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Correlation of spinule dynamics and plasticity of the horizontal cell spectral response in cyprinid fish retina: quantitative analysis

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Summary

A negative feedback interaction between luminosity type horizonatal cells (HCs) and green-sensitive cones generates the long-wavelength-sensitive depolarizing response in biphasic chromaticity type HCs. This interaction is suppressed in the dark and is potentiated by light adaptation of the retina. HCs are morphologically ‘plastic’; during light adaptation, their dendritic terminals within cone pedicles extend, giving rise to “spinules”. This paper examines whether there is a quantitative correlation between the time course of light-dependent formation of the spinules and enhancement of the feedback interaction. The strength of the feedback interaction in isolated retinac of the roach was determined as the ‘neutral wavelength’ at which reversal of spectral response polarity occurred in biphasic HCs. A good correlation was found between the ‘neutral wavelength’ and the spinule/ribbon ratios of retinae. Biphasic HCs were intracellularly stained with horseradish peroxidase and the correlative ultrastructure of the contacted pedicles was examined. ‘Neutral wavelength’ was found to be correlated with the spinule number, weighted according to the number of synaptic contacts mediating feed-forward transmission. The latter was estimated from the total number of labelled Cb/H2 HC processes (central and lateral) at synaptic triads. A model in which spinules mediate the negative feedback interaction of HCs in the retina of cyprinid fish is presented.

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References

  • Baylor DA, Fuortes MGF, O'Bryan PM (1971) Receptive fields of cones in the retina of the turtle. J Physiol (Lond) 214:265–294

    Google Scholar 

  • Bloom FE, Aghajanian GK (1968) Fine structural and cytochemical analysis of the staining of synaptic junctions stained with phosphotungstic acid. J Ultrastruet Res 22:361–375

    Google Scholar 

  • Brandon JG, Coss RG (1982) Rapid dendritic spine stem shortening during one trial learning: the honeybee's first orientation flight. Brain Res 252:51–61

    Google Scholar 

  • Brown TH, Chang VC, Ganong AH, Keenan CL, Kelso SR (1988) Biophysical properties of dendrites and spines that may control the induction and expression of long-term synaptic potentiation. In: Long-term potentiation. From biophysics to behaviour. Alan R Liss, New York, pp 201–264

    Google Scholar 

  • Burkhardt DA (1977) Responses and receptive-field organization of cones in perch retina. J Neurophisiol 40:53–62

    Google Scholar 

  • Byzov AL, Shura-Bura TM (1986) Electrical feedback mechanism in the processing of signals in the outer plexiform layer of the retina. Vision Res 26:33–44

    Google Scholar 

  • Byzov AL, Golubtzov KV, Trifonov JA (1977) The model of mechanism of feedback between horizontal cells and photoreceptors in vertebrate retina. In: Barlow HB, Fatt P (eds) Vertebrate photoreception. Academic Press, London New York San Francisco, pp 265–274

    Google Scholar 

  • Coss RG (1978) Spine stems on tectal interneurons in jewel fish are shortened by social stimulation. Science 200:787–790

    Google Scholar 

  • Coss RG, Perkel DH (1985) The function of dendritic spines. A review of theoretical issues. Behav Neural Biol 44:151–185

    Google Scholar 

  • Djamgoz MBA (1984) Electrophysiological characterization of spectral sensitivities of horizontal cells in cyprinid fish retina. Vision Res 24:1677–1687

    Google Scholar 

  • Djamgoz MBA, Rudoock KH (1979) Effects of picrotoxin and strychnine on fish retinal-S potentials: evidence for inhibitory control of depolarizing responses. Neurosci Lett 12:329–334

    Google Scholar 

  • Djamgoz MBA, Wagner H-J (1987) Intracellular staining of retinal neurones: applications to studies of functional organization. Prog Retinal Res 6:85–150

    Google Scholar 

  • Djamgoz MBA, Yamada M (1990) Electrophysiological characteristics of retinal neurones: synaptic interactions and functional outputs. In: RH Douglas, MBA Djamgoz (eds) The visual system of fish Chapman & Hall, London

    Google Scholar 

  • Djamgoz MBA, Downing JEG, Wagner H-J (1985) The cellular origin of an unusual type of S-potential: an intracellular horseradish peroxidase study in a cyprinid fish retina. J Neurocytol 14:469–486

    Google Scholar 

  • Djamgoz MBA, Downing JEG, Wagner H-J (1987) Retinal neurones of cyprinid fish: intracellular marking with horseradish peroxidase and correlative morphological analysis. Exp Biol 46:203–216

    Google Scholar 

  • Djamgoz MBA, Downing JEG, Kirsch M, Prince DJ, Wagner H-J (1988) Plasticity of cone horizontal cell functioning in cyprinid fish retina: effects of background illumination of moderate intensity. J Neurocytol 17:701–710

    Google Scholar 

  • Downing JEG, Djamgoz MBA (1989) Quantitative analysis of cone photoreceptor-horizontal cell connectivity patterns in the retina of a cyprinid fish: electron microscopy of functionally-identified and HRP-labelled horizontal cells. J Comp Neurol (in press)

