide. Neurosci Lett. 1980 Apr;17(1-2):197–202. doi: 10.1016/0304-3940(80)90084-1. [DOI] [PubMed] [Google Scholar]
  5. Goldsmith T. H., Wehner R. Restrictions on rotational and translational diffusion of pigment in the membranes of a rhabdomeric photoreceptor. J Gen Physiol. 1977 Oct;70(4):453–490. doi: 10.1085/jgp.70.4.453. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Hamdorf K., Razmjoo S. The prolonged depolarizing afterpotential and its contribution to the understanding of photoreceptor function. Biophys Struct Mech. 1977 Jun 29;3(2):163–170. doi: 10.1007/BF00535813. [DOI] [PubMed] [Google Scholar]
  7. Hillman P., Hochstein S., Minke B. Nonlocal interactions in the photoreceptor transduction process. J Gen Physiol. 1976 Aug;68(2):227–245. doi: 10.1085/jgp.68.2.227. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Hillman P., Hochstein S., Minke B. Transduction in invertebrate photoreceptors: role of pigment bistability. Physiol Rev. 1983 Apr;63(2):668–772. doi: 10.1152/physrev.1983.63.2.668. [DOI] [PubMed] [Google Scholar]
  9. Hochstein S., Minke B., Hillman P. Antagonistic components of the late receptor potential in the barnacle photoreceptor arising from different stages of the pigment process. J Gen Physiol. 1973 Jul;62(1):105–128. doi: 10.1085/jgp.62.1.105. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. 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]
  11. Liebman P. A., Entine G. Lateral diffusion of visual pigment in photorecptor disk membranes. Science. 1974 Aug 2;185(4149):457–459. doi: 10.1126/science.185.4149.457. [DOI] [PubMed] [Google Scholar]
  12. Liebman P. A., Pugh E. N., Jr ATP mediates rapid reversal of cyclic GMP phosphodiesterase activation in visual receptor membranes. Nature. 1980 Oct 23;287(5784):734–736. doi: 10.1038/287734a0. [DOI] [PubMed] [Google Scholar]
  13. Minke B., Hochstein S., Hillman P. Derivation of a quantitative kinetic model for a visual pigment from observations of early receptor potential. Biophys J. 1974 Jun;14(6):490–512. doi: 10.1016/S0006-3495(74)85929-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Minke B., Hochstein S., Hillman P. Early receptor potential evidence for the existence of two thermally stable states in the barnacle visual pigment. J Gen Physiol. 1973 Jul;62(1):87–104. doi: 10.1085/jgp.62.1.87. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Minke B., Kirschfeld K. Microspectrophotometric evidence for two photointerconvertible states of visual pigment in the barnacle lateral eye. J Gen Physiol. 1978 Jan;71(1):37–45. doi: 10.1085/jgp.71.1.37. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Minke B., Wu C., Pak W. L. Induction of photoreceptor voltage noise in the dark in Drosophila mutant. Nature. 1975 Nov 6;258(5530):84–87. doi: 10.1038/258084a0. [DOI] [PubMed] [Google Scholar]
  17. Poo M., Cone R. A. Lateral diffusion of rhodopsin in the photoreceptor membrane. Nature. 1974 Feb 15;247(5441):438–441. doi: 10.1038/247438a0. [DOI] [PubMed] [Google Scholar]
  18. Saibil H. R., Michel-Villaz M. Squid rhodopsin and GTP-binding protein crossreact with vertebrate photoreceptor enzymes. Proc Natl Acad Sci U S A. 1984 Aug;81(16):5111–5115. doi: 10.1073/pnas.81.16.5111. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Shaw S. R. Decremental conduction of the visual signal in barnacle lateral eye. J Physiol. 1972 Jan;220(1):145–175. doi: 10.1113/jphysiol.1972.sp009699. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Sitaramayya A., Liebman P. A. Mechanism of ATP quench of phosphodiesterase activation in rod disc membranes. J Biol Chem. 1983 Jan 25;258(2):1205–1209. [PubMed] [Google Scholar]
  21. Sitaramayya A., Liebman P. A. Phosphorylation of rhodopsin and quenching of cyclic GMP phosphodiesterase activation by ATP at weak bleaches. J Biol Chem. 1983 Oct 25;258(20):12106–12109. [PubMed] [Google Scholar]
  22. Wey C. L., Cone R. A., Edidin M. A. Lateral diffusion of rhodopsin in photoreceptor cells measured by fluorescence photobleaching and recovery. Biophys J. 1981 Feb;33(2):225–232. doi: 10.1016/S0006-3495(81)84883-7. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES