Hostname: page-component-78c5997874-s2hrs Total loading time: 0 Render date: 2024-11-13T10:04:03.695Z Has data issue: false hasContentIssue false
  • English
  • Français

The unitary event amplitude of mouse retinal on-cone bipolar cells

Published online by Cambridge University Press:  30 March 2004

AMY BERNTSON  and
W. ROWLAND TAYLOR
AMY BERNTSON
Affiliation:
John Curtin School of Medical Research and Centre for Visual Sciences, Australian National University, Australia
W. ROWLAND TAYLOR
Affiliation:
John Curtin School of Medical Research and Centre for Visual Sciences, Australian National University, Australia
Get access Rights & Permissions [Opens in a new window]

Abstract

Light-evoked synaptic currents were recorded from on-cone bipolar cells in the mouse retina. Fluctuations in the synaptic current observed during maintained light steps were analyzed in order to estimate the amplitude of the underlying unitary event. The maximal synaptic current variance was 5-fold larger than the maximum expected from fluctuations in the number of active postsynaptic channels. Due to uncertainty in the contribution from channel variance, we calculated a range of values for the unitary event amplitude. The observed variance could be accounted for if 30–39 synaptic sites randomly generated unitary events with a waveform identical to the flash-response, and an amplitude of −3.1 to −2.4 pA. The amplitude is consistent with gating about five mGluR6 channels. The shape of the variance–mean relation suggests that in bright light transmitter release approaches zero, while in darkness transmitter release saturates the postsynaptic response. Thus the on-cone bipolar cell synapse is operating over its entire possible range. If it is assumed that the postsynaptic response saturates when one unitary event occurs per integration time, then a lower bound for the unitary event rate is 18 events/s/synaptic site. If the unitary event is generated by a single synaptic vesicle, the results suggest the total vesicle cycling rate available for encoding the on-cone bipolar cell signal is about 540–700 s−1.

Keywords

MouseRetinaBipolar cellsLight responsesNoise analysisWhole-cell voltage clamp
Type
Research Article
Information
Visual Neuroscience , Volume 20 , Issue 6 , November 2003 , pp. 621 - 626
Copyright
© 2003 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

