Skip to main content
The Journal of Physiology logoLink to The Journal of Physiology
. 1979 Jun;291:75–100. doi: 10.1113/jphysiol.1979.sp012801

Electrical coupling between cones in turtle retina.

P B Detwiler, A L Hodgkin
PMCID: PMC1280889  PMID: 225478

Abstract

1. The electrical coupling between cones of known spectral sensitivity in the peripheral part of the turtle's retina was studied by passing current through a micro-electrode inserted into one cone and recording with a second micro-electrode inserted into a neighbouring cone. 2. Spatial sensitivity profiles were determined by recording flash responses to a long narrow strip of light which was moved across the impaled cones in orthogonal directions. These measurements gave both the length constant lambda of electrical spread in the cone network and the separation of the two cones. 3. The cone separation determined from the spatial profiles agreed closely with that measured directly by injecting a fluorescent dye into two cones. 4. The length constant lambda varied from 18 to 39 micron with a mean of 25 micron for red-sensitive cones and 26 micron for green-sensitive cones. 5. The majority of cone pairs studied were electrically coupled provided they had the same spectral sensitivity and were separated by less than 60 micron: thirty-two out of thirty-six red-red pairs, two out of two green-green pairs, none out of eight red-green pairs: no blue cones were observed. 6. The strength of electrical coupling was expressed as a mutual resistance defined as the voltage in one cell divided by the current flowing into the other. Mutual resistances decreased from a maximum value of about 30 M omega at separations close to zero to 0.2 M omega, the lower limit of detectable coupling at separations of about 60 micron. Mutual resistances were always positive and were independent of which cell was directly polarized. The coupling seemed to be ohmic and any rectification or non-linearity probably arose in the cone membranes rather than in the coupling resistances. 7. The results were analysed in terms of the Lamb & Simon (1977) theories of square and hexagonal lattices, which approximate to the continuous sheet model except in the case of the cone to which current is applied. 8. The total membrane resistance of a single cone was estimated as 100--300 M omega and the connecting resistances as 100 M omega for a square array and 170 M omega for a hexagonal array. The input resistance of a cone in the network was 25--50 M omega. Lower values were often obtained but may be due to injury by the micro-electrodes. 9. The time constant of an isolated cone was estimated as about 20 msec and the capacity as about 100 pF. 10. Discrepancies between experimental findings and theoretical predictions of the hexagonal or square array models were tentatively attributed to an overestimate of lambda resulting from light scattering.

Full text

PDF
75

Images in this article

Selected References

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

  1. 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]
  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. 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]
  4. 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]
  5. Cohen A. I. Some electron microscopic observations on inter-receptor contacts in the human and macaque retinae. J Anat. 1965 Jul;99(Pt 3):595–610. [PMC free article] [PubMed] [Google Scholar]
  6. 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]
  7. 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]
  8. 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]
  9. Hodgkin A. L., Obryan P. M. Internal recording of the early receptor potential in turtle cones. J Physiol. 1977 Jun;267(3):737–766. doi: 10.1113/jphysiol.1977.sp011836. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Hodgkin A. L. The membrane resistance of a non-medullated nerve fibre. J Physiol. 1947 Jul 31;106(3):305–318. doi: 10.1113/jphysiol.1947.sp004214. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Lamb T. D., Simon E. J. Analysis of electrical noise in turtle cones. J Physiol. 1977 Nov;272(2):435–468. doi: 10.1113/jphysiol.1977.sp012053. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. MISSOTTEN L., APPELMANS M., MICHIELS J. L'ULTRA-STRUCTURE DES SYNAPSES DES CELLULES VISUELLES DE LA R'ETINE HUMAINE. Bull Mem Soc Fr Ophtalmol. 1963;76:59–82. [PubMed] [Google Scholar]
  14. NILSSON S. E. INTERRECEPTOR CONTACTS IN THE RETINA OF THE FROG (RANA PIPIENS). J Ultrastruct Res. 1964 Aug;11:147–165. doi: 10.1016/s0022-5320(64)80099-x. [DOI] [PubMed] [Google Scholar]
  15. Peracchia C., Dulhunty A. F. Low resistance junctions in crayfish. Structural changes with functional uncoupling. J Cell Biol. 1976 Aug;70(2 Pt 1):419–439. doi: 10.1083/jcb.70.2.419. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Peracchia C. Gap junctions. Structural changes after uncoupling procedures. J Cell Biol. 1977 Mar;72(3):628–641. doi: 10.1083/jcb.72.3.628. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. 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]
  19. Scholes J. H. Colour receptors, and their synaptic connexions, in the retina of a cyprinid fish. Philos Trans R Soc Lond B Biol Sci. 1975 Feb 20;270(902):61–118. doi: 10.1098/rstb.1975.0004. [DOI] [PubMed] [Google Scholar]
  20. 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]
  21. Stewart W. W. Functional connections between cells as revealed by dye-coupling with a highly fluorescent naphthalimide tracer. Cell. 1978 Jul;14(3):741–759. doi: 10.1016/0092-8674(78)90256-8. [DOI] [PubMed] [Google Scholar]
  22. Tomita T., Kaneko A., Murakami M., Pautler E. L. Spectral response curves of single cones in the carp. Vision Res. 1967 Jul;7(7):519–531. doi: 10.1016/0042-6989(67)90061-2. [DOI] [PubMed] [Google Scholar]
  23. WEIDMANN S. Electrical characteristics of Sepia axons. J Physiol. 1951 Jul;114(3):372–381. doi: 10.1113/jphysiol.1951.sp004628. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES