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Postsynaptic calcium feedback between rods and rod bipolar cells in the mouse retina

Published online by Cambridge University Press:  25 February 2005

AMY BERNTSON ,
ROBERT G. SMITH  and
W. ROWLAND TAYLOR
AMY BERNTSON
Affiliation:
John Curtin School of Medical Research and Centre for Visual Sciences, Australian National University, Canberra, Australia
ROBERT G. SMITH
Affiliation:
Department of Neuroscience, University of Pennsylvania, Philadelphia
W. ROWLAND TAYLOR
Affiliation:
John Curtin School of Medical Research and Centre for Visual Sciences, Australian National University, Canberra, Australia Neurological Sciences Institute, Oregon Health and Sciences University, Beaverton
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Abstract

Light-evoked currents were recorded from rod bipolar cells in a dark-adapted mouse retinal slice preparation. Low-intensity light steps evoked a sustained inward current. Saturating light steps evoked an inward current with an initial peak that inactivated, with a time constant of about 60–70 ms, to a steady plateau level that was maintained for the duration of the step. The inactivation was strongest at hyperpolarized potentials, and absent at positive potentials. Inactivation was mediated by an increase in the intracellular calcium concentration, as it was abolished in cells dialyzed with 10 mM BAPTA, but was present in cells dialyzed with 1 mM EGTA. Moreover, responses to brief flashes of light were broader in the presence of intracellular BAPTA indicating that the calcium feedback actively shapes the time course of the light responses. Recovery from inactivation observed for paired-pulse stimuli occurred with a time constant of about 375 ms. Calcium feedback could act to increase the dynamic range of the bipolar cells, and to reduce variability in the amplitude and duration of the single-photon signal. This may be important for nonlinear processing at downstream sites of convergence from rod bipolar cells to AII amacrine cells. A model in which intracellular calcium rapidly binds to the light-gated channel and reduces the conductance can account for the results.

Keywords

Calcium feedbackMetabotropic synapseRetinal neuronsRod bipolar cellScotopic signalsVisual system
Type
Research Article
Information
Visual Neuroscience , Volume 21 , Issue 6 , November 2004 , pp. 913 - 924
Copyright
© 2004 Cambridge University Press

