Advertisement

Journal of Computational Neuroscience

, Volume 21, Issue 2, pp 131–151 | Cite as

The temporal structure of transient ON/OFF ganglion cell responses and its relation to intra-retinal processing

  • Andreas Thiel
  • Martin Greschner
  • Josef Ammermüller
Article

Abstract

A subpopulation of transient ON/OFF ganglion cells in the turtle retina transmits changes in stimulus intensity as series of distinct spike events. The temporal structure of these event sequences depends systematically on the stimulus and thus carries information about the preceding intensity change. To study the spike events' intra-retinal origins, we performed extracellular ganglion cell recordings and simultaneous intracellular recordings from horizontal and amacrine cells. Based on these data, we developed a computational retina model, reproducing spike event patterns with realistic intensity dependence under various experimental conditions. The model's main features are negative feedback from sustained amacrine onto bipolar cells, and a two-step cascade of ganglion cell suppression via a slow and a fast transient amacrine cell. Pharmacologically blocking glycinergic transmission results in disappearance of the spike event sequence, an effect predicted by the model if a single connection, namely suppression of the fast by the slow transient amacrine cell, is weakened. We suggest that the slow transient amacrine cell is glycinergic, whereas the other types release GABA. Thus, the interplay of amacrine cell mediated inhibition is likely to induce distinct temporal structure in ganglion cell responses, forming the basis for a temporal code.

Keywords

Retinal circuitry Temporal coding Amacrine cells Glycine Reciprocal feedback Concatenated inhibition Computational model 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Ammermüller J, Kolb H (1995) The organization of the turtle inner retina. I. ON and OFF-center pathways. J. Comp. Neurol. 358: 1–34.PubMedCrossRefGoogle Scholar
  2. Ammermüller J, Muller J, Kolb H (1995) The organization of the turtle inner retina. II. Analysis of color-coded and directionally selective cells. J. Comp. Neurol. 358: 35–62.PubMedCrossRefGoogle Scholar
  3. Ammermüller J, Kolb H (1996) Functional architecture of the turtle retina. Prog. Retin. Eye Res. 15: 393–433.CrossRefGoogle Scholar
  4. Ariel M, Daw NW, Rader RK (1983) Rhythmicity in rabbit retinal ganglion cell responses. Vision Res. 23: 1485–1493.PubMedCrossRefGoogle Scholar
  5. Awatramani GB, Slaughter MM (2000) Origin of transient and sustained responses in ganglion cells of the retina. J. Neurosci. 20: 7087–7095.PubMedGoogle Scholar
  6. Belgum JH, Dvorak DR, McReynolds JS (1982) Sustained synaptic input to ganglion cells of mudpuppy retina. J. Physiol. 326: 91–108.PubMedGoogle Scholar
  7. Belgum JH, Dvorak DR, McReynolds JS (1983) Sustained and transient synaptic inputs to ON – OFF ganglion cells in the mudpuppy retina. J. Physiol. 340: 599–610.PubMedGoogle Scholar
  8. Belgum JH, Dvorak DR, McReynolds JS (1984) Strychnine blocks transient but not sustained inhibition in mudpuppy retinal ganglion cells. J. Physiol. 354: 273–286.PubMedGoogle Scholar
  9. Berry MJ, Brivanlou IH, Jordan TA, Meister M (1999) Anticipation of moving stimuli by the retina. Nature 398: 334–338.PubMedCrossRefGoogle Scholar
  10. Berry MJ, Warland DK, Meister M (1997) The structure and precision of retinal spike trains. Proc. Natl. Acad. Sci. USA 94: 5411–5416.PubMedCrossRefGoogle Scholar
  11. Berry MJ, Meister M (1998) Refractoriness and neural precision. J. Neurosci. 18: 2200–2211.PubMedGoogle Scholar
  12. Bowling DB (1980) Light response of ganglion cells in the retina of the turtle. J. Physiol. 299: 173–196.PubMedGoogle Scholar
  13. Burns ME, Lamb TD (2003) Visual transduction by rod and cone photoreceptors. In: LM Chalupa, JH Werner, eds. Visual Neurosciences. MIT Press, Cambridge, MA, pp. 215–233.Google Scholar
  14. Cajal SR y (1892) The structure of the retina (Thorpe SA and Glickstein M, trans 1972) Thomas, Springfield, IL.Google Scholar
  15. Dearworth JR, Granda AM (2002) Multiplied functions unify shapes of ganglion-cell receptive fields in retina of turtle. J. Vis. 2: 204–217.PubMedGoogle Scholar
  16. Dowling JE (1987) The retina: An approachable part of the brain. Belknapp Press, Cambridge, MA.Google Scholar
  17. Eckhorn R, Reitboeck HJ, Arndt M, Dicke P (1990) Feature linking via synchronization among distributed assemblies: Simulations of results from cat visual cortex. Neural Comput. 2: 293–307.Google Scholar
  18. Eldred WD, Cheung K (1989) Immunocytochemical localization of glycine in the retina of the turtle (Pseudemys scripta). Vis. Neurosci. 2: 331–338.PubMedGoogle Scholar
  19. Flannery BP, Teukolski SA, Press WH, Vettering WT (1993) Numerical recipes in C. Cambridge UP, Cambridge, MA.Google Scholar
  20. Gaudiano P (1994) Simulations of X and Y retinal ganglion cell behavior with a nonlinear push-pull model of spatiotemporal retinal processing. Vision Res. 34: 1767–1784.PubMedCrossRefGoogle Scholar
  21. Golcich MA, Morgan IG, Dvorak DR (1990) Selective abolition of OFF-responses in kainic acid-lesioned chicken retina. Brain Res. 535: 288–300.PubMedCrossRefGoogle Scholar
  22. Granda AM, Fulbrook JE (1989) Classification of turtle retinal ganglion cells. J. Neurophysiol. 62: 723–737.PubMedGoogle Scholar
  23. Guiloff GD, Jones J, Kolb H (1988) Organization of the inner plexiform layer of the turtle retina: An electron microscopic study. J. Comp. Neurol. 272: 280–292.PubMedCrossRefGoogle Scholar
