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. 1984 Jul;352:703–737. doi: 10.1113/jphysiol.1984.sp015318

A quantitative analysis of interactions between photoreceptors in the salamander (Ambystoma) retina.

D Attwell, M Wilson, S M Wu
PMCID: PMC1193238  PMID: 6747904

Abstract

A quantitative description of the electrical properties of the photoreceptor layer in the salamander retina was obtained from earlier data on the characteristics of isolated rods and cones and on rod-rod coupling, and from new data on rod-cone and cone-cone coupling and on the rod photocurrent. Injecting -1 nA current into a rod elicits hyperpolarizations of about 20 mV in an adjacent rod and 4 mV in an adjacent cone. Responses of more distant receptors are smaller. Injecting -1 nA into a cone elicits hyperpolarizations of about 4 mV in an adjacent rod and 0.4 mV in a nearby cone. Depolarizing current evokes smaller responses. Assuming, in agreement with anatomical evidence, that each rod is electrically coupled to four rods and to four cones around it, and that there is no direct electrical coupling between cones, we found these results could be predicted from the properties of isolated rods and cones if adjacent rods are coupled by a resistance of 300 M omega and adjacent rods and cones are coupled by a resistance of 5000 M omega. The small cone-cone coupling seen is due to coupling via intervening rods. The two halves of double cones are not electrically coupled. The spectral sensitivity of both halves is a maximum around 620 nm wave-length. The rod photocurrent has been characterized by voltage-clamping rods isolated from the retina. In agreement with Bader, MacLeish & Schwartz (1979) we found the time course of the photocurrent to be approximately independent of voltage between -35 and -85 mV. The voltage responses of rods, single cones and double cones isolated from the retina obey the principle of univariance. Responses of receptors in the retina do not obey univariance. The main deviations from univariance observed can be explained if adjacent rods and cones are coupled by a resistance of 5000 M omega. Our data demonstrate that rod-cone coupling is relatively weak. We simplified our description of the photoreceptor network, by omitting cones, to investigate the spatiotemporal processing that the rod network is capable of. Computer simulations predict, as is found experimentally, that the rod voltage response to a large spot of bright light should show a much more pronounced initial transient hyperpolarization than the response to a small spot of light of the same intensity. This difference is produced by the combination of electrical coupling of the rods with the existence of a voltage-gated current, IA, in the rod membrane.(ABSTRACT TRUNCATED AT 400 WORDS)

