Hostname: page-component-848d4c4894-x5gtn Total loading time: 0 Render date: 2024-05-13T14:46:12.265Z Has data issue: false hasContentIssue false
  • English
  • Français

A comparison of receptive field and tracer coupling size of horizontal cells in the rabbit retina

Published online by Cambridge University Press:  02 June 2009

Stewart A. Bloomfield ,
Daiyan Xin  and
Seth E. Persky
Stewart A. Bloomfield
Affiliation:
Department of Ophthalmology, New York University Medical Center, New York Department of Physiology and Neuroscience, New York University Medical Center, New York
Daiyan Xin
Affiliation:
Department of Ophthalmology, New York University Medical Center, New York
Seth E. Persky
Affiliation:
Department of Ophthalmology, New York University Medical Center, New York
Get access Rights & Permissions [Opens in a new window]

Abstract

The large receptive fields of retinal horizontal cells are thought to reflect extensive electrical coupling via gap junctions. It was shown recently that the biotinylated tracers, biocytin and Neurobiotin, provide remarkable images of coupling between many types of retinal neuron, including horizontal cells. Further, these demonstrations of tracer coupling between horizontal cells rivaled the size of their receptive fields, suggesting that the pattern of tracer coupling may provide some index of the extent of electrical coupling. We studied this question by comparing the receptive field and tracer coupling size of dark-adapted horizontal cells recorded in the superfused, isolated retina-eyecup of the rabbit. Both the edge-to-edge receptive field and space constants (λ) were computed for each cell using a long, narrow slit of light displaced across the retinal surface. Cells were subsequently labeled by iontophoretic injection of Neurobiotin. The axonless A-type horizontal cells showed extensive, homologous tracer coupling in groups greater than 1000 covering distances averaging about 2 mm. The axon-bearing B-type horizontal cells were less extensively tracer coupled, showing homologous coupling of the somatic endings in groups of about 100 cells spanning approximately 400 μm and a separate homologous coupling of the axon terminal endings covering only about 275 μm. Moreover, we observed a remarkable, linear relationship between the size of the receptive fields of each of the three horizontal cell endings and the magnitude of their tracer coupling. Our findings suggest that the extent of tracer coupling provides a strong, linear index of the magnitude of electrical current flow, as derived from receptive-field measures, across groups of coupled horizontal cells. These data thus provide the first direct evidence that the receptive-field size of horizontal cells is related to the extent of their coupling via gap junctions.

Keywords

Receptive fieldsElectrical couplingBiotinylated tracersGap junctionsHorizontal cellsRetina
Type
Research Articles
Information
Visual Neuroscience , Volume 12 , Issue 5 , September 1995 , pp. 985 - 999
Copyright
Copyright © Cambridge University Press 1995

