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The network properties of bipolar–bipolar cell coupling in the retina of teleost fishes

Published online by Cambridge University Press:  02 June 2009

Osamu Umino ,
Michiyo Maehara ,
Soh Hidaka ,
Shigeo Kita  and
Yoko Hashimoto
Osamu Umino
Affiliation:
Department of Information Sciences, Toho University, Funabashi-shi, Chiba 274, Japan
Michiyo Maehara
Affiliation:
Department of Physiology, Tokyo Women's Medical College, Shinjuku-Ku, Tokyo 162, Japan
Soh Hidaka
Affiliation:
Department of Physiology, Tokyo Women's Medical College, Shinjuku-Ku, Tokyo 162, Japan
Shigeo Kita
Affiliation:
Division of Electron Microscope Laboratory, Medical Research Institute, Tokyo Women's Medical College, Shinjuku-Ku, Tokyo 162, Japan
Yoko Hashimoto
Affiliation:
Department of Physiology, Tokyo Women's Medical College, Shinjuku-Ku, Tokyo 162, Japan
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Abstract

Retinal bipolar cells exhibit a center-surround antagonistic receptive field to a light stimulus (Werblin & Dowling, 1969; Kaneko, 1970), and thus constitute an early stage of spatial information processing. We injected Lucifer Yellow and a small biotinylated tracer, biocytin, into bipolar cells of the teleost retina to examine electrical coupling in these cells. Lucifer-Yellow coupling was observed in one of 55 stained bipolar cells; the coupling pattern was one injected bipolar cell and three surrounding cells. Biocytin coupling was observed in 16 of 55 stained bipolar cells, six of which were ON center and ten OFF center. Although biocytin usually coupled to three to six bipolar cells, some OFF-center bipolar cells showed strong coupling to more than 20 cells. The biocytin-coupled bipolar cells were morphologically homologous. Membrane appositions resembling gap junctions were found between dendrites and between axon terminals of neighboring bipolar cells.

In the strongest biocytin-coupled bipolar cells, the contacts between bipolar cells and cone photoreceptor cells were examined after reconstruction of the dendritic trees of five well-stained, serially sectioned OFF-center bipolar cells. Each of these bipolar cells was in contact with different numbers of cones: 11 to 20 for twin cones and two to four for single cones. This implies that, although these bipolar cells belong to the same category, the signal inputs differ among bipolar cells. Numerical simulation conducted on a hexagonal array network model demonstrated that the electrical coupling of bipolar cells can decrease the difference in input (≈80%) without causing significant loss of spatial resolution. Our results suggest that electrical coupling of bipolar cells has the advantage of decreasing the dispersion of input signals from cones, and permits bipolar cells of the same class to respond to light with similar properties.

Keywords

Electrical couplingBipolar cellsConesBiocytinRetina
Type
Research Articles
Information
Visual Neuroscience , Volume 11 , Issue 3 , May 1994 , pp. 533 - 548
Copyright
Copyright © Cambridge University Press 1994