  24. Hennig MH, Funke K (2001) A biophysically realistic simulation of the vertebrate retina. Neurocomputing 38–40: 659–665.CrossRefGoogle Scholar
  25. Hennig MH, Funke K, Wörgötter F (2002) The influence of different retinal subcircuits on the nonlinearity of ganglion cell behavior. J. Neurosci. 22: 8726–8738.PubMedGoogle Scholar
  26. Itzhaki A, Perlman I (1984) Light adaptation in luminosity horizontal cells in the turtle retina. Vision Res. 24: 1119–1126.PubMedCrossRefGoogle Scholar
  27. Jensen RJ, DeVoe RD (1982) Ganglion cells and (dye-coupled) amacrine cells in the turtle retina that have possible synaptic connection. Brain Res. 240: 146–150.PubMedCrossRefGoogle Scholar
  28. Keat J, Reinagel P, Reid RC, Meister M (2001) Predicting every spike: A model for the responses of visual neurons. Neuron 30: 803–817.PubMedCrossRefGoogle Scholar
  29. Kenyon GT, Moore B, Jeffs J, Denning KS, Stephens GJ, Travis BJ, George JS, Theiler J, Marshak DW (2003) A model of high-freqeuncy oscillatory potentials in retinal ganglion cells. Vis. Neurosci. 20: 465–480.PubMedCrossRefGoogle Scholar
  30. Kittila CA, Granda AM (1994) Functional morphologies of retinal ganglion cells in the turtle. J. Comp. Neurol. 350: 623–645.PubMedCrossRefGoogle Scholar
  31. Lukasiewicz PD, Werblin FS (1990) The spatial distribution of excitatory and inhibitory inputs to ganglion cell dendrites in the tiger salamander retina. J. Neurosci. 10: 210–221.PubMedGoogle Scholar
  32. Lukasiewicz PD, Lawrence JE, Valentino TL (1995) Desensitizing glutamate receptors shape excitatory synaptic inputs to tiger salamander retinal ganglion cells. J. Neurosci. 15: 6189–6199.PubMedGoogle Scholar
  33. MacNeil MA, Masland RH (1998) Extreme diversity among amacrine cells: implications for function. Neuron 20: 971–982.PubMedCrossRefGoogle Scholar
  34. Maguire G, Lukasiewicz PD, Werblin FS (1989) Amacrine cell interactions underlying the response to change in the tiger salamander retina. J. Neurosci. 10: 210–221.Google Scholar
  35. Mainen ZF, Sejnowski TJ (1995) Reliability of spike timing in neocortical neurons. Science 268: 1503–1506.PubMedGoogle Scholar
  36. Marchiafava PL (1979) The responses of retinal ganglion cells to stationary and moving visual stimuli. Vision Res. 19: 1203–1211.PubMedCrossRefGoogle Scholar
  37. Marchiafava PL, Weiler R (1982) The photoresponses of structurally identified amacrine cells in the turtle retina. Proc. Royal Soc. London B 214: 403–415.CrossRefGoogle Scholar
  38. Masland RH (2001a) Neuronal diversity in the retina. Curr. Opin. Neurobiol. 11: 431–436.PubMedCrossRefGoogle Scholar
  39. Masland RH (2001b) The fundamental plan of the retina. Nat. Neurosci. 4: 877–886.PubMedCrossRefGoogle Scholar
  40. Miller RF (1979) The neuronal basis of ganglion cell receptive field organization and the physiology of amacrine cells. In: FO Schmitt, FG Worden, eds. The Neuroscience, Fourth Study Program. MIT Press, Cambridge, MA. pp. 227–245.Google Scholar
  41. Miller RF, Dacheux RF (1976) Synaptic organization and ionic basis of ON and OFF channels in the mudpuppy retina. III. A model of ganglion cell receptive field organization based on chloride-free experiments. J. Gen. Physiol. 67: 679–690.CrossRefPubMedGoogle Scholar
  42. Morgan IG (1992) What do amacrine cells do? Prog. Retin. Res. 11: 193–214.CrossRefGoogle Scholar
  43. Muller JF, Ammermüller J, Normann RA, Kolb H (1991) Synaptic inputs to physiologically defined turtle retinal ganglion cells. Vis. Neurosci. 7: 409–429.PubMedGoogle Scholar
  44. Müller F, Kaupp UB (1998) Signaltransduktion in Sehzellen. Naturwissenschaften 85: 49–61.PubMedCrossRefGoogle Scholar
  45. Netzer E, DeKorver L, Ammermüller J, Kolb H (1997) Neural circuitry and light responses of the dopamine amacrine cell in the turtle retina. Mol. Vis. 3: 6–12.PubMedGoogle Scholar
  46. Nirenberg S, Meister M (1997) The light response of retinal ganglion cells is truncated by a displaced amacrine cell circuit. Neuron 18: 637–650.PubMedCrossRefGoogle Scholar
