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Transmission of single photon signals through a binary synapse in the mammalian retina

Published online by Cambridge University Press:  01 September 2004

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, Pennsylvania
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 & Sciences University, Beaverton, Oregon
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Abstract

At very low light levels the sensitivity of the visual system is determined by the efficiency with which single photons are captured, and the resulting signal transmitted from the rod photoreceptors through the retinal circuitry to the ganglion cells and on to the brain. Although the tiny electrical signals due to single photons have been observed in rod photoreceptors, little is known about how these signals are preserved during subsequent transmission to the optic nerve. We find that the synaptic currents elicited by single photons in mouse rod bipolar cells have a peak amplitude of 5–6 pA, and that about 20 rod photoreceptors converge upon each rod bipolar cell. The data indicates that the first synapse, between rod photoreceptors and rod bipolar cells, signals a binary event: the detection, or not, of a photon or photons in the connected rod photoreceptors. We present a simple model that demonstrates how a threshold nonlinearity during synaptic transfer allows transmission of the single photon signal, while rejecting the convergent neural noise from the 20 other rod photoreceptors feeding into this first synapse.

Keywords

VisionScotopicBipolar cellMouse retinamGluR6Electrophysiology
Type
Research Article
Information
Visual Neuroscience , Volume 21 , Issue 5 , September 2004 , pp. 693 - 702
Copyright
2004 Cambridge University Press

