Cell and Tissue Research

, Volume 339, Issue 2, pp 311–320 | Cite as

Synaptic connections of calbindin-immunoreactive cone bipolar cells in the inner plexiform layer of rabbit retina

  • Shin Ae Kim
  • Choong Ki Jung
  • Tae-Hoon Kang
  • Ji Hyun Jeon
  • Jiook Cha
  • In-Beom Kim
  • Myung-Hoon Chun
Regular Article


In the mammalian retina, information concerning various aspects of an image is transferred in parallel, and cone bipolar cells are thought to play a major role in this parallel processing. We have examined the synaptic connections of calbindin-immunoreactive (IR) ON cone bipolar cells in the inner plexiform layer (IPL) of rabbit retina and have compared these synaptic connections with those that we have previously described for neurokinin 1 (NK1) receptor-IR cone bipolar cells. A total of 325 synapses made by calbindin-IR bipolar axon terminals have been identified in sublamina b of the IPL. The axons of calbindin-IR bipolar cells receive synaptic inputs from amacrine cells through conventional synapses and are coupled to putative AII amacrine cells via gap junctions. The major output from calbindin-IR bipolar cells is to amacrine cell processes. These data resemble our findings for NK1 receptor-IR bipolar cells. However, the incidences of output synapses to ganglion cell dendrites of calbindin-IR bipolar cells are higher compared with the NK1-receptor-IR bipolar cells. On the basis of stratification level and synaptic connections, calbindin-IR ON cone bipolar cells might thus play an important role in the processing of various visual aspects, such as contrast, orientation, and approach sensing, and in transferring rod signals to the ON cone pathway.


ON cone bipolar cell Synaptic circuit Calbindin Parallel processing Retina Rabbit (New Zealand) 