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References

REFERENCES

Barlow, H.B., Levick, W.R., & Yoon, M. (1971). Responses to single quanta of light in retinal ganglion cells of the cat. Vision Research (Suppl) 3, 87–101.Google Scholar
Baylor, D.A., Nunn, B.J., & Schnapf, J.L. (1984). The photocurrent, noise and spectral sensitivity of rods of the monkey Macaca fascicularis. Journal of Physiology 357, 575–607.Google 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.Google Scholar
Berntson, A., Smith, R.G., & Taylor, W.R. (2003). Transmission of single photon signals through a binary synapse in the mammalian retina. Visual Neuroscience 20, 621–626.Google Scholar
Bloomfield, S.A. & Dacheux, R.F. (2001). Rod vision: Pathways and processing in the mammalian retina. Progress in Retinal Eye Research 20, 351–384.Google Scholar
Dacheux, R. & Raviola, E. (1986). The rod pathway in the rabbit retina: a depolarizing bipolar and amacrine cell. Journal of Neuroscience 6, 331–345.Google Scholar
DeVries, S. & Baylor, D. (1995). An alternative pathway for signal flow from rod photoreceptors to ganglion cells in mammalian retina. Proceedings of the National Academy of Sciences of the U.S.A. 92, 10658–10662.Google Scholar
Dhingra, A., Lyubarsky, A., Jiang, M., Pugh, E.N., Jr., Birnbaumer, L., Sterling, P., & Vardi, N. (2000). The light response of ON bipolar neurons requires G[alpha]o. Journal of Neuroscience 20, 9053–9058.Google Scholar
Dhingra, A., Jiang, M., Wang, T.L., Lyubarsky, A., Savchenko, A., Bar-Yehuda, T., Sterling, P., Birnbaumer, L., & Vardi, N. (2002). Light response of retinal ON bipolar cells requires a specific splice variant of Galpha(o). Journal of Neuroscience 22, 4878–4884.Google 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
Field, G.D. & Rieke, F. (2002a). Nonlinear signal transfer from mouse rods to bipolar cells and implications for visual sensitivity. Neuron 34, 773–785.Google Scholar
Field, G.D. & Rieke, F. (2002b). Mechanisms regulating variability of the single photon responses of mammalian rod photoreceptors. Neuron 35, 733–747.Google Scholar
Hack, I., Frech, M., Dick, O., Peichl, L., & Brandstatter, J.H. (2001). Heterogeneous distribution of AMPA glutamate receptor subunits at the photoreceptor synapses of rodent retina. European Journal of Neuroscience 13, 15–24.Google Scholar
Henry, D., Burke, S., Shishido, E., & Matthews, G. (2003). Retinal bipolar neurons express the cyclic nucleotide-gated channel of cone photoreceptors. Journal of Neurophysiology 89, 754–761.Google Scholar
Kamphuis, W., Dijk, F., & O'Brien, B.J. (2003). Gene expression of AMPA-type glutamate receptor subunits in rod-type ON bipolar cells of rat retina. European Journal of Neuroscience 18, 1085–1092.Google Scholar
Kolb, H. & Nelson, R. (1983). Rod pathways in the retina of the cat. Vision Research 23, 301–312.Google Scholar
Kuo, C.C. & Bean, B.P. (1994). Na+ channels must deactivate to recover from inactivation. Neuron 12, 819–829.Google Scholar
Mastronarde, D.N. (1983). Correlated firing of cat retinal ganglion cells. II. Responses of X- and Y-cells to single quantal events. Journal of Neurophysiology 49, 325–349.Google Scholar
Masu, M., Iwakabe, H., Tagawa, Y., Miyoshi, T., Yamashita, M., Fukuda, Y., Sasaki, H., Hiroi, K., Nakamura, Y., Shigemoto, R. al e (1995). Specific deficit of the ON response in visual transmission by targeted disruption of the mGluR6 gene. Cell 80, 757–765.Google Scholar
Nawy, S. (1999). The metabotropic receptor mGluR6 may signal through G(o), but not phosphodiesterase, in retinal bipolar cells. Journal of Neuroscience 19, 2938–2944.Google Scholar
Nawy, S. (2000). Regulation of the on bipolar cell mGluR6 pathway by Ca2+. Journal of Neuroscience 20, 4471–4479.Google Scholar
Nawy, S.A. (2004). Desensitization of the mGluR6 transduction current in tiger salamander on bipolar cells. Journal of Physiology 558, 137–146.Google Scholar
Nawy, S. & Jahr, C.E. (1990). Suppression by glutamate of cGMP-activated conductance in retinal bipolar cells. Nature 346, 269–271.Google Scholar
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, 109–135.Google Scholar
Nikonov, S., Engheta, N., & Pugh, E.N., Jr. (1998). Kinetics of recovery of the dark-adapted salamander rod photoresponse. Journal of General Physiology 111, 7–37.Google Scholar
Penn, R. & Hagins, W. (1972). Kinetics of the photocurrent of retinal rods. Biophysical Journal 12, 1073–1094.Google Scholar
Rieke, F. & Baylor, D.A. (1998). Origin of reproducibility in the responses of retinal rods to single photons. Biophysical Journal 75, 1836–1857.Google Scholar
Robson, J.G. & Frishman, L.J. (1995). Response linearity and kinetics of the cat retina: The bipolar cell component of the dark-adapted electroretinogram. Visual Neuroscience 12, 837–850.Google Scholar
Robson, J.G., Maeda, H., Saszik, S., & Frishman, L.J. (2004). In vivo studies of signaling in rod pathways using the electroretinogram. Vision Research 44, 3253–3268.Google Scholar
