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A unified neural model of spatiotemporal processing in X and Y retinal ganglion cells

I. Analytical results

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Abstract

This work presents unified analyses of spatial and temporal visual information processing in a feed-forward network of neurons that obey membrane, or shunting equations. The feed-forward shunting network possesses properties that make it well suited for processing of static, spatial information. However, it is shown here that those same properties of the shunting network that lead to good spatial processing imply poor temporal processing characteristics. This article presents an extension of the feed-forward shunting network model that solves this problem by means of preprocessing layers. The anatomical interpretation of the resulting model is structurally analogous to recently discovered data on a retinal circuit connecting cones to retinal ganglion cells through pairs of pushpull bipolar cells. Mathematical analysis of the lumped model leads to the hypothesis that X and Y retinal ganglion cells may consist of a single mechanism acting in different parameter ranges. This hypothesis is confirmed in the companion article, wherein the model in conjunction with a nonlinear temporal adaptation mechanism — is used to reproduce experimental data of both X and Y cells by simple changes in morphological and physiological parameters.

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References

  1. Barlow HB (1953) Summation and inhibition in the frog retina. J Physiol (London) 119:69–88

  2. Baylor DA, Hodgkin L (1974), Changes in time scale and sensitivity in turtle photoreceptors. J Physiol (London) 242:729–758

  3. Boycott BB, Wässle H (1974) The morphological types of ganglion cells of the domestic cat's retina. J Physiol (London) 240:397–419

  4. Carpenter GA, Grossberg S (1981) Adaptation and transmitter gating in vertebrate photoreceptors. J Theor Neurobiol 1:1–42

  5. Cleland BG, Levick WR (1974) Brisk and sluggish concentrically organized ganglion cells in the cat's retina. J Physiol (London) 240:421–456

  6. Dowling JE (1987) The retina: an approachable part of the brain. Belknap, Cambridge

  7. Enroth-Cugell C, Robson JG (1966) The contrast sensitivity of retinal ganglion cells of the cat. J Physiol (London) 187:517–552

  8. Freed MA, Sterling P (1988) The ON-alpha ganglion cell of the cat retina and its presynaptic cell types. J Neurosci 8:2303–2320

  9. Fukuda Y, Hsiao CF, Watanabe M, Ito H (1984) Morphological correlates of physiologically identified Y, X and W cells in the cat retina. J Neurophysiol (London) 52:999–1013

  10. Furman GG (1965) Comparison of models for subtractive and shunting lateral-inhibition in receptor-neuron fields. Kybernetyk 2:257–274

  11. Gaudiano P (1991) Neural network models for spatio-temporal visual processing and adaptive sensory-motor control. Unpublished Doctoral Dissertation, Boston University

  12. Gaudiano P (1992) A unified neural network model of spatiotemporal processing in X and Y retinal ganglion cells. II: Temporal adaptation and simulation of experimental data. Biol Cybern (this issue)

  13. Grossberg S (1970) Neural pattern discrimination. J Theor Biol 27:291–337

  14. Grossberg S (1973) Contour enhancement, short-term memory, and constancies in reverberating neural networks. Studies Appl Math 52:217–257

  15. Grossberg S (1980) Intracellular mechanisms of adaptation and selfregulation in self-organizing networks: the role of chemical transducers. Bull Math Biol 42:365–396

  16. Grossberg S (1983) The quantized geometry of visual space: The coherent computation of depth, form, and lightness. Behav Brain Sci 6:625–692

  17. Grossberg S (1988) Nonlinear neural networks: Principles, mechanisms, and architectures. Neural Networks 1:17–61

  18. Hochstein S, Shapley RM (1976a) Quantitative analysis of retinal ganglion cell classifications. J Physiol (London) 262:237–264

  19. Hochstein S, Shapley RM (1976b) Linear and nonlinear spatial subunits in Y cat retinal ganglion cells. J Physiol (London) 262:265–284

  20. Hodgkin AL (1964) The conduction of the nervous impulse. Liverpool University Press, Liverpool

  21. Koch C, Poggio T, Torre V (1983) Nonlinear interactions in a dendritic tree: localization, timing and role in information processing. Proc Natl Acad Sci USA 80:2799–2802

  22. Kolb H, Nelson R, Mariani A (1981) Amacrine cells, bipolar cells and ganglion cells of the cat retina: a Golgi study. Vision Res 21:1081–1114

  23. Kuffler SW (1953) Discharge patterns and functional organization of the mammalian retina. J Physiol (London) 16:37–68

  24. Lennie P, Trevarthen C, Van Essen D, Wässle H (1990) Parallel processing of visual information. In: Spillman L, Werner W (eds) Visual perception: the neurophysiological foundations, chap 6. Academic Press, San Diego, pp 103–128

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

  26. Pinter RB (1985) Adaptation of spatial modulation transfer functions via nonlinear lateral inhibition. Biol Cybern 51:285–291

  27. Rodieck RW (1965) Quantitative analysis of cat retinal ganglion cell response to visual stimuli. Vision Res 5:583–601

  28. Saito H (1983) Morphology of physiologically identified X-, Y- and W-type retinal ganglion cells of the cat. J Comp Neurol 221:279–288

  29. Schiller P (1982) Central connections of the retinal On and Off pathways. Nature 297:580–583

  30. Slaughter MM, Miller RF (1981) 2-Amino-4-phosphonobutyric acid: a new pharmacological tool for retina research. Science 211:182–185

  31. Sperling G (1970) Model of visual adaptation and contrast detection. Percept Psychophys 8:143–157

  32. Sperling G, Sondhi MM (1968) Model for visual luminance discrimination and flicker detection. J Opt Soc Am 58:1133–1145

  33. Sterling P (1990) Retina. In: Shepherd GM (ed) The synaptic organization of the brain, 3rd edn, chap 6. Oxford University Press, New York, pp 170–213

  34. Werblin F (1971) Adaptation in a vertebrate retina: Intracellular recordings in Necturus. J Neurophysiol 34:228–241

  35. Werblin F, Dowling JE (1969) Organization of the retina of the mudpuppy, Necturus maculosus. II. Intracellular recording. J Neurophysiol 32:339–355

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Gaudiano, P. A unified neural model of spatiotemporal processing in X and Y retinal ganglion cells. Biol. Cybern. 67, 11–21 (1992). https://doi.org/10.1007/BF00201798

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Keywords

  • Visual Information
  • Spatial Information
  • Retinal Ganglion Cell
  • Parameter Range
  • Bipolar Cell