Skip to main content

The Cone Pedicle, the First Synapse in the Retina

  • Conference paper

Part of the book series: Keio University International Symposia for Life Sciences and Medicine ((KEIO,volume 11))

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].

This is a preview of subscription content, log in via an institution.

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   39.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   54.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Attwell D, Barbour B, Szatkowski M (1993) Nonvesicular release of neurotransmitter. Neuron 11: 401–407

    Article  PubMed  CAS  Google Scholar 

  2. Awatramani GB, Slaughter MM (2000) Origin of transient and sustained responses in ganglion cells of the retina. J Neurosci 20: 7087–7095

    PubMed  CAS  Google Scholar 

  3. Barbour B, Häusser M (1997) Intersynaptic diffusion of neurotransmitter. Trends Neurosci 20: 377–384

    Article  PubMed  CAS  Google Scholar 

  4. 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

    Article  PubMed  CAS  Google Scholar 

  5. Boycott BB, Hopkins JM (1993) Cone synapses of a flat diffuse cone bipolar cell in the primate retina. J Neurocytol 22: 765–778

    Article  PubMed  CAS  Google Scholar 

  6. Boycott BB, Wässle H (1991) Morphological classification of bipolar cells of the primate retina. Eur J Neurosci 3: 1069–1088

    Article  PubMed  Google Scholar 

  7. Brandstätter JH, Hack I (2001) Localization of glutamate receptors at a complex synapse. Cell Tissue Res 303: 1–14

    Article  PubMed  Google Scholar 

  8. 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

    PubMed  Google Scholar 

  9. Brandstätter JH, Koulen P, Wässle H (1998) Diversity of glutamate receptors in the mammalian retina. Vision Res 38: 1385–1397

    Article  PubMed  Google Scholar 

  10. 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

    Article  PubMed  Google Scholar 

  11. 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

    Article  PubMed  CAS  Google Scholar 

  12. 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

    Article  PubMed  CAS  Google Scholar 

  13. 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

    Article  PubMed  CAS  Google Scholar 

  14. 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

    Article  PubMed  CAS  Google Scholar 

  15. Dacey DM, Lee BB, Stafford DK, et al. (1996) Horizontal cells of the primate retina: cone specificity without spectral opponency. Science 271: 656–659

    Article  PubMed  CAS  Google Scholar 

  16. 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

    Article  PubMed  CAS  Google Scholar 

  17. DeVries SH (2000) Bipolar cells use kainate and AMPA receptors to filter visual information into separate channels. Neuron 28: 847–856

    Article  PubMed  CAS  Google Scholar 

  18. Dingledine R, Borgs K, Bowie D, et al. (1999) The glutamate receptor ion channels. Pharmacol Rev 51: 7–61

    PubMed  CAS  Google Scholar 

  19. Dowling JE, Boycott BB (1966) Organization of the primate retina: electron microscopy. Proc R Soc Lond B Biol Sci 166: 80–111

    Article  PubMed  CAS  Google Scholar 

  20. 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

    PubMed  CAS  Google Scholar 

  21. Garner CC, Nash J, Huganir RL (2000) PDZ domains in synapse assembly and signalling. Trends Cell Biol 10: 274–280

    Article  PubMed  CAS  Google Scholar 

  22. Gersdorff von H (2001) Synaptic ribbons: versatile signal transducers. Neuron 29: 7–10

    Article  Google Scholar 

  23. Greferath U, Grünert U, Müller F, et al. (1994) Localization of GABAA receptors in the rabbit retina. Cell Tissue Res 276: 295–307

