Skip to main content
NCBI home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1974 Feb;236(3):575–591. doi: 10.1113/jphysiol.1974.sp010453

Ionic mechanism for the photoreceptor potential of the retina of Bufo marinus

J E Brown, L H Pinto
PMCID: PMC1350850  PMID: 4207130

Abstract

1. Membrane potentials were recorded from single rods in the isolated retina of Bufo marinus while the ionic composition of the extracellular medium was rapidly changed. Substitution of 2 mM aspartate- for Cl- produced a prompt depolarization of horizontal cells, but no modification of either resting potential or response to light in receptor cells. This implies that feed-back from horizontal cells to receptor cells was not active.

2. During substitution of choline+ or Li+ for Na+, and during isosmotic substitution of sucrose for NaCl, the resting potential of receptor cells became more negative and responses to light were abolished. During exposure to K+-free medium, the resting potential became slightly more negative and the responses to light became larger and developed small after-depolarizations. Exposure to [K+]out of four times normal resulted in permanent diminution of response magnitude and permanent change of response waveshape. Removal of Mg2+, four times normal [Mg2+]out or substitution of methylsulphate- for Cl- had no effect on resting potential or responses to light. With the exception of the small effects seen with altered [K+]out these results are consistent with the receptor potential being generated by a light-induced decrease of membrane conductance to Na+.

3. Exposure to decreased [Ca2+]out caused both a depolarization of the receptor membrane in the dark and an increase in the magnitude of the maximal response that could be evoked by a test stimulus. The magnitude of the increase in response equalled the magnitude of the depolarization. Exposure to increased [Ca2+]out or steady background light caused both a steady hyperpolarization and a decrease in the magnitude of the maximal response that could be evoked by a test stimulus. For steady hyperpolarizations greater than 3·5 mV, whether caused by elevated [Ca2+]out or steady background light, the decrease in response magnitude exceeded the magnitude of the hyperpolarization. These results imply that externally applied Ca2+ ions mimic the effects of steady background lights, but the applied Ca2+ ions must do more than merely decrease membrane conductance to Na+.

Full text

PDF
575

Selected References

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

  1. Baylor D. A., Fuortes M. G. Electrical responses of single cones in the retina of the turtle. J Physiol. 1970 Mar;207(1):77–92. doi: 10.1113/jphysiol.1970.sp009049. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Baylor D. A., Fuortes M. G., O'Bryan P. M. Receptive fields of cones in the retina of the turtle. J Physiol. 1971 Apr;214(2):265–294. doi: 10.1113/jphysiol.1971.sp009432. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bortoff A. Localization of slow potential responses in the Necturus retina. Vision Res. 1964 Dec;4(11):627–635. doi: 10.1016/0042-6989(64)90048-3. [DOI] [PubMed] [Google Scholar]
  4. Cervetto L. Influence of sodium, potassium and chloride ions on the intracellular responses of turtle photoreceptors. Nature. 1973 Feb 9;241(5389):401–403. doi: 10.1038/241401a0. [DOI] [PubMed] [Google Scholar]
  5. Cervetto L., MacNichol E. F., Jr Inactivation of horizontal cells in turtle retina by glutamate and aspartate. Science. 1972 Nov 17;178(4062):767–768. doi: 10.1126/science.178.4062.767. [DOI] [PubMed] [Google Scholar]
  6. FRANKENHAEUSER B., HODGKIN A. L. The action of calcium on the electrical properties of squid axons. J Physiol. 1957 Jul 11;137(2):218–244. doi: 10.1113/jphysiol.1957.sp005808. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Finn A. L., Handler J. S., Orloff J. Active chloride transport in the isolated toad bladder. Am J Physiol. 1967 Jul;213(1):179–184. doi: 10.1152/ajplegacy.1967.213.1.179. [DOI] [PubMed] [Google Scholar]
  8. HODGKIN A. L., HOROWICZ P. The influence of potassium and chloride ions on the membrane potential of single muscle fibres. J Physiol. 1959 Oct;148:127–160. doi: 10.1113/jphysiol.1959.sp006278. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Hagins W. A. The visual process: Excitatory mechanisms in the primary receptor cells. Annu Rev Biophys Bioeng. 1972;1:131–158. doi: 10.1146/annurev.bb.01.060172.001023. [DOI] [PubMed] [Google Scholar]
  10. Korenbrot J. I., Cone R. A. Dark ionic flux and the effects of light in isolated rod outer segments. J Gen Physiol. 1972 Jul;60(1):20–45. doi: 10.1085/jgp.60.1.20. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. 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]
  12. Penn R. D., Hagins W. A. Kinetics of the photocurrent of retinal rods. Biophys J. 1972 Aug;12(8):1073–1094. doi: 10.1016/S0006-3495(72)86145-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Penn R. D., Hagins W. A. Signal transmission along retinal rods and the origin of the electroretinographic a-wave. Nature. 1969 Jul 12;223(5202):201–204. doi: 10.1038/223201a0. [DOI] [PubMed] [Google Scholar]
  14. Sillman A. J., Ito H., Tomita T. Studies on the mass receptor potential of the isolated frog retina. II. On the basis of the ionic mechanism. Vision Res. 1969 Dec;9(12):1443–1451. doi: 10.1016/0042-6989(69)90060-1. [DOI] [PubMed] [Google Scholar]
  15. Tomita T. Electrical activity of vertebrate photoreceptors. Q Rev Biophys. 1970 May;3(2):179–222. doi: 10.1017/s0033583500004571. [DOI] [PubMed] [Google Scholar]
  16. Tomita T. Electrophysiological study of the mechanisms subserving color coding in the fish retina. Cold Spring Harb Symp Quant Biol. 1965;30:559–566. doi: 10.1101/sqb.1965.030.01.054. [DOI] [PubMed] [Google Scholar]
  17. Toyoda J., Nosaki H., Tomita T. Light-induced resistance changes in single photoreceptors of Necturus and Gekko. Vision Res. 1969 Apr;9(4):453–463. doi: 10.1016/0042-6989(69)90134-5. [DOI] [PubMed] [Google Scholar]
  18. Werblin F. S., Dowling J. E. Organization of the retina of the mudpuppy, Necturus maculosus. II. Intracellular recording. J Neurophysiol. 1969 May;32(3):339–355. doi: 10.1152/jn.1969.32.3.339. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Physiology are provided here courtesy of The Physiological Society

RESOURCES