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. 1980;300:213–250. doi: 10.1113/jphysiol.1980.sp013159

Temporal and spatial characteristics of the voltage response of rods in the retina of the snapping turtle

P B Detwiler *, A L Hodgkin *, P A McNaughton *
PMCID: PMC1279352  PMID: 7381784

Abstract

1. In response to strong, large-field flashes the dark-adapted rods of Chelydra serpentina gave initial hyperpolarizing responses of 30-40 mV, declining rapidly to plateaus of 10-15 mV which lasted 20 sec or more.

2. In the most sensitive cells the flash-sensitivity at 520 nm to a large illuminated area was 3-6 mV per photoisomerization (assuming an effective collecting area of 13·6 μm2).

3. The initial response to a step of light agreed with that predicted by super-position from the flash response but even with very weak lights the step response fell below the predicted curve at times longer than about 2 sec.

4. The step sensitivity defined from the initial peak of the response to a step of light was 2-6 mV photoisomerization-1 sec, about 1000 times greater than the most sensitive cones in the turtle retina.

5. The response to a small weakly illuminated spot (radius 21 μm) reached a peak later and lasted longer than the linear response to a weakly illuminated large area (radius 570 μm).

6. The difference in sensitivity between large and small spots was reasonably consistent with the apparent space constant of the rod network obtained from the exponential decline of the flash response on either side of an illuminated strip.

7. As others have found, strong flashes did not give an initial hyperpolarizing transient when the radius of the spot was less than about 50 μm.

8. Experiments made by flashing long narrow strips of light onto the retina showed that the response spread a long way initially (λ ≑ 70 μm) and then contracted down to a relatively small region (λ ≑ 25 μm) at times of about 2 sec. When the line source was at some distance from the impaled rod the response reached a peak earlier and was shorter than when the source was close.

9. The results in (8) can be explained quantitatively by assuming that delayed voltage-dependent conductance changes mimic an inductance and make the rod network behave like a high-pass filter with series resistance and parallel inductance.

10. In sensitive rods, flash responses varied randomly with a variance which was about 1/30 of that expected in an isolated cell; this reduction in noise is satisfactorily explained by electrical coupling between rods.

11. The variance peak usually occurred later than the potential peak of the rod response.

12. The high-pass filter characteristics of the rod-network help to explain several puzzling features of the behaviour of rods, for example (1), (5), (7), (8) and (11) of this summary.

13. The high-pass filter characteristics of the rod-network may help it to optimize the signal to noise ratio by integrating over a large area for rapid signals and over a small one for slow signals.