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Adams, J.C. (1977). Technical considerations on the use of horseradish peroxidase as a neuronal marker. Journal of Neuroscience 2, 141–145.CrossRefGoogle ScholarPubMed
Ames, A. III & Nesbett, F.B. (1981). In vitro retina as an experimental model of the central nervous system. Journal of Neurochemistry 37, 867–877.CrossRefGoogle ScholarPubMed
Ammermüller, J., Möckel, W. & Rujan, P. (1993). A geometrical description of horizontal cell networks in the turtle retina. Brain Research 616, 351–356.CrossRefGoogle ScholarPubMed
Baldridge, W.H., Ball, A.K. & Miller, A.G. (1987). Dopaminergic regulation of horizontal cell gap junction particle density in goldfish retina. Journal of Comparative Neurology 265, 428–436.CrossRefGoogle ScholarPubMed
Baldridge, W.H., Ball, A.K. & Miller, A.G. (1989). Gap junction particle density in goldfish retinas lesiones with 6-OHDA. Journal of Comparative Neurology 287, 238–246.CrossRefGoogle Scholar
Bloomfield, S.A. (1992 a). Relationship between receptive and dendritic field size of amacrine cells in the rabbit retina. Journal of Neurophysiology 68, 711–725.CrossRefGoogle ScholarPubMed
Bloomfield, S.A. (1992 b). A unique morphological subtype of horizontal cell in the rabbit retina with orientation-sensitive response properties. Journal of Comparative Neurology 320, 69–85.CrossRefGoogle ScholarPubMed
Bloomfield, S.A. (1993). A comparison of receptive field and tracer coupling size of horizontal cells in the rabbit retina. Investigative Ophthalmology and Visual Science (Suppl.) 34, 1153.Google Scholar
Bloomfield, S.A. & Miller, R.F. (1982). A physiological and morphological study of the horizontal cell types in the rabbit retina. Journal of Comparative Neurology 208, 288–303.CrossRefGoogle ScholarPubMed
Bloomfield, S.A. & Xin, D. (1994). Relationship between tracer-coupling and receptive field size of amacrine and ganglion cells in the rabbit retina. Investigative Ophthalmology and Visual Science (Suppl.) 35, 1822.Google Scholar
Dacey, D.M. & Brace, S. (1992). A coupled network for parasol but not midget ganglion cells in the primate retina. Visual Neuroscience 9, 279–290.CrossRefGoogle Scholar
Dacheux, R.F. & Raviola, F. (1982). Horizontal cells in the retina of the rabbit. Journal of Neuroscience 2, 1486–1493.CrossRefGoogle ScholarPubMed
Fisher, S.K. & Boycott, B.B. (1974). Synaptic connexions made by horizontal cells within the outer plexiform layer of the retina of the cat and the rabbit. Proceedings of the Royal Society B (London) 186, 317–331.Google Scholar
Goddard, J.C., Behrens, U.D., Wagner, H.-J. & Djamgoz, M.B.A. (1991). Biocytin: Intracellular staining, dye-coupling and immuno-cytochemistry in carp retina. Neuroreport 2, 755–758.CrossRefGoogle Scholar
Helm, G.A., Palmer, P.E., Simmons, N.E., diPerro, C.G. & Ebbesson, S.O.E. (1993). A method for utilizing biocytin to study retinofugal pathways at the light and electron microscopic levels. Journal of Neuroscience Methods 49, 97–101.CrossRefGoogle ScholarPubMed
Hidaka, S., Maehara, M., Umino, O., Lu, Y. & Hashimoto, Y. (1993). Lateral gap junction connections between retinal amacrine cells summating sustained responses. Neuroreport 5, 29–32.CrossRefGoogle ScholarPubMed
Jamieson, M.S., Baldridge, W.H. & Ball, A.K. (1994). Modulation of horizontal cell receptive field size in light-adapted goldfish retinas. Investigative Ophthalmology and Visual Science (Suppl.) 35, 1821.Google Scholar
Kaneko, A. (1970). Physiological and morphological identification of horizontal, bipolar, and amacrine cells in goldfish retina. Journal of Physiology 207, 623–633.CrossRefGoogle ScholarPubMed
Kaneko, A. (1971). Electrical connexions between horizontal cells in the dogfish retina. Journal of Physiology 213, 95–105.CrossRefGoogle ScholarPubMed
Kaneko, A. & Stuart, A.E. (1984). Coupling between horizontal cells in the carp retina revealed by diffusion of Lucifer yellow. Neuroscience Letters 47, 1–7.CrossRefGoogle ScholarPubMed
