Abstract
Cone pedicles are the output synapses of cone photoreceptors and transfer the light signal onto the dendrites of bipolar and horizontal cells. In the macaque monkey retina, cone pedicles contain between 20 and 45 ribbon synapses (triads), which are the release sites for glutamate, the cone transmitter [11, 13, 19, 22, 41]. Triads comprise a presynaptic ribbon, two horizontal dendrites as lateral elements, and one or two ON-cone bipolar cell dendrites as central elements (Fig. 1). Flat contacts are formed in most instances by the dendrites of OFF-cone bipolar cells at the cone pedicle base [19]. Glutamate released continuously at the synaptic ribbons acts not only through direct contacts but to an even greater extent through diffusion to the appropriate glutamate receptors (GluRs) [72].
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References
Attwell D, Barbour B, Szatkowski M (1993) Nonvesicular release of neurotransmitter. Neuron 11: 401–407
Awatramani GB, Slaughter MM (2000) Origin of transient and sustained responses in ganglion cells of the retina. J Neurosci 20: 7087–7095
Barbour B, Häusser M (1997) Intersynaptic diffusion of neurotransmitter. Trends Neurosci 20: 377–384
Bech-Hansen NT, Naylor MJ, Maybaum TA, et al. (1998) Loss-of-function mutations in a calcium-channel al-subunit gene in Xp11.23 cause incomplete X-linked congenital stationary night blindness. Nat Genet 19: 264–267
Boycott BB, Hopkins JM (1993) Cone synapses of a flat diffuse cone bipolar cell in the primate retina. J Neurocytol 22: 765–778
Boycott BB, Wässle H (1991) Morphological classification of bipolar cells of the primate retina. Eur J Neurosci 3: 1069–1088
Brandstätter JH, Hack I (2001) Localization of glutamate receptors at a complex synapse. Cell Tissue Res 303: 1–14
Brandstätter JH, Koulen P, Wässle H (1997) Selective synaptic distribution of kainate receptor subunits in the two plexiform layers of the rat retina. J Neurosci 17: 9298–9307
Brandstätter JH, Koulen P, Wässle H (1998) Diversity of glutamate receptors in the mammalian retina. Vision Res 38: 1385–1397
Brandstätter JH, Fletcher EL, Garner CC, et al. (1999) Differential expression of the presynaptic cytomatrix protein bassoon among ribbon synapses in the mammalian retina. Eur J Neurosci 11: 3683–3693
Calkins DJ, Tsukamoto Y, Sterling P (1996) Foveal cones form basal as well as invaginating junctions with diffuse ON bipolar cells. Vision Res 36: 3373–3381
Chan TL, Grünert U (1998) Horizontal cell connections with short wavelength-sensitive cones in the retina: a comparison between new world and old world primates. J Comp Neurol 393: 196–209
Chun M-H, Grünert U, Martin PR, et al. (1996) The synaptic complex of cones in the fovea and in the periphery of the macaque monkey retina. Vision Res 36: 3383–3395
Cueva JG, Haverkamp S, Reimer RJ, et al. (2002) Vesicular y-aminobutyric acid transporter expression in amacrine and horizontal cells. J Comp Neurol 445: 227–237
Dacey DM, Lee BB, Stafford DK, et al. (1996) Horizontal cells of the primate retina: cone specificity without spectral opponency. Science 271: 656–659
Derouiche A, Rauen T (1995) 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. J Neurosci Res 42: 131–143
DeVries SH (2000) Bipolar cells use kainate and AMPA receptors to filter visual information into separate channels. Neuron 28: 847–856
Dingledine R, Borgs K, Bowie D, et al. (1999) The glutamate receptor ion channels. Pharmacol Rev 51: 7–61
Dowling JE, Boycott BB (1966) Organization of the primate retina: electron microscopy. Proc R Soc Lond B Biol Sci 166: 80–111
Enz R, Brandstätter JH, Wässle H, et al. (1996) Immunocytochemical localization of the GABAc receptor p subunits in the mammalian retina. J Neurosci 16: 4479–4490
Garner CC, Nash J, Huganir RL (2000) PDZ domains in synapse assembly and signalling. Trends Cell Biol 10: 274–280
Gersdorff von H (2001) Synaptic ribbons: versatile signal transducers. Neuron 29: 7–10
Greferath U, Grünert U, Müller F, et al. (1994) Localization of GABAA receptors in the rabbit retina. Cell Tissue Res 276: 295–307
Grünert U, Wässle H (1990) GABA-like immunoreactivity in the macaque monkey retina: a light and electron microscopic study. J Comp Neurol 297: 509–524
Gumbiner BM (1996) Cell adhesion: the molecular basis of tissue architecture and morphogenesis. Cell 84: 345–357
Hack I, Frech M, Dick O, et al. (2001) Heterogeneous distribution of AMPA glutamate receptor subunits at the photoreceptor synapses of rodent retina. Eur J Neurosci 13: 15–24
