Journal of Computational Neuroscience

, Volume 2, Issue 1, pp 5–18

Mechanisms of dendritic integration underlying gain control in fly motion-sensitive interneurons

  • Alexander Borst
  • Martin Egelhaaf
  • Jürgen Haag
Article

Abstract

In the compensatory optomotor response of the fly the interesting phenomenon of gain control has been observed by Reichardt and colleagues (Reichardt et al., 1983): The amplitude of the response tends to saturate with increasing stimulus size, but different saturation plateaus are assumed with different velocities at which the stimulus is moving. This characteristic can already be found in the motion-sensitive large field neurons of the fly optic lobes that play a role in mediating this behavioral response (Hausen, 1982; Reichardt et al, 1983; Egelhaaf, 1985; Haag et al., 1992). To account for gain control a model was proposed involving shunting inhibition of these cells by another cell, the so-called pool cell (Reichardt et al., 1983), both cells sharing common input from an array of local motion detectors. This article describes an alternative model which only requires dendritic integration of the output signals of two types of local motion detectors with opposite polarity. The explanation of gain control relies on recent findings that these input elements are not perfectly directionally selective and that their direction selectivity is a function of pattern velocity. As a consequence, the resulting postsynaptic potential in the dendrite of the integrating cell saturates with increasing pattern size at a level between the excitatory and inhibitory reversal potentials. The exact value of saturation is then set by the activation ratio of excitatory and inhibitory input elements which in turn is a function of other stimulus parameters such as pattern velocity. Thus, the apparently complex phenomenon of gain control can be simply explained by the biophysics of dendritic integration in conjunction with the properties of the motion-sensitive input elements.

