Skip to main content
The Journal of General Physiology logoLink to The Journal of General Physiology
. 1990 Jan 1;95(1):177–198. doi: 10.1085/jgp.95.1.177

Structural and functional properties of two types of horizontal cell in the skate retina

PMCID: PMC2216294  PMID: 2299330

Abstract

Two morphologically distinct types of horizontal cell have been identified in the all-rod skate retina by light- and electron- microscopy as well as after isolation by enzymatic dissociation. The external horizontal cell is more distally positioned in the retina and has a much larger cell body than does the internal horizontal cell. However, both external and internal horizontal cells extend processes to the photoreceptor terminals where they end as lateral elements adjacent to the synaptic ribbons within the terminal invaginations. Whole-cell voltage-clamp studies on isolated cells similar in appearance to those seen in situ showed that both types displayed five separate voltage-sensitive conductances: a TTX-sensitive sodium conductance, a calcium current, and three potassium-mediated conductances (an anomalous rectifier, a transient outward current resembling an A current, and a delayed rectifier). There was, however, a striking difference between external and internal horizontal cells in the magnitude of the current carried by the anomalous rectifier. Even after compensating for differences in the surface areas of the two cell types, the sustained inward current elicited by hyperpolarizing voltage steps was a significantly greater component of the current profile of external horizontal cells. A difference between external and internal horizontal cells was seen also in the magnitudes of their TEA-sensitive currents; larger currents were usually obtained in recordings from internal horizontal cells. However, the currents through these K+ channels were quite small, the TEA block was often judged to be incomplete, and except for depolarizing potentials greater than or equal to +20 mV (i.e., outside the normal operating range of horizontal cells), this current did not provide a reliable indicator of cell type. The fact that two classes of horizontal cell can be distinguished by their electrophysiological responses, as well as by their morphological appearance and spatial distribution in the retina, suggests that they may play different roles in the processing of visual information within the retina.

Full Text

The Full Text of this article is available as a PDF (3.8 MB).

