Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-23T19:55:44.708Z Has data issue: false hasContentIssue false
  • English
  • Français

Simulation analysis of receptive-field size of retinal horizontal cells by ionic current model

Published online by Cambridge University Press:  05 April 2005

TOSHIHIRO AOYAMA ,
YOSHIMI KAMIYAMA  and
SHIRO USUI
TOSHIHIRO AOYAMA
Affiliation:
Department of Electronic and Information Engineering, Suzuka National College of Technology, Shiroko, Suzuka-City, Japan
YOSHIMI KAMIYAMA
Affiliation:
Faculty of Information Science and Technology, Aichi Prefectural University, Nagakute, Japan
SHIRO USUI
Affiliation:
Brain Science Institute, RIKEN, Wako, Saitama, Japan
Get access Rights & Permissions [Opens in a new window]

Abstract

The size of the receptive field of retinal horizontal cells changes with the state of dark/light adaptation. We have used a mathematical model to determine how changes in the membrane conductance affect the receptive-field properties of horizontal cells. We first modeled the nonlinear membrane properties of horizontal cells based on ionic current mechanisms. The dissociated horizontal cell model reproduced the voltage–current (V–I) relationships for various extracellular glutamate concentrations measured in electrophysiological studies. Second, a network horizontal cell model was also described, and it reproduced the V–I relationship observed in vivo. The network model showed a bell-shaped relationship between the receptive-field size and constant glutamate concentration. The simulated results suggest that the calcium current is a candidate for the bell-shaped length constant relationship.

Keywords

Retinal horizontal cellReceptive fieldIonic currentMathematical model
Type
Research Article
Information
Visual Neuroscience , Volume 22 , Issue 1 , January 2005 , pp. 65 - 78
Copyright
© 2005 Cambridge University Press

