The Cone Pedicle, a Complex Synapse in the Retina

Cone pedicles, the synaptic terminals of cone photoreceptors, are connected in the macaque monkey retina to several hundred postsynaptic dendrites. Using light and electron microscopy, we found underneath each cone pedicle a laminated distribution of dendritic processes of bipolar and horizontal cells. Superimposed were three strata of glutamate receptor (GluR) aggregates, including a novel layer of glutamate receptors clustered at desmosome-like junctions. They are, most likely, postsynaptic densities on horizontal cell dendrites. GABA(A) and GABA(C) receptors are aggregated on bipolar cell dendrites in a narrow band underneath the cone pedicle. Glutamate released from cone pedicles and GABA released from horizontal cell dendrites act not only through direct synaptic contacts but also (more so) through diffusion to the appropriate receptors.

[1]  L. Missotten,et al.  The ultrastructure of the human retina , 1965 .

[2]  P. Witkovsky,et al.  Dependence of photoreceptor glutamate release on a dihydropyridine-sensitive calcium channel , 1997, Neuroscience.

[3]  H. Wässle,et al.  Immunocytochemical localization of the synapse‐associated protein SAP102 in the rat retina , 1998, The Journal of comparative neurology.

[4]  Juliette Johnson,et al.  Multiple γ‐aminobutyric acid plasma membrane transporters GAT‐1, GAT‐2, GAT‐3 in the rat retina , 1996 .

[5]  E. A. Schwartz,et al.  A GABA transporter operates asymmetrically and with variable stoichiometry , 1994, Neuron.

[6]  豊田 順一 The retinal basis of vision , 1999 .

[7]  J. Pokorny,et al.  Horizontal cells reveal cone type-specific adaptation in primate retina. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[8]  S. Yazulla,et al.  Co-localization of Shaker A-type K+ channel (Kv1.4) and AMPA-glutamate receptor (GluR4) immunoreactivities to dendrites of OFF-bipolar cells of goldfish retina , 1999, Journal of neurocytology.

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

[10]  S. Archer,et al.  Neurobiology and Clinical Aspects of the Outer Retina , 1995, Springer Netherlands.

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

[12]  T. Südhof,et al.  Binding of neuroligins to PSD-95. , 1997, Science.

[13]  C. Morgans Calcium channel heterogeneity among cone photoreceptors in the tree shrew retina , 1999, The European journal of neuroscience.

[14]  H. Wässle,et al.  Diversity of glutamate receptors in the mammalian retina , 1998, Vision Research.

[15]  S. Wu,et al.  Synaptic transmission in the outer retina. , 1994, Annual review of physiology.

[16]  B. Ehinger,et al.  Expression of GABA transporter subtypes (GAT1, GAT3) in the adult rabbit retina. , 1999, Acta ophthalmologica Scandinavica.

[17]  R. Pourcho,et al.  Distribution of AMPA-selective glutamate receptor subunits in the cat retina , 1996, Brain Research.

[18]  T. Rauen,et al.  High-affinity glutamate transporters in the rat retina: a major role of the glial glutamate transporter GLAST-1 in transmitter clearance , 1997, Cell and Tissue Research.

[19]  H. Wässle,et al.  Differential expression of the presynaptic cytomatrix protein bassoon among ribbon synapses in the mammalian retina , 1999, The European journal of neuroscience.

[20]  J. L. Schnapf,et al.  The Photovoltage of Macaque Cone Photoreceptors: Adaptation, Noise, and Kinetics , 1999, The Journal of Neuroscience.

[21]  S. Massey,et al.  Chapter 11 Cell types using glutamate as a neurotransmitter in the vertebrate retina , 1990 .

[22]  S. Yazulla Neurotransmitter release from horizontal cells , 1995 .

[23]  Heinz Wässle,et al.  Immunocytochemical analysis of bipolar cells in the macaque monkey retina , 1994, The Journal of comparative neurology.

[24]  M. Häusser,et al.  Intersynaptic diffusion of neurotransmitter. , 1997, Trends in neurosciences.

[25]  C. Grund,et al.  The arm-repeat protein NPRAP (neurojungin) is a constituent of the plaques of the outer limiting zone in the retina, defining a novel type of adhering junction. , 1999, Experimental cell research.

