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Synaptic connections of cone bipolar cells that express the neurokinin 1 receptor in the rabbit retina

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Abstract

We have investigated and further characterized, in the rabbit retina, the synaptic connectivity of the ON-type cone bipolar cells that are immunoreactive for an antibody against the neurokinin-1 receptor (NK1R). NK1R-immunoreactive bipolar cell axons terminate in stratum 4 of the inner plexiform layer. The axons of NK1R-positive bipolar cells receive synaptic inputs from amacrine cells through conventional synapses and from putative AII amacrine cells via gap junctions. The major outputs from NK1R-positive bipolar cells make contacts with amacrine cell processes. The most frequent postsynaptic dyads comprise two amacrine cell processes. Double-labeling experiments with antibodies against NK1R and either calretinin or glycine have demonstrated that NK1R-immunoreactive bipolar cells form gap junctions with AII amacrine cells. Thus, NK1R-positive cone bipolar cells, together with calbindin-positive cone bipolar cells, may play an important role in transferring rod signals to the ON-type ganglion cells of the cone pathway in the rabbit retina.

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References

  1. Bloomfield SA, Dacheux RF (2001) Rod vision: pathways and processing in the mammalian retina. Prog Ret Eye Res 20:351–384

  2. Boycott B, Wässle H (1999) Parallel processing in the mammalian retina. Invest Ophthal Vis Sci 40:1313–1327

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

  4. Brown SP, Masland RH (1999) Costratification of a population of bipolar cells with the direction-selective circuitry of the rabbit retina. J Comp Neurol 408:97–106

  5. Casini G, Sabatini A, Catalani E, Willems D, Bosco L, Brecha NC (2002) Expression of the neurokinin 1 receptor in the rabbit retina. Neuroscience 115:1309–1321

  6. Chun M-H, Han S-H, Chung J-W, Wässle H (1993) Electron microscopic analysis of the rod pathway of the rat retina. J Comp Neurol 332:421–432

  7. Cohen E, Sterling P (1986) Accumulation of (3H) glycine by cone bipolar neurons in the cat retina. J Comp Neurol 250:1–7

  8. Cohen E, Sterling P (1990) Demonstration of cell types among cone bipolar neurons of cat retina. Proc R Soc Lond [Biol] 330:305–321

  9. Dacheux RF, Raviola E (1986) The rod pathway in the rabbit retina: a depolarizing bipolar and amacrine cell. J Neurosci 6:331–345

  10. Dubin MW (1970) The inner plexiform layer of the vertebrate retina: a quantitative and comparative electron microscopic analysis. J Comp Neurol 140:479–506

  11. Famiglietti EV, Kolb H (1975) A bistratified amacrine cell and synaptic circuitry in the inner plexiform layer of the retina. Brain Res 84:293–300

  12. Flagg-Newton J, Simpson I, Loewenstein WR (1979) Permeability of the cell-to-cell membrane channels in mammalian cell junction. Science 205:404–407

  13. Freed MA (1992) GABAergic circuits in the mammalian retina. Prog Brain Res 90:107–131

  14. Hampson EC, Vaney DI, Weiler R (1992) Dopaminergic modulation of gap junction permeability between amacrine cells in mammalian retina. J Neurosci 12:4911–4922

  15. Kim I-B, Lee E-J, Oh S-J, Park C-B, Pow DV, Chun M-H (2002) Light and electron microscopic analysis of aquaporin 1-like-immunoreactive amacrine cells in the rat retina. J Comp Neurol 452:178–191

  16. Kim I-B, Lee E-J, Kang T-H, Chung J-W, Chun M-H (2003) Morphological analysis of the hyperpolarization-activated cyclic nucleotide-gated cation channel 1 (HCN1) immunoreactive bipolar cells in the rabbit retina. J Comp Neurol 467:389–402

  17. Kolb H (1979) The inner plexiform layer in the retina of the cat: electron microscopic observations. J Neurocytol 8:295–329

  18. Kolb H, Famiglietti EV (1974) Rod and cone pathways in the inner plexiform layer of the cat retina. Science 186:47–49

  19. MacNeil MA, Heussy JK, Dacheux RF, Raviola E, Masland RH (2004) The population of bipolar cells in the rabbit retina. J Comp Neurol 472:73–86

  20. Marc RE (1989) The role of glycine in the mammalian retina. Prog Ret Res 8:67–107

  21. Massey SC (1990) Cell types using glutamate as a neurotransmitter in the vertebrate retina. Prog Ret Res 9:399–425

  22. Massey SC, Mills SL (1996) A calbindin-immunoreactive cone bipolar cell type in the rabbit retina. J Comp Neurol 355:15–33

  23. Massey SC, Mills SL (1999a) An antibody to calretinin stains AII amacrine cells in the rabbit retina: double label and confocal analysis. J Comp Neurol 411:3–18

  24. Massey SC, Mills SL (1999b) Gap junctions between AII amacrine cells and calbindin-positive bipolar cells in the rabbit retina. Vis Neurosci 16:1181–1189

  25. McGillem GS, Dacheux RF (2001) Rabbit cone bipolar cells: correlation of their morphologies with whole-cell recordings. Vis Neurosci 18:675–685

  26. McGuire BA, Stevens JK, Sterling P (1980) Beta ganglion cells receive convergent input from 2 types of cine bipolars. Soc Neurosci Abstr 6:347