  47. Normann RA, Perlman I (1979a) The effect of background illumination on the photoresponses of red and green cones. J. Physiol. 286: 491–507.PubMedGoogle Scholar
  48. Normann RA, Perlman I (1979b) Signal transmission from red cones to horizontal cells in the turtle retina. J. Physiol. 286: 509– 524.PubMedGoogle Scholar
  49. Puchalla JL, Schneidmann E, Harris RA, Berry MJ (2005) Redundancy in the population code of the retina. Neuron 46: 493–504.PubMedCrossRefGoogle Scholar
  50. Roska B, Nemeth E, Werblin F (1998) Response to change is facilitated by a three-neuron disinhibitory pathway in the tiger salamander retina. J. Neurosci. 18: 3451–3459.PubMedGoogle Scholar
  51. Sakai HM, Naka K-I (1987a) Signal transmission in the catfish retina. IV. Transmission to ganglion cells. J. Neurophysiol. 58: 1307–1328.PubMedGoogle Scholar
  52. Sakai HM, Naka K-I (1987b) Signal transmission in the catfish retina. V. Sensitivity and circuit. J. Neurophysiol. 58: 1329–1350.PubMedGoogle Scholar
  53. Sakai HM, Naka K-I (1988) Neuron network in catfish retina. Prog. Retin. Res. 7: 149–208.CrossRefGoogle Scholar
  54. Schwartz EA (1973) Organization of ON-OFF cells in the retina of the turtle. J. Physiol. 230: 1–14.PubMedGoogle Scholar
  55. Sestokas AK, Lehmkuhle S, Kratz KE (1991) Relationship between response latency and amplitude for ganglion and geniculate X- and Y-cells in the cat. Int. J. Neurosci. 60: 59–64.PubMedGoogle Scholar
  56. Teeters J, Jacobs A, Werblin F (1997) How neural interactions form neural responses in the salamander retina. J. Comput. Neurosci. 4: 5–27.PubMedCrossRefGoogle Scholar
  57. Toyoda J, Hashimoto H, Ohtsu K (1973) Bipolar-amacrine transmission in the carp retina. Vision Res. 13: 295–307.PubMedCrossRefGoogle Scholar
  58. van Hateren JH (1997) Processing of natural time series of intensities by the visual system of the blowfly. Vision Res. 37: 3407–3416.PubMedCrossRefGoogle Scholar
  59. van Hateren JH, Rüttiger L, Sun H, Lee BB (2002) Processing of natural temporal stimuli by macaque retinal ganglion cells. J. Neurosci. 22: 9945–9960.PubMedGoogle Scholar
  60. Victor JD (1987) The dynamics of the cat retinal X cell centre. J. Physiol. 386: 219–246.PubMedGoogle Scholar
  61. Victor JD, Purpura KP (1996) Nature and precision of temporal coding in visual cortex: A metric-space analysis. J. Neurophysiol. 76: 1310–1326.PubMedGoogle Scholar
  62. Vigh J, Witkovsky P (2004) Neurotransmitter actions on transient amacrine and ganglion cells of the turtle retina. Vis. Neurosci. 21: 1–11.PubMedCrossRefGoogle Scholar
  63. Werblin FS, Dowling JE (1969) Organization of the retina of the mudpuppy, Necturus maculosus. II. Intracellular recording. J. Neurophysiol. 32: 339–355.PubMedGoogle Scholar
  64. Werblin FS (1977) Regenerative amacrine cell depolarization and the formation of ON – OFF ganglion cell response. J. Physiol. 264: 767–785.PubMedGoogle Scholar
  65. Werblin FS, Maguire G, Lukasiewicz PD, Eliasof S, Wu SM (1988) Neural interactions mediating the detection of motion in the retina of the tiger salamander. Vis. Neurosci. 1: 317–329.PubMedGoogle Scholar
  66. Weiler R, Ball AK, Ammermüller J (1991) Neurotransmitter systems in the turtle retina. Prog. Retin. Res. 10: 1–26.CrossRefGoogle Scholar
  67. Wilson HR (1997) A neural model of foveal light adaptation and afterimage formation. Vis. Neurosci. 14: 403–423.PubMedGoogle Scholar
  68. Zhagloul KA, Boahen K (2004) Optic nerve signals in a neuromorphic chip I: outer and inner retina models. IEEE Trans. Bio-Med. Eng. 51: 657–666.CrossRefGoogle Scholar
  69. Zucker CL, Ehinger B (1993) Synaptic connections involving immunoreactive glycine receptors in the turtle retina. Vis. Neurosci. 10: 907–914.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science + Business Media, LLC 2006

Authors and Affiliations

  • Andreas Thiel
    • 1
  • Martin Greschner
    • 1
  • Josef Ammermüller
    • 1
  1. 1.NeurobiologyCarl von Ossietzky University OldenburgOldenburgGermany

Personalised recommendations