Signal Processing in the Crayfish Optic Lobe: Contrast, Motion and Polarization Vision

  • Raymon M. Glantz
  • Clyde S. Miller
Conference paper

Abstract

Between 1952 and 1978, C.A.G. Wiersma and several coworkers surveyed the integrative properties of the neurons in the decapod optic tract. A comparative analysis of lobsters, crayfish, and crabs (summarized in Wiersma et al. 1982) revealed a sophisticated, parallel distributed information pathway. In each species, all or most of the visual field is simultaneously analyzed by multiple classes of interneurons. Thus, contrast polarity, and local and global motion are assessed across the panoramic visual space at multiple loci defined by the visual receptive fields. Several neuron classes (e.g., sustaining fibers) were discovered in each species, and the members of each class are uniquely distinguished by their receptive fields. The number of neurons in each class is small (e.g., there are 14 sustaining fibers in the crayfish Procambarus clarkii) and their receptive fields overlap extensively. There are several types of motion detectors, sustaining and dimming fibers, cells that track moving objects (seeing fibers) and space constant fibers with visual receptive fields modulated by signals from the statocysts.

Keywords

Retina NMDA Acetylcholine Ghost Mellon 

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References

  1. Atwood H (1980) Synapses and neurotransmitters. In: Atwood HL, Sandeman DC (eds) Biology of Crustacea, vol 3. Academic Press, New York, pp 105–150Google Scholar
  2. Brodie SE, Knight BW, Ratliff F (1978) The spatiotemporal transfer function of the Limulus lateral eye. J Gen Physiol 72: 167–202PubMedCrossRefGoogle Scholar
  3. Cummins D, Goldsmith TH (1981) Cellular identification of the violet receptor in the crayfish eye. J Comp Physiol 142: 199–202CrossRefGoogle Scholar
  4. Dubs A (1982) The spatial integration of signals in the retina and lamina of the fly compound eye of different conditions of luminance. J Comp Physiol 146: 321–343CrossRefGoogle Scholar
  5. Fuortes MGF, Hodgkin AL (1964) Changes in time scale and sensitivity in the ommatidia of Limulus. J Physiol 172: 239–263PubMedGoogle Scholar
  6. Glantz RM (1977) Visual input and motor output of command interneurons of the defense reflex pathway in the crayfish. In: Hoyle G (ed) Identified neurons and behavior in arthropods. Plenum, New York, pp 259–274CrossRefGoogle Scholar
  7. Glantz RM (1991) Motion detection and adaptation in crayfish photoreceptors. J Gen Physiol 97: 777–797PubMedCrossRefGoogle Scholar
  8. Glantz RM (1994) Directional selectivity in a nonspiking interneuron of the crayfish optic lobe: evaluation of a linear model. J Neurophysiol 72: 180–193PubMedGoogle Scholar
  9. Glantz RM (1996a) Polarization sensitivity in crayfish lamina monopolar neurons. J Comp Physiol A 178: 413–425CrossRefGoogle Scholar
  10. Glantz RM (1996b) Polarization sensitivity in the crayfish optic lobe: peripheral contributions to opponency and directionally selective motion detection. J Neurophysiol 76: 3404–3414PubMedGoogle Scholar
  11. Glantz RM (1998) Directionality and inhibition in crayfish tangential cells. J Neurophysiol 79: 1157–1166PubMedGoogle Scholar
  12. Glantz RM, Bartels A (1994) The spatiotemporal transfer function of crayfish lamina monopolar neurons. J Neurophysiol 71: 2168–2182PubMedGoogle Scholar