  1. Amthor FR, Takahashi ES, Oyster CW (1989) Morphologies of rabbit retinal ganglion cells with complex receptive fields. J Comp Neurol 280:97–121CrossRefPubMedGoogle Scholar
  2. Berson DM (2003) Strange vision: ganglion cells as circadian photoreceptors. Trends Neurosci 26:314–320CrossRefPubMedGoogle Scholar
  3. Bloomfield SA, Dacheux RF (2001) Rod vision: pathways and processing in the mammalian retina. Prog Retin Eye Res 20:351–384CrossRefGoogle Scholar
  4. Boycott B, Wässle H (1999) Parallel processing in the mammalian retina. Invest Ophthalmol Vis Sci 40:1313–1327PubMedGoogle Scholar
  5. Brandon C (1987) Cholinergic neurons in the rabbit retina: immunocytochemical localization, and relationship to GABAergic and cholinesterase-containing neurons. Brain Res 401:385–391CrossRefPubMedGoogle Scholar
  6. Brown SP, Masland RH (1999) Costratification of a population of bipolar cells with the direction-selective circuitry of the rabbit retina. J Comp Neurol 408:97–106CrossRefPubMedGoogle Scholar
  7. Caldwell JH, Daw NW, Wyatt HJ (1978) Effects of picrotoxin and strychnine on rabbit retinal ganglion cells: lateral interactions for cells with more complex receptive fields. J Physiol (Lond) 276:277–298Google Scholar
  8. Casini G, Sabatini A, Catalani E, Willems D, Bosco L, Brecha NC (2002) Expression of the neurokinin 1 receptor in the rabbit retina. Neuroscience 115:1309–1321CrossRefPubMedGoogle Scholar
  9. 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 332:421–432CrossRefPubMedGoogle Scholar
  10. Chun M-H, Kim I-B, Oh S-J, Chung J-W (1999) Synaptic connectivity of two types of recoverin-labeled cone bipolar cells and glutamic acid decarboxylase immunoreactive amacrine cells in the inner plexiform layer of the rat retina. Vis Neurosci 16:791–800PubMedGoogle Scholar
  11. Cleland BG, Levick WR (1974) Brisk and sluggish concentrically organized ganglion cells in the cat's retina. J Physiol (Lond) 240:421–456Google Scholar
  12. Dubin MW (1970) The inner plexiform layer of the vertebrate retina: a quantitative and comparative electron microscopic analysis. J Comp Neurol 140:479–506CrossRefPubMedGoogle Scholar
  13. Enroth-Cugell C, Robson JG (1966) The contrast sensitivity of retinal ganglion cells of the cat. J Physiol (Lond) 187:517–552Google Scholar
  14. Euler T, Wässle H (1995) Immunocytochemical identification of cone bipolar cells in the rat retina. J Comp Neurol 361:461–478CrossRefPubMedGoogle Scholar
  15. Famiglietti EV, Kolb H (1975) A bistratified amacrine cell and synaptic circuitry in the inner plexiform layer of the retina. Brain Res 84:293–300CrossRefPubMedGoogle Scholar
  16. Famiglietti EV, Kolb H (1976) Structural basis for ON- and OFF-center responses in retinal ganglion cells. Science 194:193–195CrossRefPubMedGoogle Scholar
  17. Famiglietti EV, Tumosa N (1987) Immunocytochemical staining of cholinergic amacrine cells in rabbit retina. Brain Res 413:398–403CrossRefPubMedGoogle Scholar
  18. Fu Y, Liao HW, Do MT, Yau KW (2005) Non-image-forming ocular photoreception in vertebrates. Curr Opin Neurobiol 15:415–422CrossRefPubMedGoogle Scholar
  19. Greferath U, Grünert U, Wässle H (1990) Rod bipolar cells in the mammalian retina show protein kinase C-like immunoreactivity. J Comp Neurol 301:433–442CrossRefPubMedGoogle Scholar
  20. Hartveit E (1997) Functional organization of cone bipolar cells in the rat retina. J Neurophysiol 4:1716–1730Google Scholar
  21. Hoshi H, Mills SL (2009) Components and properties of the G3 ganglion cell circuit in the rabbit retina. J Comp Neurol 513:69–82CrossRefPubMedGoogle Scholar
  22. Hoshi H, Liu W-L, Massey SC, Mills SL (2009) ON inputs to the OFF layer: bipolar cells that break the stratification rules of the retina. J Neurosci 29:8875–8883CrossRefPubMedGoogle Scholar
  23. Kaplan E, Shapley RM (1986) The primate retina contains two types of ganglion cells, with high and low contrast sensitivity. Proc Natl Acad Sci USA 83:2755–2757CrossRefPubMedGoogle Scholar