    PubMed  CAS  Google Scholar 

  24. 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

    Article  PubMed  Google Scholar 

  25. Gumbiner BM (1996) Cell adhesion: the molecular basis of tissue architecture and morphogenesis. Cell 84: 345–357

    Article  PubMed  CAS  Google Scholar 

  26. 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

    Article  PubMed  CAS  Google Scholar 

  27. Haverkamp S, Grünert U, Wässle H (2000) The cone pedicle, a complex synapse in the retina. Neuron 27: 85–95

    Article  PubMed  CAS  Google Scholar 

  28. 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

    PubMed  CAS  Google Scholar 

  29. 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

    Article  PubMed  CAS  Google Scholar 

  30. Hohmann M, Heinemann S (1994) Cloned glutamate receptors. Annu Rev Neurosci 17: 31–108

    Article  Google Scholar 

  31. Hopkins JM, Boycott BB (1997) The cone synapses of cone bipolar cells of primate retina. J Neurocytol 26: 313–325

    Article  PubMed  CAS  Google Scholar 

  32. 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

    Article  PubMed  CAS  Google Scholar 

  33. 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

    Article  PubMed  CAS  Google Scholar 

  34. 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

    Article  PubMed  CAS  Google Scholar 

  35. Kaneko A, Tachibana M (1986) Effects of gamma-aminobutyric-acid on isolated cone photoreceptors of the turtle retina. J Physiol (Lond) 373: 443–461

    CAS  Google Scholar 

  36. Kennedy MB (1997) The postsynaptic density at glutamatergic synapses. Trends Neurosci 20: 264–268

    Article  PubMed  CAS  Google Scholar 

  37. 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

    PubMed  CAS  Google Scholar 

  38. 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

    Article  PubMed  CAS  Google Scholar 

  39. Linberg KA, Fisher SK (1988) Ultrastructural evidence that horizontal cell axon terminals are presynaptic in the human retina. J Comp Neurol 268: 281–297

    Article  PubMed  CAS  Google Scholar 

  40. McIntire SL, Reimer RJ, Schuske K, et al. (1997) Identification and characterization of the vesicular GABA transporter. Nature 389: 870–876

    Article  PubMed  CAS  Google Scholar 

  41. Missotten L (1965) The ultrastructure of the human retina. Editions Arscia S.A., Brussels

    Google Scholar 

  42. Miyake Y, Yagasaki K, Horiguchi M, et al. (1986) Congenital stationary night blindness with negative electroretinogram: a new classification. Arch Ophthalmol 104: 1013–1020

    Article  PubMed  CAS  Google Scholar 

  43. Morgans CW (2000a) Presynaptic proteins of ribbon synapses in the retina. Microsc Res Tech 50: 141–150

    Article  PubMed  CAS  Google Scholar 

  44. Morgans CW (2000b) Neurotransmitter release at ribbon synapses in the retina. Immunol Cell Biol 78: 442–446

    Article  PubMed  CAS  Google Scholar 

  45. Morgans CW (2001) Localization of the alF calcium channel subunit in the rat retina. Invest Ophthalmol Vis Sci 42: 2414–2418

    PubMed  CAS  Google Scholar 

  46. Morigiwa K, Vardi N (1999) Differential expression of ionotropic glutamate receptor subunits in the outer retina. J Comp Neurol 405: 173–184

    Article  PubMed  CAS  Google Scholar 

  47. 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

    PubMed  CAS  Google Scholar 

  48. 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

    Article  PubMed  CAS  Google Scholar 

  49. Ozawa S, Haruyuki K, Tsuzuki K (1998) Glutamate receptors in the mammalian central nervous system. Prog Neurobiol 54: 581–618

    Article  PubMed  CAS  Google Scholar 

  50. 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

    Google Scholar 

  51. 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

    Article  PubMed  CAS  Google Scholar 

  52. 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

    Google Scholar 

  53. Rakhilin SV, Schwartz EA (1994) A GABA transporter operates asymmetrically and with variable stoichiometry. Neuron 13: 949–960

    Article  PubMed  Google Scholar 

  54. Rao-Mirotznik R, Harkins AB, Buchsbaum G, et al. (1995) Mammalian rod terminal: architecture of a binary synapse. Neuron 14: 561–569

    Article  PubMed  CAS  Google Scholar 

  55. 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

    Article  PubMed  CAS  Google Scholar 

  56. Raviola E, Gilula NB (1975) Intramembrane organization of specialized contacts in the outer plexiform layer of the retina. J Cell Biol 65: 192–222