  13. Glantz RM, Mclsaac A (1998) Two-channel polarization analyzer in the sustaining fiber-dimming fiber ensemble of crayfish visual system. J Neurophysiol 80: 2571–2583PubMedGoogle Scholar
  14. Glantz RM, Nudelman HB (1976) Sustained, synchronous oscillations in discharge of sustaining fibers of crayfish optic nerve. J Neurophysiol 39: 1257–1271PubMedGoogle Scholar
  15. Glantz RM, Nudelman HB (1988) Interval coding and band-pass filtering at oculomotor synapses in crayfish. J Neurophysiol 59: 56–76PubMedGoogle Scholar
  16. Glantz RM, Nudelman HB, Waldrop B (1984) Linear integration of convergent visual inputs in an oculomotor reflex pathway. J Neurophysiol 52: 1213–1225PubMedGoogle Scholar
  17. Glantz RM, Wyatt C, Mahncke H (1995) Directionally selective motion detection in the sustaining fibers of the crayfish optic nerve: linear and nonlinear mechanisms. J Neurophysiol 74:142–152PubMedGoogle Scholar
  18. Glantz RM, Miller CS, Nässei DR (2000) Tachykinin-related peptide and GABA-mediated presynaptic inhibition of crayfish photoreceptors. J Neurosci (in press)Google Scholar
  19. Hirsch R (1977) Crustacean optomotor memory. In: Hoyle G (ed) Identified neurons and behavior in arthropods. Plenum, New York, pp 405–421CrossRefGoogle Scholar
  20. Hisada M, Sugawara K, Higuchi T (1969) Visual and geotactic control of compensatory eyecup movements in the crayfish, Procambarus clarkii. J Fac Sci Hokkaido Univ Ser VI Zool 17: 224–239Google Scholar
  21. Horridge GA (1966) Optokinetic memory in the crab Carcinus. J Exp Biol 44: 233–245PubMedGoogle Scholar
  22. Johnson DH, Gruner CM, Glantz RM (2000) Quantifying information transfer in spike generation. Neurocomputing 32–33: 1047–1054CrossRefGoogle Scholar
  23. Kirk MD, Waldrop B, Glantz RM (1982) The crayfish sustaining fibers. I. Morphological representation of visual receptive fields in the second optic neuropile. J Comp Physiol 146: 175–179CrossRefGoogle Scholar
  24. Kirk MD, Waldrop B, Glantz RM (1983) A quantitative correlation of contour sensitivity with dendritic density in an identified visual neuron. Brain Res 274: 231–237PubMedCrossRefGoogle Scholar
  25. Knight B, Toyoda J-I, Dodge FA (1970) A quantitative description of the dynamics of excitation and inhibition in the eye of Limulus. J Gen Physiol 56: 421–437PubMedCrossRefGoogle Scholar
  26. Krausz H, Naka K-I (1980) Spatiotemporal testing and modeling of catfish retinal neurons. Biophysical J 29: 13–36CrossRefGoogle Scholar
  27. Miller CS, Glantz RM (2000) Measurement and simulation of stimulus and response in the dorsal light reflex of the crayfish. 9th Annu Computational Neuroscience Meet Abstr 99 ppGoogle Scholar
  28. Nalbach H-O, Nalbach G, Furzin L (1989) Visual control of eyestalk orientation in crabs: vertical optokinetics, visual fixation on the horizon and eye design. J Comp Physiol 165: 577–587CrossRefGoogle Scholar
  29. Nässel DR, Waterman TH (1977) Golgi EM evidence for visual information channeling in crayfish lamina ganglionaris. Brain Res 130: 556–563CrossRefGoogle Scholar
  30. Neil DM (1982) Compensatory eye movements. In: Bliss DE (ed) Biology of Crustacea. Academic Press, New York, pp 133–163Google Scholar
  31. Okada Y, Yamaguchi T (1988) Nonspiking giant interneurons in the crayfish brain: morphological and physiological characteristics of the neurons postsynaptic to visual interneurons. J Comp Physiol 162: 705–714CrossRefGoogle Scholar