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Selected References

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  1. Attwell D., Werblin F. S., Wilson M. The properties of single cones isolated from the tiger salamander retina. J Physiol. 1982 Jul;328:259–283. doi: 10.1113/jphysiol.1982.sp014263. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Attwell D., Werblin F. S., Wilson M., Wu S. M. A sign-reversing pathway from rods to double and single cones in the retina of the tiger salamander. J Physiol. 1983 Mar;336:313–333. doi: 10.1113/jphysiol.1983.sp014583. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Attwell D., Wilson M. Behaviour of the rod network in the tiger salamander retina mediated by membrane properties of individual rods. J Physiol. 1980 Dec;309:287–315. doi: 10.1113/jphysiol.1980.sp013509. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. BARLOW H. B. Temporal and spatial summation in human vision at different background intensities. J Physiol. 1958 Apr 30;141(2):337–350. doi: 10.1113/jphysiol.1958.sp005978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bader C. R., Macleish P. R., Schwartz E. A. A voltage-clamp study of the light response in solitary rods of the tiger salamander. J Physiol. 1979 Nov;296:1–26. doi: 10.1113/jphysiol.1979.sp012988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. 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]
  7. 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]
  8. 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]
  9. 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]
  10. Custer N. V. Structurally specialized contacts between the photoreceptors of the retina of the axolotl. J Comp Neurol. 1973 Sep 1;151(1):35–56. doi: 10.1002/cne.901510104. [DOI] [PubMed] [Google Scholar]
  11. 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]
  12. 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]
  13. Detwiler P. B., Hodgkin A. L., McNaughton P. A. Temporal and spatial characteristics of the voltage response of rods in the retina of the snapping turtle. J Physiol. 1980 Mar;300:213–250. doi: 10.1113/jphysiol.1980.sp013159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Fain G. L. Interactions of rod and cone signals in the mudpuppy retina. J Physiol. 1975 Nov;252(3):735–769. doi: 10.1113/jphysiol.1975.sp011168. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. 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]
  16. Gold G. H., Dowling J. E. Photoreceptor coupling in retina of the toad, Bufo marinus. I. Anatomy. J Neurophysiol. 1979 Jan;42(1 Pt 1):292–310. doi: 10.1152/jn.1979.42.1.292. [DOI] [PubMed] [Google Scholar]
  17. 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]
  18. Griff E. R., Pinto L. H. Interactions among rods in the isolated retina of Bufo marinus. J Physiol. 1981 May;314:237–254. doi: 10.1113/jphysiol.1981.sp013704. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hanani M., Vallerga S. Rod and cone signals in the horizontal cells of the tiger salamander retina. J Physiol. 1980 Jan;298:397–405. doi: 10.1113/jphysiol.1980.sp013089. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. 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]
  21. Liebman P. A., Entine G. Visual pigments of frog and tadpole (Rana pipiens). Vision Res. 1968 Jul;8(7):761–775. doi: 10.1016/0042-6989(68)90128-4. [DOI] [PubMed] [Google Scholar]
  22. Manteuffel G., Plasa L., Sommer T. J., Wess O. Involuntary eye movements in salamanders. Naturwissenschaften. 1977 Oct;64(10):533–534. doi: 10.1007/BF00483559. [DOI] [PubMed] [Google Scholar]
  23. McNaughton P. A., Yau K. W., Lamb T. D. Spread of activation and desensitisation in rod outer segments. Nature. 1980 Jan 3;283(5742):85–87. doi: 10.1038/283085a0. [DOI] [PubMed] [Google Scholar]
  24. Naka K. I., Rushton W. A. S-potentials from colour units in the retina of fish (Cyprinidae). J Physiol. 1966 Aug;185(3):536–555. doi: 10.1113/jphysiol.1966.sp008001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Nelson R. Cat cones have rod input: a comparison of the response properties of cones and horizontal cell bodies in the retina of the cat. J Comp Neurol. 1977 Mar 1;172(1):109–135. doi: 10.1002/cne.901720106. [DOI] [PubMed] [Google Scholar]
  26. Nishimura Y., Shimai K. Clasping structure in the double cone of the retina of the turtle (Gyoclemys reevesii). Cell Tissue Res. 1980;209(3):391–398. doi: 10.1007/BF00234754. [DOI] [PubMed] [Google Scholar]
  27. Raviola E., Gilula N. B. Gap junctions between photoreceptor cells in the vertebrate retina. Proc Natl Acad Sci U S A. 1973 Jun;70(6):1677–1681. doi: 10.1073/pnas.70.6.1677. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Richter A., Simon E. J. Electrical responses of double cones in the turtle retina. J Physiol. 1974 Nov;242(3):673–683. doi: 10.1113/jphysiol.1974.sp010730. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Schwartz E. A. Cones excite rods in the retina of the turtle. J Physiol. 1975 Apr;246(3):639–651. doi: 10.1113/jphysiol.1975.sp010908. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. 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]
  31. Uga S., Nakao F., Mimura M., Ikui H. Some new findings on the fine structure of the human photoreceptor cells. J Electron Microsc (Tokyo) 1970;19(1):71–84. [PubMed] [Google Scholar]
  32. 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]
  33. Wilson M., Attwell D. A new method for obtaining isolated photoreceptors from the amphibian retina. Pflugers Arch. 1983 Nov;399(3):238–240. doi: 10.1007/BF00656722. [DOI] [PubMed] [Google Scholar]

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