Keywords

motion detection gain control visual interneuron dendritic integratio 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Borst A and Bahde S (1986) What kind of movement detector is triggering the landing response of the housefly?Biol. Cybern. 55:59–69.Google Scholar
  2. Borst A and Egelhaaf M (1989) Principles of visual motion detection.Trends Neumsci. 12:297–306.Google Scholar
  3. Borst A and Egelhaaf M (1990) Direction selectivity of fly motion-sensitive neurons is computed in a two-stage process.Proc. Natl. Acad. Sci. USA 87:9363–9367.Google Scholar
  4. Borst A and Egelhaaf M(1992) In vivo imaging of calcium accumulation in fly interneurons as elicited by visual motion stimulation.Proc. Natl. Acad. Sci. USA 89:4139–4143.Google Scholar
  5. Borst A and Egelhaaf M (1993) Detecting visual motion: Theory and models. In: FA Miles and J Wallman, eds. Visual motion and its role in the stabilization of gaze. Amsterdam, London, New York, Tokyo: Elsevier, pp. 3–27.Google Scholar
  6. Buchner E (1984) Behavioral analysis of spatial vision in insects. In: MA Ali, ed. Photoreception and vision in invertebrates. New York, London: Plenum Press, pp. 561–621.Google Scholar
  7. Carandini M and Heeger DJ (1994) Summation and division by neurons in primate visual cortex.Science 264:1333–1336.Google Scholar
  8. Dvorak DR, Bishop LG, and Eckert HE (1975) On the identification of movement detectors in the fly optic lobe.J. Comp. Physiol. 100:5–23.Google Scholar
  9. Egelhaaf M (1985) On the neuronal basis of figure-ground discrimination by relative motion in the visual system of the fly. I. Behavioral constraints imposed on the neuronal network and the role of the optomotor system.Biol. Cybern. 52:123–140.Google Scholar
  10. Egelhaaf M, Borst A, and Reichardt W (1989) Computational structure of a biological motion detection system as revealed by local detector analysis in the fly visual system.J. Opt. Soc. Am. A 6:1070–1087.Google Scholar
  11. Egelhaaf M, Borst A, and Pilz B (1990) The role of GABA in detecting visual motion.Brain Res. 509:156–160.Google Scholar
  12. Egelhaaf M and Borst A (1989) Transient and steady-state response properties of movement detectors.J. Opt. Soc. Am. A 6:116–127. Erata:J. Opt. Soc. Am. A 7:172.Google Scholar
  13. Egelhaaf M and Borst A (1993) Movement detection in arthropods. In: FA Miles and J Wallman, eds. Visual motion and its role in the stabilization of gaze. Amsterdam, London, New York, Tokyo: Elsevier, pp. 53–77.Google Scholar
  14. Geiger G and Nässei DR (1981) Visual orientation behavior of flies after selective laser beam ablation of interneurones.Nature 293:398–399.Google Scholar
  15. Geiger G and Nässei DR (1982) Visual processing of moving single objects and wide-field patterns in flies: behavioral analysis after laser-surgical removal of interneurons.Biol. Cybern. 44:141–149.Google Scholar
  16. Gilbert C (1991) Membrane conductance changes associated with the response of motion sensitive insect visual neurons.2. Naturforsch. 45c:1222–1224.Google Scholar
  17. Götz KG (1972) Principles of optomotor reactions in insects.Bibl. Ophthal. 82:251–259.Google Scholar
  18. Haag J, Egelhaaf J, and Borst A (1992) Dendritic integration of motion information in visual interneurons of the blowfly.Neurosci. Lett. 140:173–176.Google Scholar
  19. Haag J, Egelhaaf M, and Borst A (1993) Active membrane properties of motion-sensitive neurons of the fly Calliphora erythrocephala. In: N Elsner and M. Heisenberg, eds. Gene-Brain-Behavior. Proceedings of the 21th Göttingen Neurobiology Conference, p. 96.Google Scholar
  20. Haag J and Borst A (1994) Membrane parameters and potential spread in fly lobula-plate neurons. In: N Elsner and H Breer, eds. Göttingen Neurobiology Report 1994. Stuttgart, New York: Georg Thieme, p. 447.Google Scholar
  21. Hausen K (1976) Functional characterization and anatomical identification of motion sensitive neurons in the lobula plate of the blowfly Calliphora erythrocephala.Z. Naturforsch. 31c:629–633.Google Scholar
  22. Hausen K, Wolburg-Buchholz K, and Ribi WA (1980) The synaptic organization of visual interneurons in the lobula complex of flies.Cell Tissue Res. 208:371–387.Google Scholar
  23. Hausen K, (1982) Motion sensitive interneurons in the optomotor system of the fly. II. The Horizontal Cells: Receptive field organization and response characteristics.Biol. Cybern. 46:67–79.Google Scholar
  24. Hausen K and Wehrhahn C(1983) Microsurgical lesion of horizontal cells changes optomotor yaw response in the blowfly Calliphora erythocephala.Proc. R. Soc. Lond. B 219:211–216.Google Scholar
  25. Hausen K and Wehrhahn C (1990) Neural circuits mediating visual flight control in flies. II. Separation of two control systems by microsurgical brain lesions.J. Neumsci. 10:351–360.Google Scholar
  26. Heisenberg M, Wonneberger R, and Wolf R (1978) Optomotor-blind (H31)—a Drosophila mutant of the lobula plate giant neurons.J. Comp. Physiol. 124:287–296.Google Scholar
  27. Hengstenberg R (1982) Common visual response properties of giant vertical cells in the lobula plate of the blowfly Calliphora.J. Comp. Physiol. A 149:179–193.Google Scholar
  28. Hengstenberg R, Hausen K, and Hengstenberg B (1982) The number and structure of giant vertical cells (VS) in the lobula plate of the blowfly Calliphora erytrocephala.J. Comp. Physiol. A 149:163–177.Google Scholar
  29. Laurent G (1993) A dendritic gain control mechanism in axon-less neurons of the locust, Schistocerca americana.J. Physiol. 470:45–54.Google Scholar
  30. Pierantoni R (1976) A look into the cock-pit of the fly.Cell Tissue Res. 171:101–122.Google Scholar
  31. Poggio T, Reichardt W, and Hausen K (1981) A neural circuitry for relative movement discrimination by the visual system of the fly.Naturwiss 443:446.Google Scholar
  32. Reichardt W (1961) Autocorrelation, a principle for the evaluation of sensory information by the central nervous system. In: WA Rosenblith, ed. Sensory Communication. New York, London: The MIT Press and John Wiley & Sons, pp. 303–317.Google Scholar
  33. Reichardt W, Poggio T, and Hausen K (1983) Figure-Ground discrimination by relative movement in the visual system of the fly. Part II: Towards the neural circuitry.Biol. Cybern. 46:1–30.Google Scholar
  34. Reichardt W (1987) Evaluation of optical motion information by movement detectors.J. Comp. Physiol. A 161:533–547.Google Scholar
  35. Schmid A and Bülthoff H (1988) Using neuropharmacology to distinguish between excitatory and inhibitory movement detection mechanisms in the fly Calliphora erythrocephala.Biol. Cybern. 59:71–80.Google Scholar
  36. Segev I, Fleshman JW, and Burke RE (1989) Compartmental models of complex neurons. In: C Koch and I Segev, eds. Methods in neuronal modeling: From synapses to networks. Cambridge, London: MIT Press, pp. 63–96.Google Scholar

Copyright information

© Kluwer Academic Publishers 1995

Authors and Affiliations

  • Alexander Borst
    • 1
  • Martin Egelhaaf
    • 1
  • Jürgen Haag
    • 1
  1. 1.Max-Planck-Institut für biologische KybernetikTübingenGermany
  2. 2.Friedrich-Miescher-Laboratorium der Max-Planck-GesellschaftTübingenGermany
  3. 3.Centre for Visual SciencesResearch School of Biological SciencesCanberra CityAustralia

Personalised recommendations