  32. Pfeiffer C, Glantz RM (1989) Cholinergic synapses and the organization of contrast detection in the crayfish optic lobe. J Neurosci 9: 1872–1882PubMedGoogle Scholar
  33. Pfeiffer-Linn C, Glantz RM (1989) Acetylcholine and GAB A mediate opposing actions on neuronal chloride channels in crayfish. Science 245: 1249–1251PubMedCrossRefGoogle Scholar
  34. Pfeiffer-Linn C, Glantz RM (1991a) An arthropod NMDA receptor. Synapse 9: 35–42PubMedCrossRefGoogle Scholar
  35. Pfeiffer-Linn C, Glantz RM (1991b) GABA-mediated inhibition of visual interneurons in the crayfish medulla. J Comp Physiol A 168: 373–381CrossRefGoogle Scholar
  36. Reid RC, Soodak RE, Shapley RM (1991) Directional selectivity and spatiotemporal structure of receptive fields of simple cells in cat striate cortex. J Neurophsyiol 66: 505–529Google Scholar
  37. Sandeman DC, Kien J, Erber J (1975) Optokinetic eye movements in the crab Carcinus. II Responses of optokinetic interneurons. J Comp Physiol 101: 259–274CrossRefGoogle Scholar
  38. Schöne H, Schöne H (1961) Eyestalk movements induced by polarized light in the ghost crab, Ocypode quadrata. Science 134: 675–676CrossRefGoogle Scholar
  39. Shaw S (1966) Polarized light responses from crab retinula cells. Nature Lond 211: 92–93PubMedCrossRefGoogle Scholar
  40. Strausfeld N, Nässel DR (1981) Neuroarchitectures serving compound eyes of Crustacea and insects. In: Autrum H (ed) Handbook of sensory physiology, vol VII/6B. Springer, Berlin Heidelberg New York, pp 1–132Google Scholar
  41. Waldrop B, Glantz RM (1985a) Synaptic mechanisms of a tonic EPSP in crustacean visual interneurons: analysis and simulation. J Neurophysiol 54: 636–650PubMedGoogle Scholar
  42. Waldrop B, Glantz RM (1985b) Nonspiking local interneurons mediate surround inhibition of crayfish sustaining fibers. J Comp Physiol 156: 763–774CrossRefGoogle Scholar
  43. Wang-Bennett L, Glantz RM (1987a) Functional organization of the crayfish lamina ganglionaris. I. Nonspiking monopolar cells. J Comp Physiol A 161: 131–145PubMedCrossRefGoogle Scholar
  44. Wang-Bennett L, Glantz RM (1987b) Functional organization of the crayfish lamina ganglionaris. II. Large field spiking and non-spiking cells. J Comp Physiol A 161: 147–160PubMedCrossRefGoogle Scholar
  45. Waterman TH (1981) Polarization sensitivity. In: Autrum H (ed) Handbook of sensory physiology, vol VII/6B. Springer, Berlin Heidelberg New York, pp 261–469Google Scholar
  46. Waterman TH, Wiersma CAG (1963) Electrical responses in decapod crustacean visual systems. J Cell Comp Physiol 61: 1–16PubMedCrossRefGoogle Scholar
  47. Wiersma CAG, Oberjat T (1968) The selective responsiveness of various crayfish oculomotor fibers to sensory stimuli. Comp Biochem Physiol 26: 1–16PubMedCrossRefGoogle Scholar
  48. Wiersma CAG, Yamaguchi T (1967) Integration of visual stimuli by the crayfish central nervous system. J Exp Biol 47: 409–431PubMedGoogle Scholar
  49. Wiersma CAG, Roach JLM, Glantz RM (1982) Neural integration in the optic system. In: Sandeman DC, Atwood HL (eds) The biology of Crustacea. Vol 4: Neural integration and behavior. Academic Press, New York, pp 1–31Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2002

Authors and Affiliations

  • Raymon M. Glantz
    • 1
  • Clyde S. Miller
    • 1
  1. 1.Department of Biochemistry and Cell BiologyRice UniversityHoustonUSA

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