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Heterogeneous expression of voltage-dependent Na+ and K+ channels in mammalian retinal bipolar cells

Published online by Cambridge University Press:  02 June 2005

YU-PING MA ,
JINJUAN CUI  and
ZHUO-HUA PAN
YU-PING MA
Affiliation:
Department of Anatomy and Cell Biology, Wayne State University School of Medicine, Detroit
JINJUAN CUI
Affiliation:
Department of Anatomy and Cell Biology, Wayne State University School of Medicine, Detroit
ZHUO-HUA PAN
Affiliation:
Department of Anatomy and Cell Biology, Wayne State University School of Medicine, Detroit
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Abstract

Retinal bipolar cells show heterogeneous expression of voltage-dependent Na+ and K+ currents. We used whole-cell patch-clamp recordings to investigate the possible roles of these currents in the response properties of bipolar cells in rats. Isolated bipolar cells showed robust spontaneous regenerative activity, but the regenerative potential of rod bipolar cells reached a more depolarized level than that of cone bipolar cells. In both isolated cells and cells in retinal slices, the membrane depolarization evoked by current injection was apparently capped. The evoked membrane potential was again more depolarized in rod bipolar cells than in cone bipolar cells. Application of tetraethylammonium and 4-aminopyridine shifted the spontaneous regenerative potential as well as the evoked potential to a more depolarized level. In addition, a subclass of cone bipolar cells showed a prominent spike in the initial phase of the voltage response when the cells were depolarized from a relatively negative membrane potential. The spike was mediated mainly by tetrodotoxin-sensitive Na+ current. The presence of the spike sped up the response kinetics and enhanced the peak membrane potential. Results of this study raise the possibility that voltage-dependent K+ currents may play a role in defining different membrane operating ranges of rod and cone bipolar cells and that voltage-dependent Na+ currents may enhance the response kinetics and amplitude of certain cone bipolar cells.

Keywords

Voltage-dependent Na+ channelsVoltage-dependent K+ channelsCone bipolar cellsRod bipolar cellsRats
Type
Research Article
Information
Visual Neuroscience , Volume 22 , Issue 2 , March 2005 , pp. 119 - 133
Copyright
© 2005 Cambridge University Press