Haverkamp S, Grünert U, Wässle H (2000) The cone pedicle, a complex synapse in the retina. Neuron 27: 85–95
Haverkamp S, Grünert U, Wässle H (2001a) The synaptic architecture of AMPA receptors at the cone pedicle of the primate retina. J Neurosci 21: 2488–2500
Haverkamp S, Grünert U, Wässle H (2001b) Localization of kainate receptors at the cone pedicles of the primate retina. J Comp Neurol 436: 471–486
Hohmann M, Heinemann S (1994) Cloned glutamate receptors. Annu Rev Neurosci 17: 31–108
Hopkins JM, Boycott BB (1997) The cone synapses of cone bipolar cells of primate retina. J Neurocytol 26: 313–325
Honda S, Yamamoto M, Saito N (1995) Immunocytochemical localization of three subtypes of GABA transporter in rat retina. Brain Res Mol Brain Res 33: 319–325
Hu M, Bruun A, Ehinger B (1999) Expression of GABA transporter subtypes (GAT1, GAT3) in the adult rabbit retina. Acta Ophthalmol Scand 77: 255–260
Johnson J, Chen TK, Rickman DE, et al. (1996) Multiple y-aminobutyric acid plasma membrane transporters (GAT-1, GAT-2, GAT-3) in the rat retina. J Comp Neurol 375: 212–224
Kaneko A, Tachibana M (1986) Effects of gamma-aminobutyric-acid on isolated cone photoreceptors of the turtle retina. J Physiol (Lond) 373: 443–461
Kennedy MB (1997) The postsynaptic density at glutamatergic synapses. Trends Neurosci 20: 264–268
Koulen P, Fletcher EL, Craven SE, et al. (1998) Immunocytochemical localization of the postsynaptic density protein PSD-95 in the mammalian retina. J Neurosci 18: 10136–10149
Lee BB, Dacey DM, Smith VC, et al. (1999) Horizontal cells reveal cone type-specific adaptation in primate retina. Proc Natl Acad Sci USA 96: 14611–14616
Linberg KA, Fisher SK (1988) Ultrastructural evidence that horizontal cell axon terminals are presynaptic in the human retina. J Comp Neurol 268: 281–297
McIntire SL, Reimer RJ, Schuske K, et al. (1997) Identification and characterization of the vesicular GABA transporter. Nature 389: 870–876
Missotten L (1965) The ultrastructure of the human retina. Editions Arscia S.A., Brussels
Miyake Y, Yagasaki K, Horiguchi M, et al. (1986) Congenital stationary night blindness with negative electroretinogram: a new classification. Arch Ophthalmol 104: 1013–1020
Morgans CW (2000a) Presynaptic proteins of ribbon synapses in the retina. Microsc Res Tech 50: 141–150
Morgans CW (2000b) Neurotransmitter release at ribbon synapses in the retina. Immunol Cell Biol 78: 442–446
Morgans CW (2001) Localization of the alF calcium channel subunit in the rat retina. Invest Ophthalmol Vis Sci 42: 2414–2418
Morigiwa K, Vardi N (1999) Differential expression of ionotropic glutamate receptor subunits in the outer retina. J Comp Neurol 405: 173–184
Muresan V, Lyass A, Schnapp BJ (1999) The kinesin motor KIF3A is a component of the presynaptic ribbon in vertebrate photoreceptors. J Neurosci 19: 1027–1037
Nomura A, Shigemoto R, Nakamura Y, et al. (1994) Developmentally regulated post-synaptic localization of a metabotropic glutamate receptor in rat rod bipolar cells. Cell 77: 361–369
Ozawa S, Haruyuki K, Tsuzuki K (1998) Glutamate receptors in the mammalian central nervous system. Prog Neurobiol 54: 581–618
Petralia RS, Wang YX, Wenthold RJ (2002) NMDA receptors and PSD-95 are found in attachment plaques in cerebellar granular layer glomeruli. Eur J Neurosci 15: 583587
Pow DV, Barnett NL (1999) Changing pattern of spatial buffering of glutamate in developing rat retinae are mediated by the Müller cell glutamate transporter GLAST. Cell Tissue Res 297: 57–66
Qin P, Pourcho RG (1999) Localization of AMPA-selective glutamate receptor subunits in the cat retina: a light-and electron microscopic study. Vis Neurosci 16: 169177
Rakhilin SV, Schwartz EA (1994) A GABA transporter operates asymmetrically and with variable stoichiometry. Neuron 13: 949–960
Rao-Mirotznik R, Harkins AB, Buchsbaum G, et al. (1995) Mammalian rod terminal: architecture of a binary synapse. Neuron 14: 561–569
Rauen T, Taylor WR, Kuhlbrodt K, et al. (1998) High-affinity glutamate transporters in the rat retina: a major role of the glial glutamate transporter GLAST-1 in transmitter clearance. Cell Tissue Res 291: 19–31
Raviola E, Gilula NB (1975) Intramembrane organization of specialized contacts in the outer plexiform layer of the retina. J Cell Biol 65: 192–222
Rieke F, Schwartz EA (1994) A cGMP-gated current can control exocytosis at cone synapses. Neuron 13: 863–873
Röhrenbeck J, Wässle H, Boycott BB (1989) Horizontal cells in the monkey retina: immunocytochemical staining with antibodies against calcium binding proteins. Eur J Neurosci 1: 407–420
