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Cone synapses in macaque fovea: II. Dendrites of OFF midget bipolar cells exhibit Inner Densities similar to their Outer synaptic Densities in basal contacts with cone terminals

Published online by Cambridge University Press:  28 January 2011

STEVE HERR ,
IVY TRAN NGO ,
TERESA M. HUANG ,
KARL KLUG ,
PETER STERLING  and
STAN SCHEIN
STEVE HERR
Affiliation:
Department of Psychology, Franz Hall, University of California, Los Angeles, Los Angeles, California
IVY TRAN NGO
Affiliation:
Department of Psychology, Franz Hall, University of California, Los Angeles, Los Angeles, California
TERESA M. HUANG
Affiliation:
Department of Psychology, Franz Hall, University of California, Los Angeles, Los Angeles, California
KARL KLUG
Affiliation:
Brain Research Institute, University of California, Los Angeles, Los Angeles, California
PETER STERLING
Affiliation:
Department of Neuroscience, University of Pennsylvania, Philadelphia, Pennsylvania
STAN SCHEIN*
Affiliation:
Department of Psychology, Franz Hall, University of California, Los Angeles, Los Angeles, California Brain Research Institute, University of California, Los Angeles, Los Angeles, California California NanoSystems Institute, University of California, Los Angeles, Los Angeles, California
*
*Address correspondence and reprint requests to: Stan Schein, Department of Psychology, Franz Hall, Mailcode 951563, University of California, Los Angeles, Los Angeles, CA 90095-1563. E-mail: [email protected]
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Abstract

As described in the companion paper, the synaptic terminal of a cone photoreceptor in macaque monkey makes an average of 35 or 46 basal contacts with the tips of the dendrites of its OFF midget bipolar cell. Each basal contact has one or more symmetrically thickened dense regions. These “Outer Densities,” averaging 48 or 67 in number, harbor clusters of ionotropic glutamate receptors and are ~0.8 μm (and ~1-ms diffusion time) from active zones associated with synaptic ribbons. Here, we show similarly appearing “Inner Densities,” averaging 53 or 74 in number, located more proximally on the dendrites of these OFF midget bipolar cells, ~0.4 μm inward from the tips of the dendrites and out of contact with the basal surface of the cone terminal. Compared to desmosome-like junctions, Inner Densities are closer to the terminal and are less dense and less thick. Each Inner Density is shared with another cell, the partners including diffuse bipolar cells, ON midget bipolar cells, and horizontal cells. Given the diversity of the partners, the OFF midget bipolar cells are unlikely to be in a synaptic relationship with the partners. Instead, Inner Densities are near enough to the active zones associated with synaptic ribbons to receive pulses of glutamate at concentrations effective for glutamate receptors. The role of Inner Densities is not known, but they might represent additional clusters of glutamate receptors.

Keywords

PrimatePhotoreceptorRetinaPedicleVision
Type
Research Article
Information
Visual Neuroscience , Volume 28 , Issue 1 , January 2011 , pp. 17 - 28
Copyright
Copyright © Cambridge University Press 2011