King, M.A., Louis, P.M., Hunter, B.E. & Walker, D.W. (1989). Biocytin: A versatile anterograde anatomical tract-tracing alternative. Brain Research 497, 361–367.CrossRefGoogle Scholar
Kita, H. & Armstrong, W. (1991). A biotin-containing compound N-(2-aminoethyl) biotinamide for intracellular labeling and neuronal tracing studies: Comparison with biocytin. Journal of Neuroscience Methods 37, 141–150.CrossRefGoogle ScholarPubMed
Knapp, A.G. & Dowling, J.E. (1987). Dopamine enhances excitatory amino acid-gated conductances in cultured retinal horizontal cells. Nature (London) 325, 437–439.CrossRefGoogle ScholarPubMed
Knapp, A.G., Schmidt, K.F. & Dowling, J.E. (1990). Dopamine modulates the kinetics of ion channels gated by excitatory amino acids in retinal horizontal cells. Proceedings of the National Academy of Science of the U.S.A. 87, 767–771.CrossRefGoogle ScholarPubMed
Kolb, H. (1977). The organization of the outer plexiform layer in the retina of the cat: Electron microscopic observations. Journal of Neurocytology 6, 131–153.CrossRefGoogle ScholarPubMed
Kurz-Isler, G., Voight, T. & Wolberg, H. (1992). Modulation of connexon densities in gap junctions of horizontal cell perikarya and axon terminals in fish retina: Effects of light/dark cycles, interruption of the optic nerve and application of dopamine. Cell and Tissue Research 268, 267–275.CrossRefGoogle ScholarPubMed
Lachica, E.A., Mavity-Hudson, J.A. & Casagrande, V.A. (1991). Morphological details of primate axons and dendrites revealed by extracellular injection of biocytin: An economic and reliable alternative to PHA-L. Brain Research 564, 1–11.CrossRefGoogle ScholarPubMed
Lamb, T.D. (1976). Spatial properties of horizontal cell responses in the turtle retina. Journal of Physiology 263, 239–255.CrossRefGoogle ScholarPubMed
Mangel, S.C. (1991). Analysis of the horizontal cell contribution to the receptive field surround of ganglion cells in the rabbit retina. Journal of Physiology 442, 211–234.CrossRefGoogle Scholar
Mangel, S.C. & Miller, R.F. (1987). Horizontal cells contribute to the receptive field surround of ganglion cells in the rabbit retina. Brain Research 414, 182–186.CrossRefGoogle Scholar
Marchiafava, P.L. (1978). Horizontal cells influence membrane potential of bipolar cells in the retina of the turtle. Nature (London) 275, 141–142.CrossRefGoogle ScholarPubMed
McMahon, D.G. (1992). Dopamine reduces channel open time in zebrafish horizontal cell electrical synapses. Society for Neuroscience Abstracts 18, 839.Google Scholar
Miller, R.F. & Dacheux, R.F. (1976). Synaptic organization and ionic basis of on- and off-channels in the mudpuppy retina. I. Intracellular analysis of chloride-sensitive electrogenic properties of receptors, horizontal cells, bipolar cells, and amacrine cells. Journal of General Physiology 67, 639–659.CrossRefGoogle Scholar
Mills, S.L. & Massey, S.C. (1994). Distribution and coverage of A- and B-type horizontal cells stained with Neurobiotin in the rabbit retina. Visual Neuroscience 11, 549–560.CrossRefGoogle ScholarPubMed
Naka, K.-I. & Nye, P.W. (1971). Roles of horizontal cells in organization of the catfish retinal receptive field. Journal of Neurophysiology 34, 785–801.CrossRefGoogle ScholarPubMed
Naka, K.-I. & Rushton, W.A.H. (1967). The generation and spread of S-potentials in fish. (Cyprinidae). Journal of Physiology 192, 437–461.CrossRefGoogle ScholarPubMed
Naka, K.-I. & Witkovsky, P. (1972). Dogfish ganglion cells discharges resulting from extrinsic polarization of the horizontal cells. Journal of Physiology 223, 449–460.CrossRefGoogle ScholarPubMed
Nelson, R. (1977). Cat cones have rod input: A comparison of the response properties of cones and horizontal cell bodies in the retina of the cat. Journal of Comparative Neurology 172, 109–136.CrossRefGoogle ScholarPubMed
Nelson, R., Lützow, A.V. & Kolb, H. & Gouras, P. (1975). Horizontal cells in cat retina with independent dendritic systems. Science 189, 137–139.CrossRefGoogle ScholarPubMed
Piccolino, M., Neyton, J., Witkovsky, P. & Gershenfeld, H.M. (1982). γ-Aminobutyric acid antagonists decrease junctional communication between L-type horizontal cells of the retina. Proceedings of the National Academy of Science of the U.S.A. 79, 3671–3675.CrossRefGoogle Scholar