  27. McGuire BA, Stevens JK, Sterling P (1984) Microcircuitry of bipolar cells in cat retina. J Neurosci 4:2920–2938

  28. McGuire BA, Stevens JK, Sterling P (1986) Microcircuitry of beta ganglion cells in cat retina. J Neurosci 6:907–918

  29. Merighi A, Raviola E, Dacheux RF (1996) Connections of two types of flat cone bipolars in the rabbit retina. J Comp Neurol 371:164–178

  30. Mills SL, Massey SC (1992) Morphology of bipolar cells labeled by DAPI in the rabbit retina. J Comp Neurol 321:133–149

  31. Mills SL, Massey SC (1995) Differential properties of two gap junctional pathways made by AII amacrine cells. Nature 377:734–737

  32. Nelson R (1982) AII amacrine cells quicken time course of rod signals in the cat retina. J Neurophysiol 47:928–947

  33. Nelson R, Kolb H (1983) Synaptic patterns and response properties of bipolar and ganglion cells in the cat retina. Vis Res 23:1183–1195

  34. Pourcho RG (1980) Uptake of (3H)glycine and (3H)GABA by amacrine cells in the cat retina. Brain Res 198:333–346

  35. Pourcho RG (1996) Neurotransmitters in the retina. Curr Eye Res 15:797–803

  36. Pourcho RG, Goebel DJ (1985) A combined Golgi and autoradiographic study of (3H) glycine-accumulating amacrine cells in the cat retina. J Comp Neurol 233:473–480

  37. Pow DV, Hendrickson AE (1999) Distribution of the glycine transporter glyt-1 in mammalian and nonmammalian retinae. Vis Neurosci 16:231–239

  38. Pow DV, Wright LL, Vaney DI (1995) Immunocytochemical detection of amino acid neurotransmitters in paraformaldehyde-fixed tissues. J Neurosci Methods 56:115–123

  39. Raviola E, Dacheux RF (1987) The excitatory dyad synapse in the rabbit retina. Proc Natl Acad Sci USA 84:7324–7328

  40. Ribak CE, Tong WMY, Brecha NC (1996) GABA plasma membrane transporters, GAT-1 and GAT-3, display different distributions in the rat hippocampus. J Comp Neurol 367:595–606

  41. Sterling P, Freed MA, Smith RG (1988) Architecture and rod and cone circuits of the ON-beta ganglion cell. J Neurosci 8:623–642

  42. Sterling P, Smith RG, Rao R, Vardi N (1995) Functional architecture of mammalian outer retina and bipolar cells. In: Archer S, Djamgoz MBA, Vallerga S (eds) Neurobiology and clinical aspects of the outer retina. Chapman & Hall, London, pp 325–348

  43. Strettoi E, Dacheux RF, Raviola E (1990) Synaptic connections of rod bipolar cells in the inner plexiform layer of the rabbit retina. J Comp Neurol 295:449–466

  44. Strettoi E, Raviola E, Dacheux RF (1992) Synaptic connections of the narrow-field bistratified rod amacrine cell (AII) in the rabbit retina. J Comp Neurol 325:152–168

  45. Strettoi E, Dacheux RF, Raviola E (1994) Cone bipolar cells as interneurons in the rod pathway of the rabbit retina. J Comp Neurol 347:139–149

  46. Vaney DI (1990) The mosaic of amacrine cells in the mammalian retina. Prog Ret Res 9:49–100

  47. Vaney DI (1991) Many diverse types of retinal neurons show tracer coupling when injected with biocytin or neurobiotin. Neurosci Lett 125:187–190

  48. Vaney DI (1997) Neuronal coupling in rod-signal pathways of the retina. Invest Ophthal Vis Sci 38:267–273

  49. Vaney DI, Gynther IC, Young HM (1991) Rod-signal interneurons in the rabbit retina. II. AII amacrine cells. J Comp Neurol 310:154–169

  50. Vaney DI, Nelson JC, Pow DV (1998) Neurotransmitter coupling through gap junctions in the retina. J Neurosci 18:10594–10602

  51. Wässle H (2004) Parallel processing in the mammalian retina. Nat Rev Neurosci 5:747–757

  52. Wässle H, Boycott BB (1991) Functional architecture of the mammalian retina. Physiol Rev 71:447–480

  53. Wässle H, Grünert U, Chun M-H, Boycott BB (1995) The rod pathway of the macaque monkey retina: identification of AII amacrine cells with antibodies against calretinin. J Comp Neurol 361:537–551

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Author information

Correspondence to Myung-Hoon Chun.

Additional information

I.-B. Kim and M.R. Park contributed equally to this work.

This work was supported by the Ministry of Science and Technology of Korea (grant no. M1-0108-00-0059; Neurobiology Support Grant).

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Kim, I., Park, M.R., Kang, T. et al. Synaptic connections of cone bipolar cells that express the neurokinin 1 receptor in the rabbit retina. Cell Tissue Res 321, 1–8 (2005). https://doi.org/10.1007/s00441-005-1122-8

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Keywords

  • Retina
  • NK1 receptor
  • Cone bipolar cell
  • Rod pathway
  • Immunocytochemistry
  • Electron microscopy
  • Rabbit (New Zealand)