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References

REFERENCES

Ashmore, J.F. & Falk, G. (1980). The single-photon signal in rod bipolar cells of the dogfish retina. Journal of Physiology (London) 300, 151–166.Google Scholar
Ashmore, J.F. & Falk, G. (1982). An analysis of voltage noise in rod bipolar cells of the dogfish retina. Journal of Physiology (London) 332, 273–297.Google Scholar
Attwell, D., Borges, S., Wu, S.M., & Wilson, M. (1987). Signal clipping by the rod output synapse. Nature 328, 522–524.Google Scholar
Barlow, H.B. & Levick, W.R. (1976). Threshold setting by the surround of cat retinal ganglion cells. Journal of Physiology 259, 737–757.Google Scholar
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., Lamb, T.D., & Yau, K.W. (1979). Responses of retinal rods to single photons. Journal of Physiology (London) 288, 613–634.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
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 396, 225–245.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
Calvert, P.D., Govardovskii, V.I., Krasnoperova, N., Anderson, R.E., Lem, J., & Makino, C.L. (2001). Membrane protein diffusion sets the speed of rod phototransduction. Nature 411, 90–94.Google Scholar
Calvert, P.D., Krasnoperova, N.V., Lyubarsky, A.L., Isayama, T., Nicolo, M., Kosaras, B., Wong, G., Gannon, K.S., Margolskee, R.F., Sidman, R.L., Pugh, E.N., Jr., Makino, C.L., & Lem, J. (2000). Phototransduction in transgenic mice after targeted deletion of the rod transducin alpha-subunit. Proceedings of the National Academy of Sciences of the U.S.A. 97, 13913–13918.Google Scholar
Chun, M.H., Han, S.H., Chung, J.W., & Wässle, H. (1993). Electron microscopic analysis of the rod pathway of the rat retina. Journal of Comparative Neurology 332, 421–432.Google Scholar
Copenhagen, D.R., Hemila, S., & Reuter, T. (1990). Signal transmission through the dark-adapted retina of the toad (Bufo marinus). Gain, convergence, and signal/noise. Journal of General Physiology 95, 717–732.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
Daw, N., Jensen, R., & Brunken, W. (1990). Rod pathways in mammalian retinae. Trends in Neurosciences 13, 110–115.Google Scholar
Enroth-Cugell, C. & Lennie, P. (1975). The control of retinal ganglion cell discharge by receptive field surrounds. Journal of Physiology 247, 551–578.Google Scholar
Famiglietti, E.V.J. & Kolb, H. (1975). A bistratified amacrine cell and synaptic circuitry in the inner plexiform layer of the retina. Brain Research 84, 293–300.Google Scholar
Field, G.D. & Rieke, F. (2002). Nonlinear signal transfer from mouse rods to bipolar cells and implications for visual sensitivity. Neuron 34, 773–785.Google Scholar
Freed, M.A. (2000). Rate of quantal excitation to a retinal ganglion cell evoked by sensory input. Journal of Neurophysiology 83, 2956–2966.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
Hecht, S., Schlaer, S., & Pirenne, M. (1942). Energy, quanta and vision. Journal of General Physiology 25, 819–840.Google Scholar
Hetling, J.R. & Pepperberg, D.R. (1999). Sensitivity and kinetics of mouse rod flash responses determined in vivo from paired-flash electroretinograms. Journal of Physiology 516 (Pt 2), 593–609.Google Scholar
Kaplan, E., Marcus, S., & So, Y.T. (1979). Effects of dark adaptation on spatial and temporal properties of receptive fields in cat lateral geniculate nucleus. Journal of Physiology 294, 561–580.Google Scholar
Lamb, T.D. (1995). Photoreceptor spectral sensitivities: Common shape in the long-wavelength region. Vision Research 35, 3083–3091.Google Scholar
Levick, W., Thibos, L., Cohn, T., Catanzaro, D., & Barlow, H. (1983). Performance of cat retinal ganglion cells at low light levels. Journal of General Physiology 82, 405–426.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
Morgans, C.W. (1999). Calcium channel heterogeneity among cone photoreceptors in the tree shrew retina. European Journal of Neuroscience 11, 2989–2993.Google Scholar
Peichl, L. & Gonzalez-Soriano, J. (1994). Morphological types of horizontal cell in rodent retinae: A comparison of rat, mouse, gerbil, and guinea pig. Visual Neuroscience 11, 501–517.Google Scholar
Penn, R. & Hagins, W. (1972). Kinetics of the photocurrent of retinal rods. Biophysical Journal 12, 1073–1094.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., Harkins, A.B., Buchsbaum, G., & Sterling, P. (1995). Mammalian rod terminal: Architecture of a binary synapse. Neuron 14, 561–569.Google Scholar
Rieke, F. & Baylor, D. (1996). Molecular origin of continuous dark noise in rod photoreceptors. Biophysical Journal 71, 2553–2572.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
Sakitt, B. (1972). Counting every quantum. Journal of Physiology 223, 131–150.Google Scholar
Sakmann, B., Creutzfeldt, O., & Scheich, H. (1969). An experimental comparison between the ganglion cell receptive field and the receptive field of the adaptation pool in the cat retina. Pflugers Archive 307, 133–137.Google Scholar
Saszik, S.M., Robson, J.G., & Frishman, L.J. (2002). The scotopic threshold response of the dark-adapted electroretinogram of the mouse. Journal of Physiology 543, 899–916.Google Scholar
Schneeweis, D. & Schnapf, J. (1995). Photovoltage of rods and cones in the macaque retina. Science 268, 1053–1056.Google Scholar
Schneeweis, D.M. & Schnapf, J.L. (2000). Noise and light adaptation in rods of the macaque monkey. Visual Neuroscience 17, 659–666.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
Sieving, P.A., Frishman, L.J., & Steinberg, R.H. (1986). Scotopic threshold response of proximal retina in cat. Journal of Neurophysiology 56, 1049–1061.Google Scholar
Singer, J.H. & Diamond, J.S. (2003). Sustained Ca2+ entry elicits transient postsynaptic currents at a retinal ribbon synapse. Journal of Neuroscience 23, 10923–10933.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., 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
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
Taylor, W.R. & Morgans, C.W. (1998). Localization and properties of voltage-gated calcium channels in cone photoreceptors of Tupaia belangeri. Visual Neuroscience 15, 541–552.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
Wässle, H., Boycott, B., & Peichl, L. (1978). Receptor contacts of horizontal cells in the retina of the domestic cat. Proceedings of the Royal Society B (London) 203, 247–267.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
Wiesel, T.N. & Hubel, D.H. (1966). Spatial and chromatic interactions in the lateral geniculate body of the rhesus monkey. Journal of Neurophysiology 29, 1115–1156.Google Scholar
Wyszecki, G. & Stiles, W. (1967). Colour Science. New York: John Wiley & Sons, Inc.