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H1 horizontal cells of carp retina have different postsynaptic mechanisms to mediate short-versus long-wavelength visual signals

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Vertebrate photoreceptors release neuro-transmitter substance(s) tonically in the dark and this release is curtailed by light. Recently, we have become increasingly aware of the possibility that short- and long-wavelength visual signals are mediated differently during the synaptic transmission to second-order retinal neurons. The experiment described here advances this notion further by demonstrating a postsynaptic difference. Treatment of the carp retina by dopamine reduced the gap-junctional coupling of horizontal cells, and we made use of this known effect to measure the input resistance (Rin) of H1-type horizontal cells. Flashes of light increased Rin. This increase, however, was found to be smaller with short wavelengths, even though the comparison was made when voltage responses were equal in amplitude. Often, Rin was even found to decrease at the blue end of spectrum. No single postsynaptic mechanism can account for any equal-voltage Rin difference such as this. The synaptic spectral segregation thus revealed is probably subserved by a dual scheme wherein the transmitter from blue-sensitive cone photoreceptors acts to decrease the membrane conductance of H1 cells whereas the synapses made by red-and green-sensitive cones are of a classical excitatory type.

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  1. Attwell D, Mobbs P, Tessier-Lavigne M, Wilson M (1987) Neurotransmitter-induced currents in retinal bipolar cells of the axolotl, Ambystoma mexicanum. J Physiol 387: 125–161

  2. Byzov AL, Trifonov YuA, Chailahian LM, Golubtzov KW (1977) Amplification of graded potentials in horizontal cells of the retina. Vision Res 17: 265–273

  3. Dowling JE (1978) Information processing by local circuits: the vertebrate retina as a model system. In: Schmitt F (ed) The neurosciences. MIT Press, Cambridge Mass, pp 163–181

  4. Dowling JE, Ehinger B (1978) The interplexiform cell system I. Synapses of the dopaminergic neurons of the goldfish retina. Proc R Soc B201: 7–26

  5. Franceschini N (1979) Voltage clamp by light: rapid measurement of the spectral and polarization sensitivities of receptor cells. Invest Ophthalmol Suppl 18: p 5 (Abstr)

  6. Hida E, Negishi K, Naka K-I (1984) Effects of dopamine on photopic L-type S-potentials in the catfish retina. J Neurosci Res 11: 373–382

  7. Ishida AT, Kaneko A, Tachibana M (1984) Responses of solitary retinal horizontal cells from Carassius auratus to L-glutamate and related amino acids. J Physiol 348: 255–270

  8. Ishida AT, Neyton J (1985) Quisqualate and L-glutamate inhibit retinal horizontal-cell responses to kainate. Proc Natl Acad Sci USA 82: 1837–1841

  9. Kaneko A (1979) Physiology of the retina. Ann Rev Neurosci 2: 169–191

  10. Kaneko A, Shimazaki H (1975) Effects of external ions on the synaptic transmission from photoreceptors to horizontal cells in the carp retina. J Physiol 252: 509–522

  11. Kaneko A, Tachibana M (1985) Electrophysiological measurements of the spectral sensitivity of three types of cones in the carp retina. Jpn J Physiol 35: 355–365

  12. Kaneko A, Yamada M (1972) S-potentials in the dark-adapted retina of the carp. J Physiol 227: 261–273

  13. Knapp AG, Dowling JE (1987) Dopamine enhances excitatory amino acid-gated conductances in cultured retinal horizontal cells. Nature 325: 437–439

  14. Lasater EM, Dowling JE (1982) Carp horizontal cells in culture respond selectively to L-glutamate and its agonists. Proc Natl Acad Sci USA 79: 936–940

  15. Mangel SC, Ariel M, Dowling JE (1985) Effects of acidic amino acid antagonists upon the spectral properties of carp horizontal cells: circuitry of the outer retina. J Neurosci 5: 2839–2850

  16. Mangel SC, Dowling JE (1985) Responsiveness and receptive field size of carp horizontal cells are reduced by prolonged darkness and dopamine. Science 229: 1107–1109

  17. Marc RE, Lam DMK (1981) Uptake of aspartic and glutamic acid by photoreceptors in the goldfish retina. Proc Natl Acad Sci USA 78: 7185–7189