    Article  PubMed  CAS  Google Scholar 

  57. Rieke F, Schwartz EA (1994) A cGMP-gated current can control exocytosis at cone synapses. Neuron 13: 863–873

    Article  PubMed  CAS  Google Scholar 

  58. 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

    Article  PubMed  Google Scholar 

  59. 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

    Article  PubMed  Google Scholar 

  60. Sandmann D, Boycott BB, Peichl L (1996) The horizontal cells of artiodactyl retinae: a comparison with Cajal’s descriptions. Vis Neurosci 13: 735–746

    Article  PubMed  CAS  Google Scholar 

  61. Sarantis M, Mobbs P (1992) The spatial relationship between Müller cell processes and the photoreceptor output synapse. Brain Res 584: 299–304

    Article  PubMed  CAS  Google Scholar 

  62. 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

    Article  PubMed  CAS  Google Scholar 

  63. Schmitz Y, Witkovsky P (1997) Dependence of photoreceptor glutamate release on a dihydropyridine-sensitive calcium channel. Neuroscience 78: 1209–1216

    Article  PubMed  CAS  Google Scholar 

  64. 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

    Article  PubMed  CAS  Google Scholar 

  65. Schneeweis DM, Schnapf JL (1995) Photovoltage of rods and cones in the macaque retina. Science 268: 1053–1056

    Article  PubMed  CAS  Google Scholar 

  66. Schneeweis DM, Schnapf JL (1999) The photovoltage of macaque cone photoreceptors: adaptation, noise, and kinetics. J Neurosci 19: 1203–1216

    PubMed  CAS  Google Scholar 

  67. Schwartz EA (1993) Depolarization without calcium can release y-aminobutyric acid from a retinal neuron. Science 238: 350–355

    Article  Google Scholar 

  68. 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

    Google Scholar 

  69. 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

    Article  PubMed  CAS  Google Scholar 

  70. Taylor WR, Morgans CW (1998) Localization and properties of voltage-gated calcium channels in cone photoreceptors of Tupaia belangen. Vis Neurosci 15: 541–552

    CAS  Google Scholar 

  71. Thoreson WB, Witkovsky P (1999) Glutamate receptors and circuits in the vertebrate retina. Prog Retin Eye Res 18: 765–810

    Article  PubMed  CAS  Google Scholar 

  72. 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

    Article  Google Scholar 

  73. 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

    Article  PubMed  CAS  Google Scholar 

  74. Vardi N, Sterling P (1994) Subcellular localization of GABAA receptor on bipolar cells in macaque and human retina. Vision Res 34: 1235–1246

    Article  PubMed  CAS  Google Scholar 

  75. 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

    Article  PubMed  CAS  Google Scholar 

  76. 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

    Article  PubMed  CAS  Google Scholar 

  77. Vardi N, Morigiwa K, Wang T-L, et al. (1998) Neurochemistry of the mammalian cone “synaptic complex.” Vision Res 38: 1359–1369

    PubMed  CAS  Google Scholar 

  78. 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

    PubMed  CAS  Google Scholar 

  79. 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

    Article  PubMed  Google Scholar 

  80. Wilkinson MF, Barnes S (1996) The dihydropyridine-sensitive calcium channel subtype in cone photoreceptors. J Gen Physiol 107: 621–630

    Article  PubMed  CAS  Google Scholar 

  81. Wu SM (1994) Synaptic transmission in the outer retina. Annu Rev Physiol 56: 141–168

    Article  PubMed  CAS  Google Scholar 

  82. 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

    PubMed  CAS  Google Scholar 

  83. Yagi T, MacLeish P (1994) Ionic conductances of monkey solitary cone inner segments. J Neurophysiol 71: 656–665

    PubMed  CAS  Google Scholar 

  84. 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

    Chapter  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2003 Springer-Verlag Tokyo

About this paper

Cite this paper

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

Download citation

  • DOI: https://doi.org/10.1007/978-4-431-68447-3_6

  • Publisher Name: Springer, Tokyo

  • Print ISBN: 978-4-431-68449-7

  • Online ISBN: 978-4-431-68447-3

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics