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Amacrine cells in the retina of a cyprinid fish: functional characterization and intracellular labelling with horseradish peroxidase

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Summary

Forty amacrine cells in retinae of a cyprinid fish, the roach, were intracellularly labelled with horseradish peroxidase following electrophysiological identification as sustained depolarizing, sustained hyperpolarizing or transient units. Labelled cells were analysed by light microscopy and compared with a catalogue of amacrine cells established in a previous Golgi study on the same species. About 30% of the cell types characterized by the Golgi method were encountered in the present study. When intracellularly labelled cells were differentiated on the basis of their dendritic organization in the plane of the retina, a given electrophysiological response pattern was found to be generated by different morphological types, and vice versa. However, examination of the ramification patterns of the dendrites within the inner plexiform layer (i.e. in the radial dimension of the retina), showed that this morphological parameter of a given amacrine cell could be correlated with its light-evoked response. Several amacrine cell types were found to possess special distal dendrites which arose from the main dendritic branches and extended well over a mm in the retina. Distal dendrites were oriented tangentially with respect to the optic nerve papilla, but did not appear to be involved in any synaptic connectivity. It is concluded that the Golgi-based classification is a valuable tool for identifying intracellularly labelled amacrine cells. However, although the correlation between layering of dendrites in the inner plexiform layer and electrophysiology was generally good, additional physiological parameters would be required to determine whether more extensive parallels exist between structural and functional characteristics of amacrine cells. Alternatively, the considerable morphological diversity of amacrine cells may be of limited physiological significance.

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References

  • Ammermüller J, Weiler R (1981) The ramification pattern of amacrine cells within the inner plexiform layer of the carp retina. Cell Tissue Res 220:699–723

    Google Scholar 

  • Brecha N (1983) Retinal neurotransmitters: Histochemical and biochemical studies. In: Emson PC (ed) Chemical Neuroanatomy. Raven Press, New York, pp 85–129

    Google Scholar 

  • Cajal, R (1893) La rétine des vertébrés. La cellule 9:119–257

    Google Scholar 

  • Catsicas S, Catsicas M, Clarke PGH (1987) Long-distance intraretinal connections in birds. Nature 326:186–187

    Google Scholar 

  • Chan RZ, Naka K-I (1976) The amacrine cell. Vision Res 16:1119–1129

    Google Scholar 

  • Dacey DM (1988) Dopamine-accumulating retinal neurones revealed by in vitro fluorescence display a unique morphology. Science 240:1196–1198

    Google Scholar 

  • Djamgoz MBA (1986) Common features of light-evoked amacrine cell responses in vertebrate retina. Neurosci Lett 71:187–191

    Google Scholar 

  • Djamgoz MBA, Ruddock KH (1978) Effects of local chloride injection on lateral spread of signals in fish (roach) retina. Neurosci Lett 10:23–28

    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, Downing JEG, Wagner H-J (1984) The dendritic fields of functionally identified amacrine cells in a cyprinid fish retina. J Physiol (Lond) 349:21P

    Google Scholar 

  • Dowling JE (1979) Information processing by local circuits: The vertebrate retina as a model system. In: Schmitt FO and Warden FG eds The Neurosciences Fourth Study Program. MIT Press, Cambridge, Mass, pp 163–181

    Google Scholar 

  • Famiglietti EV Jr (1981) Starburst amacrines: 2 mirror-symmetric retinal networks. Invest Ophthalmol Vis Sci 20 [Suppl]: 204

    Google Scholar 

  • Famiglietti EV Jr, Kaneko A, Tachibana M (1977) Neuronal architecture of ON and OFF pathways to ganglion cells in carp retina. Science 198:1267–1268

    Google Scholar 

  • Famiglietti EV Jr, Kolb H (1976) Structural basis for “on” and “off”-center responses in retinal ganglion cells. Science 194:193–195

    Google Scholar 

  • Kaneko A, Hashimoto H (1969) Recording site of the single cone response determined by an electrode marking technique. Vision Res 9:37–55

    Google Scholar 

  • Kaneko A (1973) Receptive field organization of bipolar and amacrine cells in the goldfish retina. J Physiol (Lond) 235:133–153

    Google Scholar 

  • Kolb H (1982) The morphology of bipolar cells, amacrine cells and ganglion cells in the retina of the turtle Pseudemys scripta elegans. Philos Trans R Soc Lond [Biol] 298:355–393

    Google Scholar 

  • Kolb H, Nelson R (1985) Functional neurocircuitry of amacrine cells in the cat retina. In: Gallego A, Gouras P (eds) Neurocircuitry of the retina. A Cajal memorial. Elsevier, Amsterdam

    Google Scholar 

  • Marc RE, Liu W-LS, Muller JF (1988) Gap junctions in the inner plexiform layer of the goldfish retina. Vision Res 28:9–24

    Google Scholar 

  • Mariani AP (1982) Association amacrine cells could mediate directional selectivity in pigeon retina. Nature 298:654–655

    Google Scholar 

  • Mesulam M-M (1982) Tracing neural connections with horseradish peroxidase. Wiley, Chichester

    Google Scholar 

  • Miller RF, Dacheux RF (1976) Dendritic and somatic spikes in mudpuppy amacrine cells: identification and TTX sensitivity. Brain Res 104:157–162