[26]  Mary B. Kennedy,et al.  The postsynaptic density at glutamatergic synapses , 1997, Trends in Neurosciences.

[27]  S. Fisher,et al.  Ultrastructural evidence that horizontal cell axon terminals are presynaptic in the human retina , 1988, The Journal of comparative neurology.

[28]  H. Wässle,et al.  Immunocytochemical Localization of the Postsynaptic Density Protein PSD-95 in the Mammalian Retina , 1998, The Journal of Neuroscience.

[29]  T. Rauen,et al.  Coincidence of L‐glutamate/L‐aspartate transporter (GLAST) and glutamine synthetase (GS) immunoreactions in retinal glia: Evidence for coupling of GLAST and GS in transmitter clearance , 1995, Journal of neuroscience research.

[30]  D. Pow,et al.  Changing patterns of spatial buffering of glutamate in developing rat retinae are mediated by the Müller cell glutamate transporter GLAST , 1999, Cell and Tissue Research.

[31]  N. Saito,et al.  Immunocytochemical localization of three subtypes of GABA transporter in rat retina. , 1995, Brain research. Molecular brain research.

[32]  S. Heinemann,et al.  Cloned glutamate receptors. , 1994, Annual review of neuroscience.

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

[34]  J. Dowling The Ultrastructure of the Human Retina , 1967 .

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

[36]  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.

[37]  H. Wässle,et al.  Glycinergic synapses in the rod pathway of the rat retina: cone bipolar cells express the alpha 1 subunit of the glycine receptor , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[38]  H. Wässle,et al.  Immunocytochemical localization of glycine receptors in the mammalian retina , 1993, The Journal of comparative neurology.

[39]  J. L. Schnapf,et al.  Photovoltage of rods and cones in the macaque retina. , 1995, Science.

[40]  B. Gumbiner,et al.  Cell Adhesion: The Molecular Basis of Tissue Architecture and Morphogenesis , 1996, Cell.

[41]  P. Sterling,et al.  Subcellular localization of GABAA receptor on bipolar cells in macaque and human retina , 1994, Vision Research.

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

[43]  Heinz Wässle,et al.  Horizontal Cells in the Monkey Retina: Immunocytochemical staining with antibodies against calcium binding proteins , 1989, The European journal of neuroscience.

[44]  L. Peichl,et al.  An alternative pathway for rod signals in the rodent retina: rod photoreceptors, cone bipolar cells, and the localization of glutamate receptors. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[45]  Boris Barbour,et al.  Nonvesicular release of neurotransmitter , 1993, Neuron.

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

[47]  B. Giros,et al.  Cloning of a functional vesicular GABA and glycine transporter by screening of genome databases , 1997, FEBS letters.

[48]  E. A. Schwartz,et al.  Depolarization without calcium can release gamma-aminobutyric acid from a retinal neuron. , 1987, Science.

[49]  H. Wässle,et al.  Immunocytochemical Localization of the GABACReceptor ρ Subunits in the Mammalian Retina , 1996, The Journal of Neuroscience.

[50]  W. Stell,et al.  Identification and localization of an immunoreactiveAMPA-type glutamate receptor subunit (GluR4) with respect to identified photoreceptor synapses in the outer plexiform layer of goldfish retina , 1997, Journal of neurocytology.

[51]  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.

[52]  T. Straser [Clearance]. , 2020, Medicinski glasnik.

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

[54]  H. Wässle,et al.  GABA‐like immunoreactivity in the macaque monkey retina: A light and electron microscopic study , 1990, The Journal of comparative neurology.

[55]  P. Sterling,et al.  Immunoreactivity to GABAA receptor in the outer plexiform layer of the cat retina , 1992, The Journal of comparative neurology.

[56]  P Sterling,et al.  Horizontal cells in cat and monkey retina express different isoforms of glutamic acid decarboxylase , 1994, Visual Neuroscience.

[57]  E. Jorgensen,et al.  Identification and characterization of the vesicular GABA transporter , 1997, Nature.

[58]  G. Buchsbaum,et al.  Mammalian rod terminal: Architecture of a binary synapse , 1995, Neuron.

[59]  P. Mobbs,et al.  The spatial relationship between Mu¨ller cell processes and the photoreceptor output synapse , 1992, Brain Research.