  24. Kim I-B, Lee M-Y, Oh S-J, Kim K-Y, Chun M-H (1998) Double-labeling techniques demonstrate that rod bipolar cells are under GABAergic control in the inner plexiform layer of the rat retina. Cell Tissue Res 292:17–25CrossRefPubMedGoogle Scholar
  25. Kim I-B, Lee E-J, Kim M-K, Park D-K, Chun M-H (2000) Choline acetyltransferase-immunoreactive neurons in the developing rat retina. J Comp Neurol 427:604–616CrossRefPubMedGoogle Scholar
  26. 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 467:389–402CrossRefPubMedGoogle Scholar
  27. Kim I-B, Park MR, Kang T-H, Kim H-J, Lee E-J, Ahn M-D, Chun M-H (2005) Synaptic connections of cone bipolar cells that express the neurokinin 1 receptor in the rabbit retina. Cell Tissue Res 321:1–8CrossRefPubMedGoogle Scholar
  28. Kim IJ, Zhang Y, Yamagata M, Meister M, Sanes JR (2008) Molecular identification of a retinal cell type that responds to upward motion. Nature 452:478–482CrossRefPubMedGoogle Scholar
  29. Kolb H (1979) The inner plexiform layer in the retina of the cat: electron microscopic observations. J Neurocytol 8:295–329CrossRefPubMedGoogle Scholar
  30. Kolb H, Famiglietti EV (1974) Rod and cone pathways in the inner plexiform layer of the cat retina. Science 186:47–49CrossRefPubMedGoogle Scholar
  31. Levick WR (1967) Receptive fields and trigger features of ganglion cells in the visual streak of the rabbits retina. J Physiol (Lond) 188:285–307Google Scholar
  32. MacNeil MA, Masland RH (1998) Extreme diversity among amacrine cells: implication for function. Neuron 20:971–982CrossRefPubMedGoogle Scholar
  33. MacNeil MA, Heussy JK, Dacheux RF, Raviola E, Masland RH (1999) The shapes and numbers of amacrine cells: matching of photofilled with Golgi-stained cells in the rabbit retina and comparison with other mammalian species. J Comp Neurol 413:305–326CrossRefPubMedGoogle Scholar
  34. MacNeil MA, Heussy JK, Dacheux RF, Raviola E, Masland RH (2004) The population of bipolar cells in the rabbit retina. J Comp Neurol 472:73–86CrossRefPubMedGoogle Scholar
  35. Manookin MB, Beaudoin DL, Ernst ZR, Flagel LJ, Demb JB (2008) Disinhibition combines with excitation to extend the operating range of the OFF visual pathway in daylight. J Neurosci 28:4136–4150CrossRefPubMedGoogle Scholar
  36. Masland RH (1988) Amacrine cells. Trends Neurosci 11:405–410CrossRefPubMedGoogle Scholar
  37. Massey SC, Mills SL (1996) A calbindin-immunoreactive cone bipolar cell type in the rabbit retina. J Comp Neurol 366:15–33CrossRefPubMedGoogle Scholar
  38. McGillem GS, Dacheux RF (2001) Rabbit cone bipolar cells: correlation of their morphologies with whole-cell recordings. Vis Neurosci 18:675–685CrossRefPubMedGoogle Scholar
  39. McGuire BA, Stevens JK, Sterling P (1984) Microcircuitry of bipolar cells in cat retina. J Neurosci 4:2920–2938PubMedGoogle Scholar
  40. McGuire BA, Stevens JK, Sterling P (1986) Microcircuitry of beta ganglion cells in cat retina. J Neurosci 6:907–918PubMedGoogle Scholar
  41. Merighi A, Raviola E, Dacheux RF (1996) Connections of two types of flat cone bipolar in the rabbit retina. J Comp Neurol 371:164–178CrossRefPubMedGoogle Scholar
  42. Münch TA, da Silveira RA, Siegert S, Viney TJ, Awatramani GB, Roska B (2009) Approach sensitivity in the retina processed by a multifunctional neural circuit. Nat Neurosci 12:1308–1316CrossRefPubMedGoogle Scholar
  43. Negishi K, Kato S, Teranishi T (1988) Dopamine cells and rod bipolar cells contain protein kinase C-like immunoreactivity in some vertebrate retinas. Neurosci Lett 94:247–252CrossRefPubMedGoogle Scholar
  44. Nelson R, Kolb H (1983) Synaptic patterns and response properties of bipolar and ganglion cells in the cat retina. Vision Res 23:1183–1195CrossRefPubMedGoogle Scholar
  45. Nelson R, Famiglietti EV, Kolb H (1978) Intracellular staining reveals different levels of stratification for ON-center and OFF-center ganglion cells in the cat retina. J Neurophysiol 4:427–483Google Scholar