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Selected References

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

  1. Bader C. R., MacLeish P. R., Schwartz E. A. Responses to light of solitary rod photoreceptors isolated from tiger salamander retina. Proc Natl Acad Sci U S A. 1978 Jul;75(7):3507–3511. doi: 10.1073/pnas.75.7.3507. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Baylor D. A., Fettiplace R. Kinetics of synaptic transfer from receptors to ganglion cells in turtle retina. J Physiol. 1977 Oct;271(2):425–448. doi: 10.1113/jphysiol.1977.sp012007. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Baylor D. A., Fettiplace R. Light path and photon capture in turtle photoreceptors. J Physiol. 1975 Jun;248(2):433–464. doi: 10.1113/jphysiol.1975.sp010983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. 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]
  5. Baylor D. A., Hodgkin A. L. Changes in time scale and sensitivity in turtle photoreceptors. J Physiol. 1974 Nov;242(3):729–758. doi: 10.1113/jphysiol.1974.sp010732. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Baylor D. A., Hodgkin A. L. Detection and resolution of visual stimuli by turtle photoreceptors. J Physiol. 1973 Oct;234(1):163–198. doi: 10.1113/jphysiol.1973.sp010340. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Baylor D. A., Hodgkin A. L., Lamb T. D. Reconstruction of the electrical responses of turtle cones to flashes and steps of light. J Physiol. 1974 Nov;242(3):759–791. doi: 10.1113/jphysiol.1974.sp010733. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Baylor D. A., Hodgkin A. L., Lamb T. D. The electrical response of turtle cones to flashes and steps of light. J Physiol. 1974 Nov;242(3):685–727. doi: 10.1113/jphysiol.1974.sp010731. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Baylor D. A., Lamb T. D., Yau K. W. Responses of retinal rods to single photons. J Physiol. 1979 Mar;288:613–634. [PMC free article] [PubMed] [Google Scholar]
  10. Baylor D. A., Lamb T. D., Yau K. W. The membrane current of single rod outer segments. J Physiol. 1979 Mar;288:589–611. [PMC free article] [PubMed] [Google Scholar]
  11. Cervetto L., Pasino E., Torre V. Electrical responses of rods in the retina of Bufo marinus. J Physiol. 1977 May;267(1):17–51. doi: 10.1113/jphysiol.1977.sp011799. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Colburn T. R., Schwartz E. A. Linear voltage control of current passed through a micropipette with variable resistance. Med Biol Eng. 1972 Jul;10(4):504–509. doi: 10.1007/BF02474198. [DOI] [PubMed] [Google Scholar]
  13. Copenhagen D. R., Owen W. G. Coupling between rod photoreceptors in a vertebrate retina. Nature. 1976 Mar 4;260(5546):57–59. doi: 10.1038/260057a0. [DOI] [PubMed] [Google Scholar]
  14. Copenhagen D. R., Owen W. G. Functional characteristics of lateral interactions between rods in the retina of the snapping turtle. J Physiol. 1976 Jul;259(2):251–282. doi: 10.1113/jphysiol.1976.sp011465. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Detwiler P. B., Hodgkin A. L. Electrical coupling between cones in turtle retina. J Physiol. 1979 Jun;291:75–100. doi: 10.1113/jphysiol.1979.sp012801. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Detwiler P. B., Hodgkin A. L., McNaughton P. A. A surprising property of electrical spread in the network of rods in the turtle's retina. Nature. 1978 Aug 10;274(5671):562–565. doi: 10.1038/274562a0. [DOI] [PubMed] [Google Scholar]
  17. Fain G. L., Gold G. H., Dowling J. E. Receptor coupling in the toad retina. Cold Spring Harb Symp Quant Biol. 1976;40:547–561. doi: 10.1101/sqb.1976.040.01.051. [DOI] [PubMed] [Google Scholar]
  18. Fain G. L., Quandt F. N., Bastian B. L., Gerschenfeld H. M. Contribution of a caesium-sensitive conductance increase to the rod photoresponse. Nature. 1978 Mar 30;272(5652):466–469. doi: 10.1038/272467a0. [DOI] [PubMed] [Google Scholar]
  19. Fain G. L. Sensitivity of toad rods: Dependence on wave-length and background illumination. J Physiol. 1976 Sep;261(1):71–101. doi: 10.1113/jphysiol.1976.sp011549. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Gold G. H. Photoreceptor coupling in retina of the toad, Bufo marinus. II. Physiology. J Neurophysiol. 1979 Jan;42(1 Pt 1):311–328. doi: 10.1152/jn.1979.42.1.311. [DOI] [PubMed] [Google Scholar]
  21. HODGKIN A. L., HUXLEY A. F. A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol. 1952 Aug;117(4):500–544. doi: 10.1113/jphysiol.1952.sp004764. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Katz B., Miledi R. The statistical nature of the acetycholine potential and its molecular components. J Physiol. 1972 Aug;224(3):665–699. doi: 10.1113/jphysiol.1972.sp009918. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Lamb T. D., Simon E. J. The relation between intercellular coupling and electrical noise in turtle photoreceptors. J Physiol. 1976 Dec;263(2):257–286. doi: 10.1113/jphysiol.1976.sp011631. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Lamb T. D. Spatial properties of horizontal cell responses in the turtle retina. J Physiol. 1976 Dec;263(2):239–255. doi: 10.1113/jphysiol.1976.sp011630. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Leeper H. F., Normann R. A., Copenhagen D. R. Evidence for passive electrotonic interactions in red rods of toad retina. Nature. 1978 Sep 21;275(5677):234–236. doi: 10.1038/275234b0. [DOI] [PubMed] [Google Scholar]
  26. Naka K. I., Rushton W. A. The generation and spread of S-potentials in fish (Cyprinidae). J Physiol. 1967 Sep;192(2):437–461. doi: 10.1113/jphysiol.1967.sp008308. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Schwartz E. A. Electrical properties of the rod syncytium in the retina of the turtle. J Physiol. 1976 May;257(2):379–406. doi: 10.1113/jphysiol.1976.sp011374. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Schwartz E. A. Responses of single rods in the retina of the turtle. J Physiol. 1973 Aug;232(3):503–514. doi: 10.1113/jphysiol.1973.sp010283. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Schwartz E. A. Rod-rod interaction in the retina of the turtle. J Physiol. 1975 Apr;246(3):617–638. doi: 10.1113/jphysiol.1975.sp010907. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Werblin F. S. Transmission along and between rods in the tiger salamander retina. J Physiol. 1978 Jul;280:449–470. doi: 10.1113/jphysiol.1978.sp012394. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Yau K. W., Lamb T. D., Baylor D. A. Light-induced fluctuations in membrane current of single toad rod outer segments. Nature. 1977 Sep 1;269(5623):78–80. doi: 10.1038/269078a0. [DOI] [PubMed] [Google Scholar]

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