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References

Baylor, D.A & Fuortes, M.G.F. (1970). Electrical responses of single cones in the retina of the turtle, Journal of Physiology (London) 207, 77–92.CrossRefGoogle ScholarPubMed
Baylor, D.A., Fuortes, M.G.F. & O'Bryan, P.M. (1971). Receptive field of cones in the retina of the turtle. Journal of Physiology (London) 214, 265–294.CrossRefGoogle ScholarPubMed
Borges, S. & Wilson, M. (1987). Structure of the receptive field of bipolar cells in the salamander retina. Journal of Neurophysiology 58, 1275–1291.CrossRefGoogle ScholarPubMed
Campbell, F.W. & Gubisch, R.W. (1966). Optical quality of the human retina. Journal of Physiology (London) 186, 558–578.CrossRefGoogle Scholar
Capovilla, M., Hare, W.A. & Owen, W.G. (1987). Voltage gain of single transmitter from retinal rods to bipolar cells in the tiger salamander. Journal of Physiology (London) 391, 125–140.CrossRefGoogle Scholar
Cohen, E. & Sterling, P. (1990 a). Demonstration of cell types among cone bipolar neurons of cat retina. Philosophical Transactions of the Royal Society B (London) 330, 305–321.Google Scholar
Cohen, E. & Sterling, P. (1990 b). Convergence and divergence of cones onto bipolar cells in the central area of cat retina. Philosophical Transactions of the Royal Society B (London) 330, 305–321.Google ScholarPubMed
Detwiler, P.B. & Hodgkin, A.L. (1979). Electrical coupling between cones in turtle retina. Journal of Physiology 291, 75–100.CrossRefGoogle ScholarPubMed
Hampson, E.C.G.M., Vaney, D.I. & Weiler, R. (1992). Dopaminergic modulation of gap junction permeability between amacrine cells in mammalian retina. Journal of Neuroscience 12, 4911–4922.CrossRefGoogle ScholarPubMed
Hare, W.A. & Owen, W.G. (1990). Spatial organization of the bipolar cell's receptive field in the retina of the tiger salamander retina. Journal of Physiology 421, 223–245.CrossRefGoogle Scholar
Hidaka, S., Maehara, M., Umino, O., Lu, Y. & Hashimoto, Y. (1993). Lateral gap junction connections between retinal amacrine cells summating sustained response. Neuro Report 5, 29–32.Google Scholar
Horikawa, K. & Armstrong, W.E. (1988). A versatile means of intracellular labeling: Injection of biocytin and its detection with avidin conjugates. Journal of Neuroscience Methods 25, 1–11.CrossRefGoogle ScholarPubMed
Kaneko, A. (1970). Physiological and morphological identification of horizontal, bipolar, and amacrine cells in the goldfish retina. Journal of Physiology (London) 207, 623–633.CrossRefGoogle ScholarPubMed
Kita, S. (1984). Wide field serial sections for electron microscopy, (in Japanese). Pathology and Clinical Medicine 2, 1115–1119.Google Scholar
Kraft, T.W. & Burkhardt, D.A. (1986). Telodendrites of cone photoreceptors: Structure and probable function. Journal of Comparative Neurology 249, 13–27.Google Scholar
Kujiraoka, T. & Saito, T. (1986). Electrical coupling between bipolar cells in carp retina. Proceedings of the National Academy of Sciences of the U.S.A. 83, 4063–4066.Google Scholar
Kujiraoka, T. & Umino, O. (1993). The effects of background light on the receptive field center of bipolar cells in carp retina. Japanese Journal of Physiology 43, S216.Google Scholar
Lamb, T.D. (1976). Spatial properties of horizontal cell responses in the turtle retina. Journal of Physiology (London) 263, 239–255.Google Scholar
Lamb, T.D. & Simon, E.J. (1976). The relation between intracellular coupling and electrical noise in turtle photoreceptors. Journal of Physiology (London) 263, 257–286.CrossRefGoogle ScholarPubMed
Mangel, S.C. & Dowling, J.E. (1985). Responsiveness and receptive field size of carp horizontal cells are reduced by prolonged darkness and dopamine. Science 229, 1107–1109.Google Scholar
Marc, R.E., Liu, W.-L.S. & Muller, J.F. (1988). Gap junctions in the inner plexiform layer of the goldfish retina. Vision Research 28, 9–24.Google Scholar