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References

REFERENCES

Attwell, D., Borges, S., Wu, S.M., & Wilson, M. (1987). Signal clipping by the rod output synapse. Nature 328, 522–524.CrossRefGoogle Scholar
Awatramani, G.B. & Slaughter, M.M. (2000). Origin of transient and sustained responses in ganglion cells of the retina. Journal of Neuroscience 20, 7087–7095.Google Scholar
Belgum, J.H. & Copenhagen, D.R. (1988). Synaptic transfer of rod signals to horizontal and bipolar cells in the retina of the toad (Bufo marinus). Journal of Physiology (London) 396, 225–245.CrossRefGoogle Scholar
Berntson, A. & Taylor, W.R. (2000). Response characteristics and receptive field widths of on-bipolar cells in the mouse retina. Journal of Physiology (London) 524, 879–889.CrossRefGoogle Scholar
Boycott, B.B. & Dowling, J.E. (1969). Organization of the primate retina: Light microscopy. Philosophical Transactions of the Royal Society B 255, 109–184.CrossRefGoogle Scholar
Boycott, B.B. & Kolb, H. (1973). The connections between the bipolar cells and photoreceptors in the retina of the domestic cat. Journal of Comparative Neurology 148, 91–114.CrossRefGoogle Scholar
Burrone, J. & Lagnado, L. (1997). Electrical resonance and calcium influx in the synaptic terminal of depolarizing bipolar cells from the goldfish retina. Journal of Physiology (London) 505, 571–584.CrossRefGoogle Scholar
Connaughton, V.P. & Maguire, G. (1998). Differential expression of voltage-gated K+ and Ca2+ currents in bipolar cells in the zebrafish retinal slice. European Journal of Neuroscience 10, 1350–1362.CrossRefGoogle Scholar
Cui, J., Ma, Y.-P., Lipton, S.A., & Pan, Z.-H. (2003). Glycine receptors and glycinergic synaptic input at the axon terminals of mammalian retinal rod bipolar cells. Journal of Physiology (London) 553, 895–909.CrossRefGoogle Scholar
Dacheux, R.F. & Raviola, E. (1986). The rod pathway in the rabbit retina: A depolarizing bipolar and amacrine cell. Journal of Neuroscience 6, 331–345.Google Scholar
de la Villa, P., Vaquero, C.F., & Kaneko, A. (1998). Two types of calcium currents of the mouse bipolar cells recorded in the retinal slice preparation. European Journal of Neuroscience 10, 317–323.CrossRefGoogle Scholar
Euler, T. & Wässle, H. (1995). Immunocytochemical identification of cone bipolar cells in the rat retina. Journal of Comparative Neurology 361, 461–478.CrossRefGoogle Scholar
Euler, T. & Masland, R.H. (2000). Light-evoked responses of bipolar cells in a mammalian retina. Journal of Neurophysiology 83, 1817–1829.Google Scholar
Famiglietti, E.V. (1981). Functional architecture of cone bipolar cells in mammalian retina. Vision Research 21, 1559–1564.CrossRefGoogle Scholar
Gillette, M.A. & Dacheux, R.F. (1995). GABA- and glycine-activated currents in the rod bipolar cell of the rabbit retina. Journal of Neurophysiology 74, 856–875.Google Scholar
Greferath, U., Grunert, U., & Wässle, H. (1990). Rod bipolar cells in the mammalian retina show protein kinase C-like immunoreactivity. Journal of Comparative Neurology 301, 433–422.CrossRefGoogle Scholar
Han, Y., Jacoby, R.A., & Wu, S.M. (2000). Morphological and electrophysiological properties of dissociated primate retinal cells. Brain Research 875, 175–186.CrossRefGoogle Scholar
Hartveit, E. (1996). Membrane currents evoked by ionotropic glutamate receptor agonists in rod bipolar cells in the rat retinal slice preparation. Journal of Neurophysiology 76, 401–422.Google Scholar
Hartveit, E. (1999). Reciprocal synaptic interactions between rod bipolar cells and amacrine cells in the rat retina. Journal of Neurophysiology 81, 2923–2936.Google Scholar
Hille, B. (1992). Ionic Channels of Excitable Membranes. Sunderland, Massachusetts: Sinauer Associates.
Hu, H.-J. & Pan, Z.-H. (2002). Differential expression of K+ currents in mammalian retinal bipolar cells. Visual Neuroscience 19, 163–173.CrossRefGoogle Scholar
Kaneko, A. (1970). Physiological and morphological identification of horizontal, bipolar and amacrine cells in goldfish retina. Journal of Physiology (London) 207, 623–633.CrossRefGoogle Scholar
Kaneko, A., Pinto, L.H., & Tachibana, M. (1989). Transient calcium current of retinal bipolar cells of the mouse. Journal of Physiology (London) 410, 613–629.CrossRefGoogle Scholar
Kaneko, A. & Tachibana, M. (1985). A voltage-clamp analysis of membrane currents in solitary bipolar cells dissociated from Carassius auratus. Journal of Physiology (London) 358, 131–152.CrossRefGoogle Scholar
Karschin, A. & Wässle, H. (1990). Voltage- and transmitter-gated currents in isolated rod bipolar cells of rat retina. Journal of Neurophysiology 63, 860–876.Google Scholar
Klumpp, D.J., Song, E.J., Ito, S., Sheng, M.H., Jan, L.Y., & Pinto, L.H. (1995a). The Shaker-like potassium channels of the mouse rod bipolar cell and their contributions to the membrane current. Journal of Neuroscience 15, 5004–5013.Google Scholar
Klumpp, D.J., Song, E.J., & Pinto, L.H. (1995b). Identification and localization of K+ channels in the mouse retina. Visual Neuroscience 12, 1177–1190.Google Scholar
Lasansky, A. (1992). Properties of depolarizing bipolar cell responses to central illumination in salamander retinal slices. Brain Research 576, 181–196.CrossRefGoogle Scholar
Lasater, E.M. (1988). Membrane currents of retinal bipolar cells in culture. Journal of Neurophysiology 60, 1460–1480.Google Scholar
Ma, Y.-P. & Pan, Z.-H. (2003). Spontaneous regenerative activity in mammalian retinal bipolar cells: Roles of multiple subtypes of voltage-dependent Ca2+ channels. Visual Neuroscience 20, 131–139.CrossRefGoogle Scholar
Mao, B.-Q., Macleish, P.R., & Victor, J.D. (1998). The intrinsic dynamics of retinal bipolar cells isolated from tiger salamander. Visual Neuroscience 15, 425–438.Google Scholar
Pan, Z.-H. (2000). Differential expression of high- and two types of low-voltage-activated calcium currents in rod and cone bipolar cells of the rat retina. Journal of Neurophysiology 83, 513–527.Google Scholar
Pan, Z.-H. & Hu, H.-J. (2000). Voltage-dependent Na+ currents in mammalian retinal cone bipolar cells. Journal of Neurophysiology, 84, 2564–2571.Google Scholar
Pourcho, R.G. & Goebel, D.J. (1987). A combined Golgi and autoradiographic study of 3H-glycine-accumulating cone bipolar cells in the cat retina. Journal of Neuroscience 7, 1178–1188.Google Scholar
Protti, D.A., Flores-Herr, N., & Von Gersdorff, H. (2000). Light evokes Ca2+ spikes in the axon terminal of a retinal bipolar cell. Neuron 25, 215–227.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.CrossRefGoogle Scholar
Tessier-Lavigne, M., Attwell, D., Mobbs, P., & Wilson, M. (1988). Membrane currents in retinal bipolar cells of the axolotl. Journal of General Physiology 91, 49–72.CrossRefGoogle Scholar
Werblin, F.S. (1978). Transmission along and between rods in the tiger salamander retina. Journal of Physiology (London) 280, 449–470.CrossRefGoogle Scholar
Werblin, F.S. & Dowling, J.E. (1969). Organization of the retina of the mudpuppy, Necturus maculosus. II. Intracellular recording. Journal of Neurophysiology 32, 339–355.Google Scholar
Wu, S.M., Gao, F., & Maple, B.R. (2000). Functional architecture of synapses in the inner retina: Segregation of visual signals by stratification of bipolar cell axon terminals. Journal of Neuroscience 20, 4462–4470.Google Scholar
Wu, S.M. & Yang, X.L. (1992). Modulation of synaptic gain by light. Proceedings of the National Academy of Sciences of the U.S.A. 89, 11755–11758.CrossRefGoogle Scholar
Yazulla, S. & Studholme, K.M. (1998). Differential distribution of Shaker-like and Shab-like K+-channel subunits in goldfish retina and retinal bipolar cells. Journal of Comparative Neurology 396, 131–140.3.0.CO;2-S>CrossRefGoogle Scholar
Zenisek, D. & Matthews, G. (1998). Calcium action potentials in retinal bipolar neurons. Visual Neuroscience 15, 69–75.CrossRefGoogle Scholar
Zenisek, D., Henry, D., Studholme, K., Yazulla, S., & Matthews, G. (2001). Voltage-dependent sodium channels are expressed in nonspiking retinal bipolar neurons. Journal of Neuroscience 21, 4543–4550.Google Scholar