  46. Peichl L, Wässle H (1981) Morphological identification of ON- and OFF-centre brisk transient (Y) cells in the cat retina. Proc R Soc Lond [Biol] 212:139–153CrossRefGoogle Scholar
  47. Sandell JH, Masland RH (1986) A system of indoleamine-accumulating neurons in the rabbit retina. J Neurosci 6:3331–3347PubMedGoogle Scholar
  48. Sterling P (2004) How retinal circuits optimize the transfer of visual inforamtion. In: Chalupa LM, Werner JS (eds) The visual neurosciences, vol 1. MIT Press, Hong Kong, pp 234–259Google Scholar
  49. Sterling P, Freed MA, Smith RG (1988) Architecture and rod and cone circuits of the on-beta ganglion cell. J Neurosci 8:623–642PubMedGoogle Scholar
  50. 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 325–348Google Scholar
  51. Strettoi E, Masland RH (1996) The number of unidentified amacrine cells in the mammalian retina. Proc Natl Acad Sci USA 93:14906–14911CrossRefPubMedGoogle Scholar
  52. 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 325:152–168CrossRefPubMedGoogle Scholar
  53. Strettoi E, Dacheux RF, Raviola E (1994) Cone bipolar cells as interneurons in the rod pathway of the rabbit retina. J Comp Neurol 347:139–149CrossRefPubMedGoogle Scholar
  54. Tauchi M, Masland RH (1984) The shape and arrangement of the cholinergic neurons in the rabbit retina. Proc R Soc Lond [Biol] 223:101–119CrossRefGoogle Scholar
  55. Trexler EB, Li W, Mills SL, Massey SC (2001) Coupling from AII amacrine cells to ON cone bipolar cells is bidirectional. J Comp Neurol 437:408–422CrossRefPubMedGoogle Scholar
  56. Trexler EB, Li W, Massey SC (2005) Simultaneous contribution of two rod pathways to AII amacrine and cone bipolar cell light responses. J Neurophysiol 93:1476–1485CrossRefPubMedGoogle Scholar
  57. Vaney DI (1984) “Coronate” amacrine cells in the rabbit retina have the “starburst” dendritic morphology. Proc R Soc Lond [Biol] 220:501–508CrossRefGoogle Scholar
  58. Vaney DI (1986) Morphological identification of serotonin-accumulating neurons in the living retina. Science 233:444–446CrossRefPubMedGoogle Scholar
  59. Vaney DI (1990) The mosaic of amacrine cells in the mammalian retina. Prog Retin Res 9:49–100CrossRefGoogle Scholar
  60. Vaney DI (1997) Neuronal coupling in rod-signal pathways of the retina. Invest Ophthalmol Vis Sci 38:267–273PubMedGoogle Scholar
  61. Wässle H (2004) Parallel processing in the mammalian retina. Nat Rev Neurosci 5:747–757CrossRefPubMedGoogle Scholar
  62. Wässle H, Boycott BB (1991) Functional architecture of the mammalian retina. Physiol Rev 71:447–480PubMedGoogle Scholar
  63. Wässle H, Yamashita M, Greferath U, Grünert U, Müller F (1991) The rod bipolar cell of the mammalian retina. Vis Neurosci 7:99–112CrossRefPubMedGoogle Scholar
  64. 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 361:537–551CrossRefPubMedGoogle Scholar
  65. Xin D, Bloomfield SA (1999) Comparison of the responses of AII amacrine cells in the dark- and light-adapted rabbit retina. Vis Neurosci 16:653–665CrossRefPubMedGoogle Scholar
  66. Young HM, Vaney DI (1991) Rod-signal interneurons in the rabbit retina. 1. Rod bipolar cells. J Comp Neurol 310:139–153CrossRefPubMedGoogle Scholar
  67. Zhang J, Li W, Trexler EB, Massey SC (2002) Confocal analysis of reciprocal feedback at rod bipolar terminals in the rabbit retina. J Neurosci 22:10871–10882PubMedGoogle Scholar
  68. Zhang J, Li W, Hoshi H, Mills SL, Massey SC (2005) Stratification of alpha ganglion cells and ON/OFF directionally selective ganglion cells in the rabbit retina. Vis Neurosci 22:535–549CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Shin Ae Kim
    • 1
  • Choong Ki Jung
    • 1
  • Tae-Hoon Kang
    • 1
  • Ji Hyun Jeon
    • 1
  • Jiook Cha
    • 1
  • In-Beom Kim
    • 1
  • Myung-Hoon Chun
    • 1
  1. 1.Department of Anatomy, College of MedicineThe Catholic University of KoreaSeoulKorea

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