  • Downing JEG, Djamgoz MBA, Bowmaker JK (1986) Photoreceptors of a cyprinid fish, the roach: morphological and spectral characteristics. J Comp Physiol (A) 159:859–868

    Google Scholar 

  • Fiszer de Plazas S, Alfie J, González NN (1986) Light and dark adaptation influences GABA receptor sites in the chick retina. Neurochem Res 11:973–981

    Google Scholar 

  • Fuortes MGF, Simon EJ (1974) Interactions leading to horizontal cell responses in the turtle retina. J Physiol (Lond) 240:177–198

    Google Scholar 

  • Hamlyn LH (1963) The fine structure of the mossy fibre endings in the hippocampus of the rabbit. J Anat 96:112–120

    Google Scholar 

  • Marc RE, Stell WK, Bok D, Lam DMK (1978) GABA-ergic path-ways in the goldfish retina. J Comp Neurol 182:221–246

    Google Scholar 

  • Murakami M, Shimoda Y, Nakatani K, Miyachi E, Watanabe S (1982a) GABA-mediated negative feedback from horizontal cells to cones in carp retina. Jpn J Physiol 32:911–926

    Google Scholar 

  • Murakami M, Shimoda Y, Nakatani K, Miyachi F, Watanabe S (1982b) GABA-mediated negative feedback and colour opponcency in carp retina. Jpn J Physiol 32:927–935

    Google Scholar 

  • Naka K-I, Rushton WHA (1966) S-potentials from colour units in the retina of fish (Cyprinidae). J Physiol (Lond) 185:587–599

    Google Scholar 

  • O'Bryan PM (1973) Properties of depolarizing synaptic potentials evoked by peripheral illumination in cones of the turtle retima. J Physiol (Lond) 235:207–223

    Google Scholar 

  • Pepperberg DR, Masland RH (1978) Retina-induced sensitization of light-adapted rabbit photoreceptors. Brain Res 151:194–200

    Google Scholar 

  • Pfenniger KH (1973) Synaptic morphology and cytochemistry. Progr in Histochem Cytochem 5:1–86

    Google Scholar 

  • Pongrácz F (1985) The function of dendritic spines: a theoretical study. Neuroscience 15:933–946

    Google Scholar 

  • Prince DJ, Djamgoz MBA, Karten HJ (1987) GABA transaminase in cyprinid fish retina: Localization and effects of inhibitors on temporal characteristics of S-potentials. Neurochem Int 11:23–30

    Google Scholar 

  • Raynauld J-P, Laviolette JR, Wagner H-J (1979) Goldfish retina: a correlate between cone activity and morphology of the horizontal cell in cone pedicles. Science 204:1436–1438

    Google Scholar 

  • Sakai H, Naka K-I (1983) Synaptic organizations involving receptor, horizontal and on-and off-centre bipolar cells in catfish retina. Vision Res 23:339–351

    Google Scholar 

  • Sakai H, Naka K-I (1986) The synaptic organization of the cone horizontal cells in the catfish retina. J Comp Neurol 345:107–115

    Google Scholar 

  • Sloper JJ (1971) Dendrodendritic synapses in the primate motor cortex. Brain Res 34:186–192

    Google Scholar 

  • Spacek J (1985) Three-dimensional analysis of dendritic spines. II. Spine apparatus and other cytoplasmic components. Anat Embryol 171:235–243

    Google Scholar 

  • Stell WK, Lightfoot DO (1975) Colorpspecific interconnections of cones and horizontal cells in the retina of the goldfish. J Comp Neurol 159:473–502

    Google Scholar 

  • Stell WK, Lightfoot DO, Wheeler T, Leeper H (1975) Goldfish retina: Functional polarization of cone horizontal cell dendrites and synapses. Science 190:989–990

    Google Scholar 

  • Stell WK, Kretz R, Lightfoot DO (1982) Horizontal cell connectivity in goldfish. In: Drujan BD, Laufer M (eds) The S-potential. Alan R Liss, Inc, New York, pp 51–75

    Google Scholar 

  • Tamura T, Niwa H (1967) Spectral sensitivity and color vision of fish as indicated by S-potential. Comp Biochem Physiol 22:745–754

    Google Scholar 

  • Wagner H-J (1980) Light-dependent plasticity of the morphology of horizontal cell terminals in cone pedicles of fish retinas. J Neurocytol 9:575–590

    Google Scholar 

  • Weiler R, Wagner H-J (1984) Light-dependent change of conehorizontal cell interactions in carp retina. Brain Res 298:1–9

    Google Scholar 

  • Yazulla S (1985) Evoked efflux of 3H-GABA from goldfish retina in the dark. Brain Res 325:171–180

    Google Scholar 

  • Yazulla S (1986) GABAergic mechanisms in the retina. In: Osborne NN, Chader GJ (eds) Prog Retinal Res, Vol 5. Pergamon, Oxford, pp 1–52

    Google Scholar 

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Kirsch, M., Djamgoz, M.B.A. & Wagner, HJ. Correlation of spinule dynamics and plasticity of the horizontal cell spectral response in cyprinid fish retina: quantitative analysis. Cell Tissue Res 260, 123–130 (1990). https://doi.org/10.1007/BF00297497

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