Selected References

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

  1. Brunken W. J., Witkovsky P., Karten H. J. Retinal neurochemistry of three elasmobranch species: an immunohistochemical approach. J Comp Neurol. 1986 Jan 1;243(1):1–12. doi: 10.1002/cne.902430102. [DOI] [PubMed] [Google Scholar]
  2. Dacheux R. F. Connections of the small bipolar cells with the photoreceptors in the turtle. An electron microscope study of Golgi-impregnated, gold-toned retinas. J Comp Neurol. 1982 Feb 10;205(1):55–62. doi: 10.1002/cne.902050106. [DOI] [PubMed] [Google Scholar]
  3. Dowling J. E., Boycott B. B. Organization of the primate retina: electron microscopy. Proc R Soc Lond B Biol Sci. 1966 Nov 15;166(1002):80–111. doi: 10.1098/rspb.1966.0086. [DOI] [PubMed] [Google Scholar]
  4. Dowling J. E., Ripps H. Adaptation in skate photoreceptors. J Gen Physiol. 1972 Dec;60(6):698–719. doi: 10.1085/jgp.60.6.698. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Dowling J. E., Ripps H. S-potentials in the skate retina. Intracellular recordings during light and dark adaptation. J Gen Physiol. 1971 Aug;58(2):163–189. doi: 10.1085/jgp.58.2.163. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Dowling J. E., Ripps H. Visual adaptation in the retina of the skate. J Gen Physiol. 1970 Oct;56(4):491–520. doi: 10.1085/jgp.56.4.491. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Ehinger B., Ottersen O. P., Storm-Mathisen J., Dowling J. E. Bipolar cells in the turtle retina are strongly immunoreactive for glutamate. Proc Natl Acad Sci U S A. 1988 Nov;85(21):8321–8325. doi: 10.1073/pnas.85.21.8321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Fox A. P., Nowycky M. C., Tsien R. W. Kinetic and pharmacological properties distinguishing three types of calcium currents in chick sensory neurones. J Physiol. 1987 Dec;394:149–172. doi: 10.1113/jphysiol.1987.sp016864. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. 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]
  10. Hagiwara S., Takahashi K. The anomalous rectification and cation selectivity of the membrane of a starfish egg cell. J Membr Biol. 1974;18(1):61–80. doi: 10.1007/BF01870103. [DOI] [PubMed] [Google Scholar]
  11. Hals G., Christensen B. N., O'Dell T., Christensen M., Shingai R. Voltage-clamp analysis of currents produced by glutamate and some glutamate analogues on horizontal cells isolated from the catfish retina. J Neurophysiol. 1986 Jul;56(1):19–31. doi: 10.1152/jn.1986.56.1.19. [DOI] [PubMed] [Google Scholar]
  12. Hamill O. P., Marty A., Neher E., Sakmann B., Sigworth F. J. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 1981 Aug;391(2):85–100. doi: 10.1007/BF00656997. [DOI] [PubMed] [Google Scholar]
  13. Hashimoto Y., Kato A., Inokuchi M., Watanabe K. Re-examination of horizontal cells in the carp retina with procion yellow electrode. Vision Res. 1976 Jan;16(1):25–29. doi: 10.1016/0042-6989(76)90072-9. [DOI] [PubMed] [Google Scholar]
  14. Ishida A. T., Fain G. L. D-aspartate potentiates the effects of L-glutamate on horizontal cells in goldfish retina. Proc Natl Acad Sci U S A. 1981 Sep;78(9):5890–5894. doi: 10.1073/pnas.78.9.5890. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kaneko A., Tachibana M. Effects of L-glutamate on the anomalous rectifier potassium current in horizontal cells of Carassius auratus retina. J Physiol. 1985 Jan;358:169–182. doi: 10.1113/jphysiol.1985.sp015546. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kaneko A. The functional role of retinal horizontal cells. Jpn J Physiol. 1987;37(3):341–358. doi: 10.2170/jjphysiol.37.341. [DOI] [PubMed] [Google Scholar]
  17. Kline R. P., Ripps H., Dowling J. E. Generation of b-wave currents in the skate retina. Proc Natl Acad Sci U S A. 1978 Nov;75(11):5727–5731. doi: 10.1073/pnas.75.11.5727. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Lasater E. M., Dowling J. E. Dopamine decreases conductance of the electrical junctions between cultured retinal horizontal cells. Proc Natl Acad Sci U S A. 1985 May;82(9):3025–3029. doi: 10.1073/pnas.82.9.3025. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Lasater E. M., Dowling J. E., Ripps H. Pharmacological properties of isolated horizontal and bipolar cells from the skate retina. J Neurosci. 1984 Aug;4(8):1966–1975. doi: 10.1523/JNEUROSCI.04-08-01966.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Lasater E. M. Ionic currents of cultured horizontal cells isolated from white perch retina. J Neurophysiol. 1986 Mar;55(3):499–513. doi: 10.1152/jn.1986.55.3.499. [DOI] [PubMed] [Google Scholar]