    CAS  PubMed  Google Scholar 

  • Mitarai G, Goto T, Tagaki S (1978) Receptive field arrangement of colour-opponent bipolar and amacrine cells in the carp retina. Sens Proc 2:375–382

    Google Scholar 

  • Murakami M, Shimoda Y (1977) Identification of amacrine and ganglion cells in the carp retina. J Physiol (Lond) 265:801–818

    Google Scholar 

  • Naka K-I, Christensen BN (1981) Direct electrical connections between transient amacrine cells in the catfish retina. Science 214:462–464

    Google Scholar 

  • Naka K-I, Ohtsuka T (1975) Morphological and functional identifications of catfish retinal neurons. II. Morphological identification. J Neurophysiol 38:72–91

    Google Scholar 

  • Naka K-I (1980) A class of catfish amacrine cells responds preferentially to objects which move vertically. Vision Res 20:961–965

    Google Scholar 

  • Normann RA, Kolb H, Hanani M, Pasino E, Holub R (1979) Orientation of horizontal cell axon terminals in the streak of the turtle retina. Nature 280:60–62

    Google Scholar 

  • Perry VH, Walker M (1980) Amacrine cells, displaced amacrine cells and interplexiform cells of the rat. Proc R Soc Lond [Biol] 208:415–431

    Google Scholar 

  • Saito T, Kujiraoka T, Yonaha T, Chino Y (1985) Reexamination of photoreceptor-bipolar connectivity patterns in carp retina: HRP-EM and Golgi-EM studies. J Comp Neurol 236:141–160

    Google Scholar 

  • Snow PJ, Rose PK, Brown AG (1976) Tracing axons and axon collaterals of spinal neurones using intracellular injection of horseradish peroxidase. Science 191:312–313

    Google Scholar 

  • Stell WK (1972) The morphological organization of the vertebrate retina. In: Fuortes MGF (ed) Handbook of Sensory Physiology VII/2 Springer, Berlin Heidelberg New York, pp 111–214

    Google Scholar 

  • Stell WK (1985) Putative peptide transmitters, amacrine cell diversity and function in the inner plexiform layer. In: Gallego A and Gouras P (eds) Neurocircuitry of the Retina. A Cajal Memorial. Oxford, Elsevier, pp 171–181

    Google Scholar 

  • Tauchi M, Masland RH (1984) The shape and arrangement of the cholinergic neurons in the rabbit retina. Proc R Soc Lond [Biol] 223:101–119

    Google Scholar 

  • Teranishi T, Negishi K, Kato S (1987) Functional and morphological correlates of amacrine cells in carp retina. Neuroscience 20:935–950

    Google Scholar 

  • Toyoda J, Hashimoto H, Ohtsu K (1973) Bipolar-amacrine transmission in the carp retina. Vision Res 13:295–307

    Google Scholar 

  • Vallerga S, Deplano S (1984) Differentiation, extent and layering of amacrine cell dendrites in the retina of a sparid fish. Proc R Soc Lond [Biol] 221: 465–477

    Google Scholar 

  • Vaney DI, Peichl L, Boycott BB (1989) Neurofibrillar long-range amacrine cells in mammalian retinae. Proc R Soc Lond [Biol] (in press)

  • Wagner H-J, Wagner E (1988) Amacrine cells in the retina of a teleost fish, the roach (Rutilus rutilus). Philos Trans R Soc Lond [Biol] 321:263–324

    Google Scholar 

  • Werblin F (1979) Time- and voltage-dependent ionic components of the rod response. J Physiol (Lond) 294:613–626

    Google Scholar 

  • Werblin FS, Dowling JE (1969) Organization of the retina of the mudpuppy Necturus maculosus II. Intracellular recording. J Neurophysiol 32:339–355

    Google Scholar 

  • West RW (1972) Superficial warming of epoxy blocks for cutting of 25–150 μm sections resectioned in the 40–90 nm range. Stain Technol 47:201–204

    Google Scholar 

  • Witkovsky P, Dowling JE (1969) Synaptic relationships of the plexiform layers of carp retina. Z Zellforsch 100:60–82

    Google Scholar 

  • Yagi T (1986) Interaction between the soma and the axon terminal of retinal horizontal cells in Cyprinus carpio. J Physiol (Lond) 375:121–135

    Google Scholar 

  • Yagi T, Kaneko A (1988) The axon terminal of goldfish retinal horizontal cells. A low membrane conductance measured in solitary preparations and its implication to the signal conductance from the soma. J Neurophysiol 59:482–494

    Google Scholar 

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Authors and Affiliations

  1. Department of Pure and Applied Biology, Neurobiology Group, Imperial College, University of London, London, UK

    M. B. A. Djamgoz & J. E. G. Downing

  2. Institut für Anatomie und Zellbiologie, Philipps Universität Marburg, Marburg, Federal Republic of Germany

    H. J. Wagner

Authors
  1. M. B. A. Djamgoz
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  2. J. E. G. Downing
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  3. H. J. Wagner
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Additional information

A preliminary account of the present findings was presented to the Physiological Society (Djamgoz et al. 1984)

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Djamgoz, M.B.A., Downing, J.E.G. & Wagner, H.J. Amacrine cells in the retina of a cyprinid fish: functional characterization and intracellular labelling with horseradish peroxidase. Cell Tissue Res. 256, 607–622 (1989). https://doi.org/10.1007/BF00225611

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  • DOI: https://doi.org/10.1007/BF00225611

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