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

Aoyama, T., Kamiyama, Y., Usui, S., Blanco, R., Vaquero, C.F., & de la Villa, R. (2000). Ionic current model of rabbit retinal horizontal cell. Neuroscience Research 37, 141–151.CrossRefGoogle Scholar
Balboa, R.M. & Grzywacz, N.M. (2000). The minimal local-asperity hypothesis of early retinal lateral inhibition. Neural Computation 12, 1485–1517.CrossRefGoogle Scholar
Benda, J., Bock, R., Rujan, P., & Ammermüller, J. (2001). Asymmetrical dynamics of voltage spread in retinal horizontal cell networks. Visual Neuroscience 18, 835–848.CrossRefGoogle Scholar
Bornstein, O., Twig, G., Benda, J., Weiler, R., & Perlman, I. (2002). Dynamic changes in the receptive fields of L1-type horizontal cells in the retina of the turtle mauremys caspica. Visual Neuroscience 19, 621–632.CrossRefGoogle Scholar
Brew, H. & Attwell, D. (1987). Electrogenic glutamate uptake is a major current carrier in the membrane of axolotl retinal glial cells. Nature 327, 707–709.CrossRefGoogle Scholar
Byzov, A.L. & Shura-Bura, T.M. (1983). Spread of potentials along the network of horizontal cells in the retina of the turtle. Vision Research 23, 389–397.CrossRefGoogle Scholar
Dixon, D.B. & Copenhagen, D.R. (1997). Metabotropic glutamate receptor-mediated suppression of an inward rectifier current is linked via a cGMP cascade. Journal of Neuroscience 17, 8945–8954.Google Scholar
Djamgoz, M.B.A., Sekaran, S., Angotzi, A.R., Haamedi, S., Vallerga, S., Hirano, J., & Yamada, M. (2000). Light-adaptive role of nitric oxide in the outer retina of lower vertebrates: A brief review. Philosophical Transactions of the Royal Society B (London) 355, 1199–1203.CrossRefGoogle Scholar
Furukawa, T., Petruv, R., Yasui, S., Yamada, M., & Djamgoz, M.A. (2002). Nitric oxide controls the light adaptive chromatic difference in receptive field size of H1 horizontal cell network in carp retina. Experimental Brain Research 147, 296–304.CrossRefGoogle Scholar
Gaal, L., Roska, B., Picaud, S.A., Wu, S.M., Marc, R., & Werblin, F.S. (1998). Postsynaptic response kinetics are controlled by a glutamate transporter at cone photoreceptors. Journal of Neurophysiology 79, 190–196.Google Scholar
Hayashida, Y. & Yagi, T. (2002). On the interaction between voltage-gated conductances and Ca2+ regulation mechanisms in retinal horizontal cells. Journal of Neurophysiology 87, 172–182.CrossRefGoogle Scholar
Hayashida, Y., Yagi, T., & Yasui, S. (1998). Ca2+ regulation by the Na+–Ca2+ exchanger in retinal horizontal cells depolarized by L-glutamate. Neuroscience Research 31, 189–199.CrossRefGoogle Scholar
Ishida, A.T., Kaneko, A., & Tachibana, M. (1984). Responses of solitary retinal horizontal cells from carassius auratus to L-glutamate and related amino acids. Journal of Physiology 348, 255–270.CrossRefGoogle Scholar
Itzhaki, A. & Perlman, I. (1984). Light adaptation in luminosity horizontal cells in the turtle retina. Vision Research 24, 1119–1126.CrossRefGoogle Scholar
Itzhaki, A. & Perlman, I. (1987). Light adaptation of red cones and L1-horizontal cells in the turtle retina: effect of the background spatial pattern. Vision Research 27, 685–696.CrossRefGoogle Scholar
Johnston, D. & Wu, S.M. (1995). Foundations of Cellular Neurophysiology. Cambridge, Massachusetts: The MIT Press.
Kamermans, M., Haak, J., Habraken, J.B., & Spekreijse, H. (1996). The size of the horizontal cell receptive fields adapts to the stimulus in the light adapted goldfish retina. Vision Research 36, 4105–4119.CrossRefGoogle Scholar
Kaneko, A. (1971). Electrical connexions between horizonal cells in the dogfish retina. Journal of Physiology 213, 95–105.CrossRefGoogle Scholar
Kaneko, A. (1987). The functional role of retinal horizontal cells. Japanese Journal of Physiology 37, 341–358.CrossRefGoogle Scholar
Kaneko, A. & Tachibana, M. (1985). Effects of L-glutamate on the anomalous rectifier potassium current in horizontal cells of carassius auratus retina. Journal of Physiology 358, 169–182.CrossRefGoogle Scholar
Lamb, T. (1976). Spatial properties of horizontal cell responses in the turtle retina. Journal of Physiology 263, 239–255.CrossRefGoogle Scholar
Lankheet, M.J., Frens, M.A., & van de Grind, W.A. (1990). Spatial properties of horizontal cell responses in the cat retina. Vision Research 30, 1257–1275.CrossRefGoogle Scholar
Lasater, E.M. & Dowling, J.E. (1985). Dopamine decreases conductance of the electrical junctions between cultured retinal horizontal cells. Proceedings of the National Academy of Sciences of the U.S.A. 82, 3025–3029.CrossRefGoogle Scholar
Lasater, E.M. (1986). Ionic currents of cultured horizontal cells isolated from perch retina. Journal of Neurophysiology 55, 499–513.Google Scholar
Linn, C.L. & Gafka, A.C. (2001). Modulation of a voltage-gated calcium channel linked to activation of glutamate receptors and calcium-induced calcium release in the catfish retina. Journal of Physiology 535, 47–63.CrossRefGoogle Scholar
Lu, C. & McMahon, D.G. (1996). Gap junction channel gating at bass retinal electrical synapses. Visual Neuroscience, 13, 1049–1057.CrossRefGoogle Scholar
Lu, C., Zhang, D., & McMahon, D.G. (1999). Electrical coupling of retinal horizontal cells mediated by distinct voltage-independent junctions. Visual Neuroscience 16, 811–818.Google Scholar
Lu, T., Shen, Y., & Yang, X. (1998). Desensitization of AMPA receptors on horizontal cells isolated from crucian carp retina. Neuroscience Research 31, 123–135.CrossRefGoogle Scholar