Ashmore, J.F. & Copenhagen, D.R. (1980). Different postsynaptic events in two types of retinal bipolar cell. Nature 288, 84–86.Google Scholar
Ashmore, J.F. & Copenhagen, D.R. (1983). An analysis of transmission from cones to hyperpolarizing bipolar cells in the retina of the turtle. Journal of Physiology 300, 115–150.Google Scholar
Attwell, D., Mobbs, P., Tessier-Lavigne, M., & Wilson, M. (1987). Neurotransmitter-induced currents in retinal bipolar cells of the axolotl, Ambystoma mexicanum. Journal of Physiology 387, 125–161.Google Scholar
Bekkers, J.M. & Stevens, C.F. (1990). Presynaptic mechanism for long-term potentiation in the hippocampus. Nature 346, 724–729.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 (Pt. 3), 879–889.Google Scholar
Bialek, W. & Owen, W. (1990). Temporal filtering in retinal bipolar cells. Elements of an optimal computation? Biophysical Journal 58, 1227–1233.Google Scholar
Clements, J.D. (1996). Transmitter timecourse in the synaptic cleft: Its role in central synaptic function. Trends in Neuroscience 19, 163–171.Google Scholar
Clements, J.D. & Silver, R.A. (2000). Unveiling synaptic plasticity: A new graphical and analytical approach. Trends in Neuroscience 23, 105–113.Google Scholar
de la Villa, P., Kurahashi, T., & Kaneko, A. (1995). L-glutamate-induced responses and cGMP-activated channels in three subtypes of retinal bipolar cells dissociated from the cat. Journal of Neuroscience 15, 3571–3582.Google Scholar
DeVries, S.H. & Schwartz, E.A. (1999). Kainate receptors mediate synaptic transmission between cones and ‘Off’ bipolar cells in a mammalian retina. Nature 397, 157–160.Google Scholar
Dvorak, D. (1984). Off-pathway synaptic transmission in the outer retina of the axolotl is mediated by a kainic acid-preferring receptor. Neuroscience Letters 50, 7–11.Google Scholar
Hopkins, J. & Boycott, B. (1995). Synapses between cones and diffuse bipolar cells of a primate retina. Journal of Neurocytology 24, 680–694.Google Scholar
Jeon, C.J., Strettoi, E., & Masland, R.H. (1998). The major cell populations of the mouse retina. Journal of Neuroscience 18, 8936–8946.Google Scholar
Katz, B. & Miledi, R. (1970). Membrane noise produced by acetylcholine. Nature 226, 962–963.Google Scholar
Kolb, H. (1979). The inner plexiform layer in the retina of the cat: Electron microscopic observations. Journal of Neurocytology 8, 295–329.Google Scholar
Malinow, R. & Tsien, R.W. (1990). Presynaptic enhancement shown by whole-cell recordings of long-term potentiation in hippocampal slices. Nature 346, 177–180.Google Scholar
Miyamoto, M.D. (1975). Binomial analysis of quantal transmitter release at glycerol treated frog neuromuscular junctions. Journal of Physiology 250, 121–142.Google Scholar
Morgans, C.W. (2000). Neurotransmitter release at ribbon synapses in the retina. Immunology and Cell Biology 78, 442–446.Google Scholar
Nakajima, Y., Iwakabe, H., Akazawa, C., Nawa, H., Shigemoto, R., Mizuno, N., & Nakanishi, S. (1993). Molecular characterization of a novel retinal metabotropic glutamate receptor mGluR6 with a high agonist selectivity for L-2-amino-4-phosphonobutyrate. Journal of Biological Chemistry 268, 11868–11873.Google Scholar
Neves, G. & Lagnado, L. (1999). The kinetics of exocytosis and endocytosis in the synaptic terminal of goldfish retinal bipolar cells. Journal of Physiology 515 (Pt. 1), 181–202.Google Scholar
Peng, Y.W., Blackstone, C.D., Huganir, R.L., & Yau, K.W. (1995). Distribution of glutamate receptor subtypes in the vertebrate retina. Neuroscience 66, 483–497.Google Scholar
Rao, R., Buchsbaum, G., & Sterling, P. (1994). Rate of quantal transmitter release at the mammalian rod synapse. Biophysical Journal 67, 57–63.Google Scholar
Rao-Mirotznik, R., Buchsbaum, G., & Sterling, P. (1998). Transmitter concentration at a three-dimensional synapse. Journal of Neurophysiology 80, 3163–3172.Google Scholar
Rieke, F. & Schwartz, E. (1996). Asynchronous transmitter release: Control of exocytosis and endocytosis at the salamander rod synapse. Journal of Physiology 493 (Pt. 1), 1–8.Google Scholar
Rouze, N.C. & Schwartz, E.A. (1998). Continuous and transient vesicle cycling at a ribbon synapse. Journal Of Neuroscience 18, 8614–8624.Google Scholar
Schneeweis, D. & Schnapf, J. (1995). Photovoltage of rods and cones in the macaque retina. Science 268, 1053–1056.Google Scholar
Schultz, K., Goldman, D.J., Ohtsuka, T., Hirano, J., Barton, L., & Stell, W.K. (1997). Identification and localization of an immunoreactive AMPA-type glutamate receptor subunit (GluR4) with respect to identified photoreceptor synapses in the outer plexiform layer of goldfish retina. Journal of Neurocytology 26, 651–666.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
Sigworth, F.J. (1980). The variance of sodium current fluctuations at the node of Ranvier. Journal of Physiology 307, 97–129.Google Scholar
Simon, E.J., Lamb, T.D., & Hodgkin, A.L. (1975). Spontaneous voltage fluctuations in retinal cones and bipolar cells. Nature 256, 661–662.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
Van Rossum, M.C. & Smith, R.G. (1998). Noise removal at the rod synapse of mammalian retina. Visual Neuroscience 15, 809–821.Google Scholar
Vardi, N. & Morigiwa, K. (1997). ON cone bipolar cells in rat express the metabotropic receptor mGluR6. Visual Neuroscience 14, 789–794.Google Scholar
Von Gersdorff, H., Vardi, E., Matthews, G., & Sterling, P. (1996). Evidence that vesicles on the synaptic ribbon of retinal bipolar neurons can be rapidly released. Neuron 16, 1221–1227.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