  18. Mitarai G, Asano T, Miyake Y (1974) Identification of five types of S-potential and their corresponding generating sites in the horizontal cells of the carp retina. Jpn J Ophthalmology 18: 161–176

  19. Murakami M, Takahashi K-I (1987) Calcium action potential and its use for potentials of horizontal cell responses in carp retina. J Physiol 386: 165–180

  20. Nawy S, Copenhagen DR (1987) Multiple classes of glutamate receptor on depolarizing bipolar cells in retina. Nature 325: 56–58

  21. Nelson R (1973) A comparison of electrical properties of neurons in Necturus retina. J Neurophysiol 36: 519–535

  22. O'Dell T, Christensen BN (1986) N-methyl-D-aspartate receptors coexist with kinate and quisqualate receptors on single catfish horizontal cells. Brain Res 381: 359–362

  23. Rowe JS (1987) Effects of external calcium on horizontal cells in the superfused goldfish retina. Neurosci Res Suppl 6: S147-S164

  24. Saito T, Kondo H, Toyoda J (1979) Ionic mechanisms of two types of on-center bipolar cells in the carp retina. I. The responses to central illumination. J Gen Physiol 73: 73–90

  25. Shepherd GM (1983) Neurobiology. Oxford University Press, pp 127–128

  26. Shiells RA, Falk G, Naghshineh S (1981) Action of glutamate and aspartate analogues on rod horizontal and bipolar cells. Nature 294: 592–594

  27. Shigematsu Y, Yamada M (1988) Effects of dopamine on spatial properties of horizontal cell response in the carp retina. Neurosci Res (in press)

  28. Slaughter MM, Miller RF (1981) 2-Amino-4-phosphonobutyric acid: a new pharmacological tool for retinal research. Science 211: 182–185

  29. Smakman JGJ, Pijpker BA (1983) An analog-digital feedback system for measuring photoreceptor properties with an equal response. J Neurosci Meth 8: 365–373

  30. Stell WK, Lightfoot DO, Wheeler TG, Leeper HF (1975) Goldfish retina: functional polarization of cone horizontal cell dendrites and synapses. Science 190: 989–990

  31. Tachibana M (1983) Ionic currents of solitary horizontal cells isolated from goldfish retina. J Physiol 345: 329–351

  32. Tachibana M (1985) Permeability changes induced by L-glutamate in solitary retinal horizontal cells isolated from Carassius auratus. J Physiol 358: 153–167

  33. Tauchi M, Yang X-L, Kaneko A (1984) Depolarizing responses of L-type external horizontal cells in the goldfish retina under intense chromatic background. Vision Res 24: 867–870

  34. Teranishi T, Negishi K, Kato S (1983) Dopamine modulates Spotential amplitude and dye-coupling between external horizontal cells in carp retina. Nature 301: 243–246

  35. Toyoda J-I, Nosaki H, Tomita T (1969) Light-induced resistance changes in single photoreceptors on Necturus and Gekko. Vision Res 9: 453–463

  36. Yang X-L, Tauchi M, Kaneko A (1982) Quantitative analysis of photoreceptor inputs to external horizontal cells in the goldfish retina. Jpn J Physiol 32: 399–420

  37. Yasui S, Ohtsuka T (1986) Horizontal cell signal is smaller with texture-like nonuniform patterns than with uniform fields of the same space average illuminance. Vision Res 26: 583–598

  38. Yasui S, Yamada M (1986) “Voltage clamp by light” reveals a novel membrane property of the crayfish photoreceptor cell. Neurosci Res Suppl 3: p S53 (Abstr)

  39. Yasui S, Yamada M (1987) Conductance-decreasing neurotransmitter action on H1 horizontal cells in the carp retina. Neurosci Res Suppl 5: p S186 (Abstr)

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Correspondence to S. Yasui.

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Yasui, S., Yamada, M. H1 horizontal cells of carp retina have different postsynaptic mechanisms to mediate short-versus long-wavelength visual signals. Exp Brain Res 74, 256–262 (1989). https://doi.org/10.1007/BF00248858

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Key words

  • Retina
  • Horizontal cell
  • Color vision
  • Synapse
  • Dopamine