Mangel, S.C. & Dowling, J.E. (1987). The interplexiform-horizontal cell system of the fish retina: Effects of dopamine, light stimulation and time in the dark. Proceedings of the Royal Society B (London) 231, 91–121.CrossRefGoogle Scholar
McMahon, D.G., Zhang, D., Ponomareva, L., & Wagner, T. (2001). Synaptic mechanisms of network adaptation in horizontal cells. Progress in Brain Research 131, 419–436.CrossRefGoogle Scholar
Micci, M.A. & Christensen, B.N. (1998). Na+/Ca2+ exchange in catfish retina horizontal cells: regulation of intracellular Ca2+ store function. American Journal of Physiology 274, C1624–C1633.Google Scholar
Miyachi, E. & Murakami, M. (1989). Decoupling of horizontal cells in carp and turtle retinae by intracellular injection of cyclic AMP. Journal of Physiology 419, 213–224.CrossRefGoogle Scholar
Neher, E. & Augustine, G.J. (1992). Calcium gradients and buffers in bovine chromaffin cells. Journal of Physiology 450, 273–301.CrossRefGoogle Scholar
O'Dell, T.J. & Christensen, B.N. (1989). Horizontal cells isolated from catfish retina contain two types of excitatory amino acid receptors. Journal of Neurophysiology 61, 1097–1109.Google Scholar
Perlman, I. & Ammermüller, J. (1994). Receptive-field size of L1 horizontal cells in the turtle retina: Effects of dopamine and background light. Journal Neurophysiology. 72, 2786–2795.Google Scholar
Pottek, M. & Weiler, R. (2000). Light-adaptive effects on retinoic acid on receptive field properties of retinal horizontal cells. European Journal of Neuroscience 12, 437–445.CrossRefGoogle Scholar
Shen, Y., Lu, T., & Yang, X.-L. (1999). Modulation of desensitization at glutamate receptors in isolated crucian carp horizontal cells by concanavalin A, cyclothiazide, aniracetam and pepa. Neuroscience 89, 979–990.CrossRefGoogle Scholar
Stell, W.K. (1975). Horizontal cell axons and axon terminals in goldfish retina. Journal of Comparative Neurology 159, 503–520.CrossRefGoogle Scholar
Tachibana, M. (1981). Membrane properties of solitary horizontal cells isolated from goldfish retina. Journal of Physiology 321, 141–161.CrossRefGoogle Scholar
Tachibana, M. (1983). Ionic currents of solitary horizontal cells isolated from goldfish retina. Journal of Physiology 345, 329–351.CrossRefGoogle Scholar
Tachibana, M. (1985). Permeability change induced by L-glutamate in solitary retinal horizontal cells isolated from carassius auratus. Journal of Physiology 358, 153–167.CrossRefGoogle Scholar
Tachibana, M. & Kaneko, A. (1988). L-glutamate-induced depolarization in solitary photoreceptors: A process that may contribute to the interaction between photoreceptors in situ. Proceedings of the National Academy of Sciences of the U.S.A. 85, 5315–5319.CrossRefGoogle Scholar
Takabayashi, A. & Mitarai, G. (1985). Electrical properties of horizontal cell network in the carp retina. Neuroscience Research (Suppl.) 2, 133–146.Google Scholar
Umino, O., Lee, Y., & Dowling, J.E. (1991). Effects of light stimuli on the release of dopamine from interplexiform cells in the white perch retina. Visual Neuroscience 7, 451–458.CrossRefGoogle Scholar
Usui, S., Kamiyama, Y., Ishii, H., & Ikeno, H. (1996). Reconstruction of retinal horizontal cell responses by the ionic current model. Vision Research 36, 1711–1719.CrossRefGoogle Scholar
van de Grind, W., Lankheet, M., van Wezel, R., Rowe, M., & Hulleman, J. (1996). Gain control and hyperpolarization level in cat horizontal cells as a function of light and dark adaptation. Vision Research 36, 3969–3985.CrossRefGoogle Scholar
Vandenbranden, C.A.V., Verweij, J., Kamermans, K., Müller, L.J., Ruijter, J.M., Vrensen, G.F.J.M., & Spekreijse, H. (1996). Clearance of neurotransmitter from the cone synaptic cleft in goldfish retina. Vision Research 36, 3859–3874.CrossRefGoogle Scholar
Verweij, J., Kamermans, M., van den Aker, C., & Spekreijse, H. (1996). Modulation of horizontal cell receptive fields in the light adapted goldfish retina. Vision Research 36, 3913–3923.CrossRefGoogle Scholar
Weiler, R., He, S., & Vaney, D.I. (1999). Retinoic acid modulates gap junctional permeability between horizontal cells of the mammalian retina. European Journal of Neuroscience 11, 3346–3350.CrossRefGoogle Scholar
Weiler, R., Pottek, M., He, S., & Vaney, D.I. (2000). Modulation of coupling between retinal horizontal cells by retinoic acid and endogenous dopamine. Brain Research Reviews 32, 121–129.CrossRefGoogle Scholar
Winslow, R.L. (1989). Bifurcation analysis of nonlinear retina horizontal cell models I. properties of isolated cells. Journal of Neurophysiology 62, 738–749.Google Scholar
Xin, D. & Bloomfield, S.A. (1999). Dark- and light-induced changes in coupling between horizontal cells in mammalian retina. Journal of Comparative Neurology 405, 75–87.3.0.CO;2-D>CrossRefGoogle Scholar
Yagi, T. & Kaneko, A. (1987). Membrane properties and the signal conduction of the horizontal cell syncytium of the teleost retina. Neuroscience Research (Suppl.) 6, S119–S132.Google Scholar
Yagi, T. & Kaneko, A. (1988). The axon terminal of goldfish retina horizontal cells: A low membrane conductance measured in solitary preparations and its implication to the signal conduction from the soma. Journal of Neurophysiology 59, 482–494.Google Scholar
Yasui, S. (1987). Ca and Na homeostasis in horizontal cells of the cyprinid fish retina: evidence for Na–Ca exchanger and Na-K pump. Neuroscience Research (Suppl.) 6, S133–S146.Google Scholar
Zhou, Z. & Neher, E. (1993). Mobile and immobile calcium buffers in bovine adrenal chromaffin cells. Journal of Physiology 469, 245–273.CrossRefGoogle Scholar