Pu, M. & Berson, D.M. (1992). A method for reliable and permanent intracellular staining of retinal ganglion cells. Journal of Neuroscience Methods 41, 45–51.CrossRefGoogle ScholarPubMed
Raviola, E. & Dacheux, R.F. (1983). Variations in structure and response properties of horizontal cells in the retina of the rabbit. Vision Research 23, 1221–1227.CrossRefGoogle ScholarPubMed
Sarrafizadeh, R., Keifer, J. & Houk, J.C. (1993). Anatomy of the turtle cerebellorubral circuit studied in vitro using neurobiotin and biocytin. Neuroscience Letters 149, 59–62.CrossRefGoogle ScholarPubMed
Shigematsu, Y. & Yamada, M. (1988). Effects of dopamine on spatial properties of horizontal cell responses in the carp retina. Neuroscience Research (Suppl.) 8, 69–80.Google ScholarPubMed
Steinberg, R.H. (1969). Rod and cone contributions to S-potentials from the cat retina. Vision Research 9, 1319–1329.CrossRefGoogle ScholarPubMed
Stewart, W.W. (1978). Functional connections between cells as revealed by dye-coupling with a highly fluorescent naphthalimide tracer. Cell 14, 741–759.CrossRefGoogle ScholarPubMed
Teranishi, T. & Negishi, K. (1994). Double-staining of horizontal and amacrine cells by intracellular injection with Lucifer yellow and biocytin in carp retina. Neuroscience 59, 217–226.CrossRefGoogle ScholarPubMed
Teranishi, T., Negishi, K. & Kato, S. (1983). Dopamine modulates S-potential amplitude and dye-coupling between external horizontal cells in carp retina. Nature (London) 301, 243–246.CrossRefGoogle ScholarPubMed
Teranishi, T., Negishi, K. & Kato, S. (1984). Regulatory effect of dopamine on spatial properties of horizontal cells in carp retina. Journal of Neuroscience 4, 1271–1280.CrossRefGoogle ScholarPubMed
Tomita, T. (1965). Electrophysiological study of the mechanisms subserving color coding in the fish retina. Cold Spring Harbor Symposium on Quantitative Biology 30, 559–566.CrossRefGoogle ScholarPubMed
Umino, O., Maehara, M., Hidaka, S., Kita, S. & Hashimoto, Y. (1994). The network properties of bipolar-bipolar cell coupling in the retina of teleost fishes. Visual Neuroscience 11, 533–548.CrossRefGoogle Scholar
Vaney, D.I. (1991). Many diverse types of retinal neurons show tracer coupling when injected with biocytin or Neurobiotin. Neuroscience Letters 125, 187–190.CrossRefGoogle ScholarPubMed
Vaney, D.l. (1992). Photochromic intensification of diaminobenzidine reaction product in the presence of tetrazolium salts: Applications for intracellular labelling and immunohistochemistry. Journal of Neuroscience Methods 44, 217–223.CrossRefGoogle ScholarPubMed
Vaney, D.I. (1993). The coupling pattern of axon-bearing horizontal cells in the mammalian retina. Proceedings of the Royal Society B (London) 252, 501–508.Google ScholarPubMed
Vaney, D.I. (1994). Patterns of neuronal coupling in the retina. Progress in Retinal Research 13, 301–355.CrossRefGoogle Scholar
Weiler, R., Kohler, K., Kolbinger, W., Wolburg, H. & Kurz-Isler, G. (1988). Dopaminergic neuromodulation in the retina of lower vertebrates. Neuroscience Research 8, 183–196.Google ScholarPubMed
Witkovsky, P., Owen, W.G. & Woodsworth, M. (1983). Gap-junctions among the perikarya, dendrites and axon terminals of the luminosity-type horizontal cells in the turtle retina. Journal of Comparative Neurology 216, 359–368.CrossRefGoogle ScholarPubMed
Witkovsky, P. & Dearry, A. (1994). Functional roles of dopamine in the vertebrate retina. Progress in Retinal Research 11, 247–292.CrossRefGoogle Scholar
Xin, D., Bloomfield, S.A. & Persky, S.E. (1994). Effect of background illumination on tracer-coupling and receptive field size of horizontal and Aii amacrine cells in the rabbit retina. Investigative Ophthalmology and Visual Science (Suppl.) 35, 1363.Google Scholar
Yamada, E. & Ishikawa, T. (1965). The fine structure of the horizontal cells in some vertebrate retinas. Cold Spring Harbor Symposium on Quantitative Biology 30, 383–392.CrossRefGoogle Scholar