Naka, K.-I. & Christensen, B.N. (1981). Direct electrical connections between transients amacrine cells in the catfish retina. Science 274, 462–464.CrossRefGoogle Scholar
Naka, K.-I. & Rushton, W.A.H. (1967). The generation and spread of S-potentials in fish (Cyprinidae). Journal of Physiology (London) 192, 437–461.CrossRefGoogle ScholarPubMed
Raviola, E. & Gilula, N.B. (1975). Intermembrane organization of specialized contacts in the outer plexiform layer of the retina. Journal of Cell Biology 65, 192–222.CrossRefGoogle Scholar
Saito, T. & Kujiraoka, T. (1982). Physiological and morphological identification of two types of ON-center bipolar cells in the carp retina. Journal of Comparative Neurology 205, 161–170.Google Scholar
Saito, T., Kujiraoka, T. & Toyoda, J.-I. (1984). Electrical and morphological properties of OFF-center bipolar cells in the carp retina. Journal of Comparative Neurology 222, 200–208.Google Scholar
Saito, T. & Kujiraoka, T. (1988). Characteristics of bipolar-bipolar coupling in the carp retina. Journal of General Physiology 91, 275–287.CrossRefGoogle ScholarPubMed
Teranishi, T. (1983). Lateral spread of light-induced response at the cell body and axon terminal levels of external horizontal cells in the carp retina. Japanese Journal of Physiology 33, 417–428.Google Scholar
Teranishi, K., Negishi, K. & Kato, S. (1983). Dopamine modulates S-potential amplitude and dye-coupling between external horizontal cells in carp retina. Nature 301, 243–246.CrossRefGoogle ScholarPubMed
Tomita, T. (1965). Electrophysiological study of the mechanisms subserving color coding in the fish retina. Cold Spring Harbour Symposium Quantal Biology 30, 559–566.CrossRefGoogle ScholarPubMed
Umino, O., Watanabe, K. & Hashimoto, Y. (1989). Neural mechanisms of chromatic adaptation in L-type cone horizontal cells of the carp retina. Japanese Journal of Physiology 39, 725–742.Google ScholarPubMed
Umino, O. & Dowling, J.E. (1991). Dopamine release from interplexiform cells in the retina: Effects of GnRH, FMRFamide, bicuculline, and enkephalin on horizontal cell activity. Journal of Neuroscience 11, 3034–3046.CrossRefGoogle ScholarPubMed
Umino, O., Lee, Y. & Dowling, J.E. (1991). Effect of light stimuli on the release of dopamine from interplexiform cells in the white perch retina. Visual Neuroscience 7, 451–458.Google Scholar
Usui, S., Mitarai, G. & Sakakibara, M. (1983). Discrete nonlinear reduction model for horizontal cell response in the carp retina. Vision Research 23, 413–420.CrossRefGoogle ScholarPubMed
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
Van Haesendonck, E. & Missotten, L. (1983). Stratification and square pattern arrangements in the dorsal inner plexiform layer in the retina of Callionymus lyra L. Journal of Ultrastructure Research 83, 296–302.CrossRefGoogle ScholarPubMed
Werblin, F.S. & Dowling, J.E. (1969). Organization of the retina of the mudpuppy, Necturus maculosus. II. Intracellular recording. Journal of Physiology (London) 32, 339–355.Google Scholar
Werblin, F.S. (1978). Transmission along and between rods in the tiger salamander retina. Journal of Physiology (London) 280, 449–470.CrossRefGoogle ScholarPubMed
Witkovsky, P. & Stell, W.K. (1973). Retinal structure in the smooth dogfish Mustelus canis: Electron microscopy of serially sectioned bipolar cell synaptic terminals. Journal of Comparative Neurology 150, 147–168.Google Scholar
Wong-Riley, M.T.T. (1974). Synaptic organization of the interplexiform layer in the retina of tiger salamander. Journal of Neurocytology 3, 1–33.CrossRefGoogle Scholar
Wu, S.M. (1985). Synaptic transmission from rods to bipolar cells in the tiger salamander retina. Proceedings of the National Academy of Sciences of the U.S.A. 82, 3944–3947.CrossRefGoogle ScholarPubMed
Yamada, M. & Saito, T. (1988). Effects of dopamine on bipolar cells in the carp retina. Biomedical Research 9s-2, 125–130.Google Scholar