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References

Ahmad, K.M., Klug, K., Herr, S., Sterling, P. & Schein, S. (2003). Cell density ratios in a foveal patch in macaque retina. Visual Neuroscience 20, 189–209.CrossRefGoogle Scholar
Boycott, B.B. & Dowling, J.E. (1969). Organization of the primate retina: Light microscopy. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 255, 109–176.Google Scholar
Boycott, B.B. & Hopkins, J.M. (1991). Cone bipolar cells and cone synapses in the primate retina. Visual Neuroscience 7, 49–60.CrossRefGoogle ScholarPubMed
Boycott, B.B. & Hopkins, J.M. (1993). Cone synapses of a flat diffuse cone bipolar cell in the primate retina. Journal of Neurocytology 22, 765–778.CrossRefGoogle ScholarPubMed
Boycott, B.B. & Wässle, H. (1991). Morphological classification of bipolar cells of the primate retina. The European Journal of Neuroscience 3, 1069–1088.CrossRefGoogle ScholarPubMed
Brandstätter, J.H. & Hack, I. (2001). Localization of glutamate receptors at a complex synapse. The mammalian photoreceptor synapse. Cell and Tissue Research 303, 1–14.CrossRefGoogle Scholar
Brandstätter, J.H., Koulen, P. & Wässle, H. (1997). Selective synaptic distribution of kainate receptor subunits in the two plexiform layers of the rat retina. The Journal of Neuroscience 17, 9298–9307.CrossRefGoogle ScholarPubMed
Calkins, D., Schein, S., Tsukamoto, Y. & Sterling, P. (1994). M and L cones in macaque fovea connect to midget ganglion cells by different numbers of excitatory synapses. Nature 371, 70–72.CrossRefGoogle ScholarPubMed
Calkins, D., Tsukamoto, Y. & Sterling, P. (1996). Foveal cones form basal as well as invaginating junctions with diffuse ON bipolar cells. Vision Research 36, 3373–3381.CrossRefGoogle ScholarPubMed
Chun, M., Grünert, U., Martin, P. & Wässle, H. (1996). The synaptic complex of cones in the fovea and in the periphery of the macaque monkey retina. Vision Research 36, 3373–3381.CrossRefGoogle ScholarPubMed
DeVries, S.H. (2000). Bipolar cells use kainate and AMPA receptors to filter visual information into separate channels. Neuron 28, 847–856.CrossRefGoogle ScholarPubMed
DeVries, S.H., Li, W. & Saszik, S. (2006). Parallel processing in two transmitter microenvironments at the cone photoreceptor synapse. Neuron 50, 735–748.CrossRefGoogle ScholarPubMed
Dowling, J.E. (1987). The Retina: An Approachable Part of the Brain. Cambridge, MA: Harvard University Press.Google Scholar
Dowling, J.E. & Boycott, B.B. (1966) Organization of the primate retina: Electron microscopy. Proceedings of the Royal Society of London. Series B 166, 80–111.Google ScholarPubMed
Hack, I., Frech, M., Dick, O., Peichl, L. & Brandstätter, J.H. (2001). Heterogeneous distribution of AMPA glutamate receptor subunits at the photoreceptor synapses of rodent retina. The European Journal of Neuroscience 13, 15–24.CrossRefGoogle ScholarPubMed
Haverkamp, S., Grünert, U. & Wässle, H. (2000). The cone pedicle, a complex synapse in the retina. Neuron 27, 85–95.CrossRefGoogle ScholarPubMed
Haverkamp, S., Grünert, U. & Wässle, H. (2001 a). Localization of kainate receptors at the cone pedicles of the primate retina. The Journal of Comparative Neurology 436, 471–486.CrossRefGoogle ScholarPubMed
Haverkamp, S., Grünert, U. & Wässle, H. (2001 b). The synaptic architecture of AMPA receptors at the cone pedicle of the primate retina. The Journal of Neuroscience 21, 2488–2500.CrossRefGoogle ScholarPubMed
Heidelberger, R., Thoreson, W.B. & Witkovsky, P. (2005) Synaptic transmission at retinal ribbon synapses. Progress in Retinal and Eye Research 24, 682–720.CrossRefGoogle ScholarPubMed
Herr, S., Klug, K., Sterling, P. & Schein, S. (2003). Inner S-cone bipolar cells provide all of the central elements for S cones in macaque retina. The Journal of Comparative Neurology 457, 185–201.CrossRefGoogle ScholarPubMed
Hopkins, J.M. & Boycott, B.B. (1997). The cone synapses of cone bipolar cells of primate retina. Journal of Neurocytology 26, 313–325.CrossRefGoogle ScholarPubMed
Klug, K., Herr, S., Ngo, I.T., Sterling, P. & Schein, S. (2003). Macaque retina contains an S-cone OFF midget pathway. The Journal of Neuroscience 23, 9881–9887.CrossRefGoogle ScholarPubMed
Kolb, H. (1970). Organization of the outer plexiform layer of the primate retina: Electron microscopy of Golgi-impregnated cells. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 258, 261–283.Google ScholarPubMed
