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

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.

[1]  S. Schein,et al.  Cone synapses in macaque fovea: I. Two types of non-S cones are distinguished by numbers of contacts with OFF midget bipolar cells , 2011, Visual Neuroscience.

[2]  S. Haverkamp,et al.  OFF midget bipolar cells in the retina of the marmoset, Callithrix jacchus, express AMPA receptors , 2007, The Journal of comparative neurology.

[3]  Kareem M. Ahmad,et al.  Efficiency of synaptic transmission of single-photon events from rod photoreceptor to rod bipolar dendrite. , 2006, Biophysical journal.

[4]  Wei Li,et al.  Parallel Processing in Two Transmitter Microenvironments at the Cone Photoreceptor Synapse , 2006, Neuron.

[5]  S. DeVries,et al.  Bipolar cell pathways for color and luminance vision in a dichromatic mammalian retina , 2006, Nature Neuroscience.

[6]  Kareem M. Ahmad,et al.  A clockwork hypothesis: synaptic release by rod photoreceptors must be regular. , 2005, Biophysical journal.

[7]  Wallace B. Thoreson,et al.  Synaptic transmission at retinal ribbon synapses , 2005, Progress in Retinal and Eye Research.

[8]  S. Schein,et al.  Evidence That Each S Cone in Macaque Fovea Drives One Narrow-Field and Several Wide-Field Blue-Yellow Ganglion Cells , 2004, The Journal of Neuroscience.

[9]  S. Schein,et al.  Macaque Retina Contains an S-Cone OFF Midget Pathway , 2003, The Journal of Neuroscience.

[10]  S. Schein,et al.  Inner S‐cone bipolar cells provide all of the central elements for S cones in macaque retina , 2003, The Journal of comparative neurology.

[11]  Kareem M. Ahmad,et al.  Cell density ratios in a foveal patch in macaque retina , 2003, Visual Neuroscience.

[12]  Kareem M. Ahmad,et al.  Two ribbon synaptic units in rod photoreceptors of macaque, human, and cat , 2003, The Journal of comparative neurology.

[13]  H. Wässle,et al.  The Cone Pedicle, the First Synapse in the Retina , 2003 .

[14]  A. Kaneko The Neural Basis of Early Vision , 2003, Keio University International Symposia for Life Sciences and Medicine.

[15]  H. von Gersdorff,et al.  Structure suggests function: the case for synaptic ribbons as exocytotic nanomachines , 2001, BioEssays : news and reviews in molecular, cellular and developmental biology.

[16]  Heinz Wässle,et al.  Localization of kainate receptors at the cone pedicles of the primate retina , 2001, The Journal of comparative neurology.

[17]  H. Wässle,et al.  The Synaptic Architecture of AMPA Receptors at the Cone Pedicle of the Primate Retina , 2001, The Journal of Neuroscience.

[18]  L. Peichl,et al.  Heterogeneous distribution of AMPA glutamate receptor subunits at the photoreceptor synapses of rodent retina , 2001, The European journal of neuroscience.

[19]  S. DeVries,et al.  Bipolar Cells Use Kainate and AMPA Receptors to Filter Visual Information into Separate Channels , 2000, Neuron.

[20]  P Sterling,et al.  Localization of mGluR6 to dendrites of ON bipolar cells in primate retina , 2000, The Journal of comparative neurology.

[21]  Heinz Wässle,et al.  The Cone Pedicle, a Complex Synapse in the Retina , 2000, Neuron.

[22]  J. Brandstätter,et al.  Localization of glutamate receptors at a complex synapse , 2000, Cell and Tissue Research.

[23]  N. Vardi,et al.  Differential expression of ionotropic glutamate receptor subunits in the outer retina , 1999, The Journal of comparative neurology.

[24]  R. Pourcho,et al.  Localization of AMPA-selective glutamate receptor subunits in the cat retina: A light- and electron-microscopic study , 1999, Visual Neuroscience.

[25]  G Buchsbaum,et al.  Transmitter concentration at a three-dimensional synapse. , 1998, Journal of neurophysiology.

[26]  Peter Sterling,et al.  Neurochemistry of the mammalian cone `synaptic complex' , 1998, Vision Research.

[27]  H. Wässle,et al.  Selective Synaptic Distribution of Kainate Receptor Subunits in the Two Plexiform Layers of the Rat Retina , 1997, The Journal of Neuroscience.

[28]  B. Boycott,et al.  The cone synapses of cone bipolar cells of primate retina , 1997, Journal of neurocytology.

[29]  Paul R. Martin,et al.  The Synaptic Complex of Cones in the Fovea and in the Periphery of the Macaque Monkey Retina , 1996, Vision Research.

[30]  P. Sterling,et al.  Foveal Cones form Basal as well as Invaginating Junctions with Diffuse ON Bipolar Cells , 1996, Vision Research.

[31]  David J. Calkins,et al.  M and L cones in macaque fovea connect to midget ganglion cells by different numbers of excitatory synapses , 1994, Nature.

[32]  Shigetada Nakanishi,et al.  Developmentally regulated postsynaptic localization of a metabotropic glutamate receptor in rat rod bipolar cells , 1994, Cell.

[33]  B. Boycott,et al.  Cone synapses of a flat diffuse cone bipolar cell in the primate retina , 1993, Journal of neurocytology.

[34]  Peter Sterling,et al.  Gap junctions between the pedicles of macaque foveal cones , 1992, Vision Research.

[35]  Kenneth R. Sloan,et al.  Surfaces from contours , 1992, TOGS.

[36]  B. Boycott,et al.  Morphological Classification of Bipolar Cells of the Primate Retina , 1991, The European journal of neuroscience.

[37]  B. Boycott,et al.  Cone bipolar cells and cone synapses in the primate retina , 1991, Visual Neuroscience.

[38]  Eric L. Schwartz,et al.  Computing Minimal Distances on Polyhedral Surfaces , 1989, IEEE Trans. Pattern Anal. Mach. Intell..

[39]  D. Puro The Retina. An Approachable Part of the Brain , 1988 .

[40]  Robert G. Smith Montage: a system for three-dimensional reconstruction by personal computer , 1987, Journal of Neuroscience Methods.

[41]  Helga Kolb,et al.  Synaptic patterns and response properties of bipolar and ganglion cells in the cat retina , 1983, Vision Research.

[42]  E. Raviola,et al.  Intramembrane organization of specialized contacts in the outer plexiform layer of the retina. A freeze-fracture study in monkeys and rabbits , 1975, The Journal of cell biology.

[43]  H. Kolb,et al.  Organization of the outer plexiform layer of the primate retina: electron microscopy of Golgi-impregnated cells. , 1970, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[44]  B. Boycott,et al.  Organization of the Primate Retina: Light Microscopy , 1969 .

[45]  B. Boycott,et al.  Organization of the primate retina: electron microscopy , 1966, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[46]  T. ATION COMPUTING MINIMAL DISTANCES ON ARBITRARY POLYHEDRAL SURFACES , .