Schneeweis, D. & Schnapf, J. (1995). Photovoltage of rods and cones in the macaque retina. Science 268, 1053–1056.Google Scholar
Sharpe, L.T. & Stockman, A. (1999). Rod pathways: the importance of seeing nothing. Trends in Neuroscience 22, 497–504.Google Scholar
Shiells, R.A. & Falk, G. (1990). Glutamate receptors of rod bipolar cells are linked to a cyclic GMP cascade via a G-protein. Proceedings of the Royal Society B (London) 242, 91–94.Google Scholar
Shiells, R.A. & Falk, G. (1992a). Properties of the cGMP-activated channel of retinal on-bipolar cells. Proceedings of the Royal Society B (London) 247, 21–25.Google Scholar
Shiells, R.A. & Falk, G. (1992b). The glutamate-receptor linked cGMP cascade of retinal on-bipolar cells is pertussis and cholera toxin-sensitive. Proceedings of the Royal Society B (London) 247, 17–20.Google Scholar
Shiells, R.A. & Falk, G. (1994). Responses of rod bipolar cells isolated from dogfish retinal slices to concentration-jumps of glutamate. Visual Neuroscience 11, 1175–1183.Google Scholar
Shiells, R.A. & Falk, G. (1999). A rise in intracellular Ca2+ underlies light adaptation in dogfish retinal ‘on’ bipolar cells. Journal of Physiology (London) 514 (Pt. 2), 343–350.Google Scholar
Shiells, R.A. & Falk, G. (2000). Activation of Ca2+–calmodulin kinase II induces desensitization by background light in dogfish retinal ‘on’ bipolar cells. Journal of Physiology 528, 327–338.Google Scholar
Singer, J. & Diamond, J.S. (2003). Sustained Ca2+ entry elicits transient postsynaptic currents at a retinal ribbon synapse. Journal of Neuroscience 23, 10923–10933.Google Scholar
Slaughter, M.M. & Miller, R.F. (1981). 2-amino-4-phosphonobutyric acid: a new pharmacological tool for retina research. Science 211, 182–185.Google Scholar
Smith, R. & Vardi, N. (1995). Simulation of the AII amacrine cell of mammalian retina: functional consequences of electrical coupling and regenerative membrane properties. Visual Neuroscience 12, 851–860.Google Scholar
Smith, R.G. (1992). NeuronC: A computational language for investigating functional architecture of neural circuits. Journal of Neuroscience Methods 43, 83–108.Google Scholar
Smith, R.G., Freed, M.A., & Sterling, P. (1986). Microcircuitry of the dark-adapted cat retina: Functional architecture of the rod-cone network. Journal of Neuroscience 6, 3505–3517.Google Scholar
Snellman, J. & Nawy, S. (2002). Regulation of the retinal bipolar cell mGluR6 pathway by calcineurin. Journal of Neurophysiology 88, 1088–1096.Google Scholar
Soucy, E., Wang, Y., Nirenberg, S., Nathans, J., & Meister, M. (1998). A novel signaling pathway from rod photoreceptors to ganglion cells in mammalian retina. Neuron 21, 481–493.Google Scholar
Sterling, P., Freed, M.A., & Smith, R.G. (1988). Architecture of rod and cone circuits to the on-beta ganglion cell. Journal of Neuroscience 8, 623–642.Google Scholar
Strettoi, E., Dacheux, R., & Raviola, E. (1990). Synaptic connections of rod bipolar cells in the inner plexiform layer of the rabbit retina. Journal of Comparative Neurology 295, 449–466.Google Scholar
Strettoi, E., Raviola, E., & Dacheux, R.F. (1992). Synaptic connections of the narrow-field, bistratified rod amacrine cell (AII) in the rabbit retina. Journal of Comparative Neurology 325, 152–168.Google Scholar
Tamura, T., Nakatani, K., & Yau, K.W. (1989). Light adaptation in cat retinal rods. Science 245, 755–758.Google Scholar
Tsukamoto, Y., Morigiwa, K., Ueda, M., & Sterling, P. (2001). Microcircuits for night vision in mouse retina. Journal of Neuroscience 21, 8616–8623.Google Scholar
van Rossum, M.C. & Smith, R.G. (1998). Noise removal at the rod synapse of mammalian retina. Visual Neuroscience 15, 809–821.Google Scholar
Vaney, D.I., Young, H.M., & Gynther, I.C. (1991). The rod circuit of the rabbit retina. Visual Neuroscience 7, 141–154.Google Scholar
Vardi, N. (1998). Alpha subunit of Go localizes in the dendritic tips of ON bipolar cells. Journal of Comparative Neurology 395, 43–52.Google Scholar
Vardi, N., Duvoisin, R., Wu, G., & Sterling, P. (2000). Localization of mGluR6 to dendrites of ON bipolar cells in primate retina. Journal of Comparative Neurology 423, 402–412.Google Scholar
Wässle, H., Yamashita, M., Greferath, U., Grünert, U., & Müller, F. (1991). The rod bipolar cell of the mammalian retina. Visual Neuroscience 7, 99–112.Google Scholar
Whitlock, G.G. & Lamb, T.D. (1999). Variability in the time course of single photon responses from toad rods: Termination of rhodopsin's activity. Neuron 23, 337–351.Google Scholar
Wilson, M., Tessier-Lavigne, M., & Attwell, D. (1987). Noise analysis predicts at least four states for channels closed by glutamate. Biophysical Journal 52, 955–960.Google Scholar
Yamashita, M. & Wässle, H. (1991). Responses of rod bipolar cells isolated from the rat retina to the glutamate agonist 2-amino-4-phosphonobutyric acid (APB). Journal of Neuroscience 11, 2372–2382.Google Scholar