  21. Leech C. A., Stanfield P. R. Inward rectification in frog skeletal muscle fibres and its dependence on membrane potential and external potassium. J Physiol. 1981;319:295–309. doi: 10.1113/jphysiol.1981.sp013909. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. MACNICHOL E. J., SVAETICHIN G. Electric responses from the isolated retinas of fishes. Am J Ophthalmol. 1958 Sep;46(3 Pt 2):26–46. doi: 10.1016/0002-9394(58)90053-9. [DOI] [PubMed] [Google Scholar]
  23. Naka K., Chappell R. L., Sakuranaga M., Ripps H. Dynamics of skate horizontal cells. J Gen Physiol. 1988 Dec;92(6):811–831. doi: 10.1085/jgp.92.6.811. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Newman E. A. Membrane physiology of retinal glial (Müller) cells. J Neurosci. 1985 Aug;5(8):2225–2239. doi: 10.1523/JNEUROSCI.05-08-02225.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Oakley B., 2nd, Green D. G. Correlation of light-induced changes in retinal extracellular potassium concentration with c-wave of the electroretinogram. J Neurophysiol. 1976 Sep;39(5):1117–1133. doi: 10.1152/jn.1976.39.5.1117. [DOI] [PubMed] [Google Scholar]
  26. Perlman I., Knapp A. G., Dowling J. E. Local superfusion modifies the inward rectifying potassium conductance of isolated retinal horizontal cells. J Neurophysiol. 1988 Oct;60(4):1322–1332. doi: 10.1152/jn.1988.60.4.1322. [DOI] [PubMed] [Google Scholar]
  27. Schwartz E. A. Depolarization without calcium can release gamma-aminobutyric acid from a retinal neuron. Science. 1987 Oct 16;238(4825):350–355. doi: 10.1126/science.2443977. [DOI] [PubMed] [Google Scholar]
  28. Shingai R., Christensen B. N. Excitable properties and voltage-sensitive ion conductances of horizontal cells isolated from catfish (Ictalurus punctatus) retina. J Neurophysiol. 1986 Jul;56(1):32–49. doi: 10.1152/jn.1986.56.1.32. [DOI] [PubMed] [Google Scholar]
  29. Shingai R., Christensen B. N. Sodium and calcium currents measured in isolated catfish horizontal cells under voltage clamp. Neuroscience. 1983 Nov;10(3):893–897. doi: 10.1016/0306-4522(83)90227-0. [DOI] [PubMed] [Google Scholar]
  30. Slaughter M. M., Miller R. F. 2-amino-4-phosphonobutyric acid: a new pharmacological tool for retina research. Science. 1981 Jan 9;211(4478):182–185. doi: 10.1126/science.6255566. [DOI] [PubMed] [Google Scholar]
  31. Stell W. K. Correlation of retinal cytoarchitecture and ultrastructure in Golgi preparations. Anat Rec. 1965 Dec;153(4):389–397. doi: 10.1002/ar.1091530409. [DOI] [PubMed] [Google Scholar]
  32. Stell W. K. Horizontal cell axons and axon terminals in goldfish retina. J Comp Neurol. 1975 Feb 15;159(4):503–520. doi: 10.1002/cne.901590405. [DOI] [PubMed] [Google Scholar]
  33. Stell W. K. The structure and relationships of horizontal cells and photoreceptor-bipolar synaptic complexes in goldfish retina. Am J Anat. 1967 Sep;121(2):401–423. doi: 10.1002/aja.1001210213. [DOI] [PubMed] [Google Scholar]
  34. Szamier R. B., Ripps H. The visual cells of the skate retina: structure, histochemistry, and disc-shedding properties. J Comp Neurol. 1983 Mar 20;215(1):51–62. doi: 10.1002/cne.902150105. [DOI] [PubMed] [Google Scholar]
  35. Tachibana M. Ionic currents of solitary horizontal cells isolated from goldfish retina. J Physiol. 1983 Dec;345:329–351. doi: 10.1113/jphysiol.1983.sp014981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Tachibana M. Permeability changes induced by L-glutamate in solitary retinal horizontal cells isolated from Carassius auratus. J Physiol. 1985 Jan;358:153–167. doi: 10.1113/jphysiol.1985.sp015545. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Toyoda J. I., Saito T., Kondo H. Three types of horizontal cells in the stingray retina: their morphology and physiology. J Comp Neurol. 1978 Jun 1;179(3):569–579. doi: 10.1002/cne.901790308. [DOI] [PubMed] [Google Scholar]
  38. Van Haesendonck E., Missotten L. Synaptic contacts of the horizontal cells in the retina of the marine teleost, Callionymus lyra L. J Comp Neurol. 1979 Mar 1;184(1):167–192. doi: 10.1002/cne.901840110. [DOI] [PubMed] [Google Scholar]
  39. Witkovsky P., Stone S., MacDonald E. D. Morphology and synaptic connections of HRP-filled, axon-bearing horizontal cells in the Xenopus retina. J Comp Neurol. 1988 Sep 1;275(1):29–38. doi: 10.1002/cne.902750104. [DOI] [PubMed] [Google Scholar]

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

RESOURCES