Kolb, H., Boycott, B.B. & Dowling, J.E. (1969). A second type of midget bipolar cell in the primate retina. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 255, 177–184.Google Scholar
Lenzi, D. & von Gersdorff, H. (2001) Structure suggests function: The case for synaptic ribbons as exocytotic nanomachines. BioEssays 23, 831–840.CrossRefGoogle ScholarPubMed
Li, W. & DeVries, S.H. (2006). Bipolar cell pathways for color and luminance vision in a dichromatic mammalian retina. Nature Neuroscience 9, 669–675.CrossRefGoogle Scholar
Meyers, D., Skinner, S. & Sloan, K. (1992). Surfaces from contours. ACM Transactions on Graphics 11, 228–258.CrossRefGoogle Scholar
Migdale, K., Herr, S., Klug, K., Ahmad, K., Linberg, K., Sterling, P. & Schein, S. (2003). Two ribbon synaptic units in rod photoreceptors of macaque, human, and cat. The Journal of Comparative Neurology 455, 100–112.CrossRefGoogle ScholarPubMed
Morigiwa, K. & Vardi, N. (1999). Differential expression of ionotropic glutamate receptor subunits in the outer retina. The Journal of Comparative Neurology 405, 173–184.3.0.CO;2-L>CrossRefGoogle ScholarPubMed
Nelson, R. & Kolb, H. (1983). Synaptic patterns and response properties of bipolar and ganglion cells in the cat retina. Vision Research 23, 1183–1195.CrossRefGoogle ScholarPubMed
Nomura, A.R., Shigemoto, Y., Nakamura, N., Okamoto, N., Mizuno, N. & Nakanishi, S. (1994). Developmentally-regulated postsynaptic localization of a metabotropic glutamate-receptor in rat rod bipolar cells. Cell 77, 361–369.CrossRefGoogle ScholarPubMed
Puller, C., Haverkamp, S. & Grünert, U. (2007). OFF midget bipolar cells in the retina of the marmoset, Callithrix jacchus, express AMPA receptors. The Journal of Comparative Neurology 20, 442–454.CrossRefGoogle Scholar
Qin, P. & Pourcho, R.G. (1999). Localization of AMPA-selective glutamate receptor subunits in the cat retina: A light- and electron-microscopic study. Visual Neuroscience 16, 169–177.CrossRefGoogle ScholarPubMed
Rao-Mirotznik, R., Buchsbaum, G. & Sterling, P. (1998). Transmitter concentration at a three-dimensional synapse. Journal of Neurophysiology 80, 3163–3172.CrossRefGoogle Scholar
Raviola, E. & Gilula, N.B. (1975). Intramembrane organization of specialized contacts in the outer plexiform layer of the retina. A freeze-fracture study in monkeys and rabbits. The Journal of Cell Biology 65, 192–222.CrossRefGoogle ScholarPubMed
Schein, S. & Ahmad, K.M. (2005). A clockwork hypothesis: Synaptic release by rod photoreceptors must be regular. Biophysical Journal 89, 3931–3949.CrossRefGoogle ScholarPubMed
Schein, S. & Ahmad, K.M. (2006) Efficiency of synaptic transmission of single-photoreceptor to rod bipolar dendrite. Biophysical Journal 91, 3257–3267.CrossRefGoogle Scholar
Schein, S., Ngo, I.T., Huang, T.M., Klug, K., Sterling, P. & Herr, S. (2011) Cone synapses in macaque fovea: I. Two types of non-S cones are distinguished by numbers of contacts with OFF midget bipolar cells. Visual Neuroscience, 28, xxx–xxx.CrossRefGoogle ScholarPubMed
Schein, S., Sterling, P., Ngo, I.-T., Huang, T.M. & Herr, S. (2004). Evidence that each S cone in macaque fovea drives one narrow-field and several wide-field blue-yellow ganglion cells. The Journal of Neuroscience 24, 8366–8378.CrossRefGoogle ScholarPubMed
Smith, R.G. (1987). Montage: A system for three-dimensional reconstruction by personal computer. Journal of Neuroscience Methods 21, 55–69.CrossRefGoogle ScholarPubMed
Tsukamoto, Y., Masarachia, P., Schein, S. & Sterling, P. (1992). Gap junctions between the terminals of macaque foveal cones. Vision Research 32, 1809–1815.CrossRefGoogle ScholarPubMed
Vardi, N., Duvoisin, R., Wu, G. & Sterling, P. (2000). Localization of mGluR6 to dendrites of ON bipolar cells in primate retina. The Journal of Comparative Neurology 423, 402–412.3.0.CO;2-E>CrossRefGoogle Scholar
Vardi, N., Morigiwa, K., Wang, T.L., Shi, Y.J. & Sterling, P. (1998). Neurochemistry of the mammalian cone ‘synaptic complex’. Vision Research 38, 1359–1369.CrossRefGoogle ScholarPubMed
Wässle, H., Haverkamp, S., Grünert, U. & Morgans, C.W. (2003). The cone pedicle, the first synapse in the retina. In The Neural Basis of Early Vision, ed. Kaneko, A., pp. 19–38. Tokyo, Japan: Springer-Verlag.CrossRefGoogle Scholar
Wolfson, E. & Schwartz, E.L. (1989). Computing minimal distances on arbitrary polyhedral surfaces. IEEE Transactions on Pattern Analysis and Machine Intelligence 11, 1001–1005.CrossRefGoogle Scholar