Sagné C, Mestikawy SE, Isambert M-F, et al. (1997) Cloning of a functional vesicular GABA and glycine transporter by screening of genome databases. FEBS Lett 417: 177–183
Sandmann D, Boycott BB, Peichl L (1996) The horizontal cells of artiodactyl retinae: a comparison with Cajal’s descriptions. Vis Neurosci 13: 735–746
Sarantis M, Mobbs P (1992) The spatial relationship between Müller cell processes and the photoreceptor output synapse. Brain Res 584: 299–304
Satoh H, Kaneda M, Kaneko A (2001) Intracellular chloride concentration is higher in rod bipolar cells than in cone bipolar cells of the mouse retina. Neurosci Lett 310: 161–164
Schmitz Y, Witkovsky P (1997) Dependence of photoreceptor glutamate release on a dihydropyridine-sensitive calcium channel. Neuroscience 78: 1209–1216
Schmitz F, Königstorfer A, Südhof TC (2000) RIBEYE, a component of synaptic ribbons: a protein’s journey through evolution provides insight into synaptic ribbon function. Neuron 28: 857–872
Schneeweis DM, Schnapf JL (1995) Photovoltage of rods and cones in the macaque retina. Science 268: 1053–1056
Schneeweis DM, Schnapf JL (1999) The photovoltage of macaque cone photoreceptors: adaptation, noise, and kinetics. J Neurosci 19: 1203–1216
Schwartz EA (1993) Depolarization without calcium can release y-aminobutyric acid from a retinal neuron. Science 238: 350–355
Schwartz EA (1999) A transporter mediates the release of GABA from horizontal cells. In: Toyoda J-I, et al. (eds) The retinal basis of vision. Elsevier, New York, pp 93–101
Strom TM, Nyakatura G, Apfelstedt-Sylla E, et al. (1998) An L-type calcium-channel gene mutated in incomplete X-linked congenital stationary night blindness. Nat Genet 19: 260–263
Taylor WR, Morgans CW (1998) Localization and properties of voltage-gated calcium channels in cone photoreceptors of Tupaia belangen. Vis Neurosci 15: 541–552
Thoreson WB, Witkovsky P (1999) Glutamate receptors and circuits in the vertebrate retina. Prog Retin Eye Res 18: 765–810
tom Dieck S, Sanmarti-Vila L, Langnaese K, et al. (1998) Bassoon, a novel zinc-finger CAG/glutamine-repeat protein selectively localized at the active zone of presynaptic nerve terminals. J Cell Biol 142: 499–509
Vandenbranden CAV, Verweij J, Kamermans M, et al. (1996) Clearance of neurotransmitter from the cone synaptic cleft in goldfish retina. Vision Res 36: 3859–3874
Vardi N, Sterling P (1994) Subcellular localization of GABAA receptor on bipolar cells in macaque and human retina. Vision Res 34: 1235–1246
Vardi N, Masarachia P, Sterling P (1992) Immunoreactivity to GABAA receptor in the outer plexiform layer of the cat retina. J Comp Neurol 320: 394–397
Vardi N, Kaufman, DL, Sterling P (1994) Horizontal cells in cat and monkey retina express different isoforms of glutamic acid decarboxylase. Vis Neurosci 11: 135–142
Vardi N, Morigiwa K, Wang T-L, et al. (1998) Neurochemistry of the mammalian cone “synaptic complex.” Vision Res 38: 1359–1369
Vardi N, Zhang L-L, Payne JA, et al. (2000) Evidence that different cation chloride cotransporters in retinal neurons allow opposite responses to GABA. J Neurosci 20: 7657–7663
Wässle H, Dacey DM, Haun T, et al. (2000) The mosaic of horizontal cells in the macaque monkey retina: with a comment on biplexiform ganglion cells. Vis Neurosci 17: 591–608
Wilkinson MF, Barnes S (1996) The dihydropyridine-sensitive calcium channel subtype in cone photoreceptors. J Gen Physiol 107: 621–630
Wu SM (1994) Synaptic transmission in the outer retina. Annu Rev Physiol 56: 141–168
Wu SM, Gao F, Maple BR (2000) Functional architecture of synapses in the inner retina: segregation of bipolar cell axon terminals. J Neurosci 20: 4462–4470
Yagi T, MacLeish P (1994) Ionic conductances of monkey solitary cone inner segments. J Neurophysiol 71: 656–665
Yazulla S (1995) Neurotransmitter release from horizontal cells. In: Djamgoz, et al. (eds) Neurobiology and clinical aspects of the outer retina. Chapman and Hall, London, pp 249–271
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Wässle, H., Haverkamp, S., Grünert, U., Morgans, C.W. (2003). The Cone Pedicle, the First Synapse in the Retina. In: Kaneko, A. (eds) The Neural Basis of Early Vision. Keio University International Symposia for Life Sciences and Medicine, vol 11. Springer, Tokyo. https://doi.org/10.1007/978-4-431-68447-3_6
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DOI: https://doi.org/10.1007/978-4-431-68447-3_6
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