Biological Cybernetics

, Volume 46, Issue 1, pp 67–79 | Cite as

Motion sensitive interneurons in the optomotor system of the fly

II. The horizontal cells: Receptive field organization and response characteristics
  • Klaus Hausen


The functional properties of the three horizontal cells (north horizontal cell, HSN; equatorial horizontal cell, HSE; south horizontal cell, HSS) in the lobula plate of the blowflyCalliphora erythrocephala were investigated electrophysiologically. 1. The receptive fields of the HSN, HSE, and HSS cover the dorsal, equatorial and ventral part of the ipsilateral visual field, respectively. In all three cells, the sensitivity to visual stimulation is highest in the frontal visual field and decreases laterally. The receptive fields and spatial sensitivity distributions of the horizontal cells are directly determined by the position and extension of their dendritic fields in the lobula plate and the dendritic density distributions within these fields. 2. The horizontal cells respond mainly to progressive (front to back) motion and are inhibited by motion in the reverse direction, the preferred and null direction being antiparallel. The amplitudes of motion induced excitatory and inhibitory responses decline like a cosine function with increasing deviation of the direction of motion from the preferred direction. Stimulation with motion in directions perpendicular to the preferred direction is ineffective. 3. The preferred directions of the horizontal cells show characteristic gradual orientation changes in different parts of the receptive fields: they are horizontally oriented only in the equatorial region and increasingly tilted vertically towards the dorsofrontal and ventrofrontal margins of the visual field. These orientation changes can be correlated with equivalent changes in the local orientation of the lattice of ommatidial axes in the pertinent compound eye. 4. The response amplitudes of the horizontal cells under stimulation with a moving periodic grating depend strongly on the contrast frequency of the stimulus. Maximal responses were found at contrast frequencies of 2–5 Hz. 5. The spatial integration properties of the horizontal cells (studied in the HSE) are highly nonlinear. Under stimulation with extended moving patterns, their response amplitudes are nearly independent of the size of the stimuli. It is demonstrated that this response behaviour does not result from postsynaptic saturation in the dendrites of the cells. The results indicate that the horizontal system is essentially involved in the neural control of optomotor torque responses performed by the fly in order to minimize unvoluntary deviations from a straight flight course.


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  1. Beersma, D.G.M., Stavenga, D.G., Kuiper J.W.: Retinal lattice, visual field and binocularities in flies. J. Comp. Physiol.119, 207–220 (1977)Google Scholar
  2. Bishop, L.G., Keehn, D.G., McCann, G.D.: Motion detection by interneurons of the optic lobes and brain of the flies,Calliphora phaenicia andMusca domestica. J. Neurophysiol.31, 509–525 (1968)Google Scholar
  3. Blondeau, J.: Electrically evoked motor activity in the fly, (Calliphora erythrocephala). Dissertation, Universität Tübingen 1977Google Scholar
  4. Blondeau, J.: Electrically evoked course control in the flyCalliphora erythrocephala. J. Exp. Biol.92, 143–153 (1981a)Google Scholar
  5. Blondeau, J.: Aerodynamic capability of flies as revealed by a new technique. J. Exp. Biol.92, 155–163 (1981b)Google Scholar
  6. Blondeau, J., Heisenberg, M.: The three-dimensional optomotor torque system ofDrosophila melanogaster. J. Comp. Physiol.145, 321–329 (1982)Google Scholar
  7. Braitenberg, V.: Periodic structures and structural gradients in the visual ganglia of the fly. In: Information processing in the visual system of arthropods. Wehner, R. (ed.), pp. 1–15. Berlin, Heidelberg, New York: Springer 1972Google Scholar
  8. Dvorak, D.R., Bishop, L.G., Eckert, H.E.: On the identification of movement detectors in the fly optic lobe. J. Comp. Physiol.100, 5–23 (1975)Google Scholar
  9. Eckert, H.: Identifizierte, bewegungssensitive Interneurone als neurophysiologische Korrelate für das Bewegungssehen der Insekten. Verh. Dtsch. Zool. Ges. 1976, p. 253. Stuttgart: Gustav Fischer 1976Google Scholar
  10. Eckert, H.: Anatomie, Elektrophysiologie und funktionelle Bedeutung bewegungssensitiver Neurone in der Sehbahn von Dipteren (Phaenicia). Habilitationsschrift, Universität Bochum 1979Google Scholar
  11. Eckert, H.: Functional properties of the H1-neurons in the third optic ganglion of the blowfly,Phaenicia. J. Comp. Physiol.135, 29–39 (1980)Google Scholar
  12. Eckert, H.: The horizontal cells in the lobula plate of the blowfly,Phaenicia sericata. J. Comp. Physiol.143, 511–526 (1981)Google Scholar
  13. Franceschini, N.: Sampling of the visual environment by the compound eye of the fly: fundamentals and applications. In: Photoreceptor optics, Snyder, A.W., Menzel, R. (eds.), pp. 98–125. Berlin, Heidelberg, New York: Springer 1975Google Scholar
  14. Geiger, G., Nässel, D.R.: Visual orientation behaviour of flies after laser beam ablation of interneurons. Nature293, 398–399 (1981)Google Scholar
  15. Geiger, G. Nässel, D.R.: Visual processing of moving single-objects and wide-field patterns in flies. Biol. Cybern.44, 141–150 (1982)Google Scholar
  16. Götz, K.G., Hengstenberg, B., Biesinger, R.: Optomotor control of wing beat and body posture inDrosophila. Biol. Cybern.35, 101–112 (1978)Google Scholar
  17. Hausen, K.: Struktur, Funktion und Konnektivität bewegungsempfindlicher Interneuronen im dritten optischen Neuropil der SchmeißfliegeCalliphora erythrocephala. Dissertation, Universität Tübingen 1976aGoogle Scholar
  18. Hausen, K.: Functional characterization and anatomical identification of motion sensitive neurons in the lobula plate of the blowflyCalliphora erythrocephala. Z. Naturforsch.31c, 629–633 (1976b)Google Scholar
  19. Hausen, K.: Funktion, Struktur und Konnektivität bewegungsempfindlicher Interneurone in der Lobula plate von Dipteren. Verh. Dtsch. Zool. Ges. 1976, p. 254. Stuttgart: Gustav Fischer 1976cGoogle Scholar
  20. Hausen, K.: Signal processing in the inset eye. In: Function and formation of neural systems. Stent, G.S. (ed.), pp. 81–110. Berlin: Dahlem Konferenzen 1977Google Scholar
  21. Hausen, K.: Monocular and binocular computation of motion in the lobula plate of the fly. Verh. Dtsch. Zool. Ges. 1981, pp. 49–70. Stuttgart: Gustav Fischer 1981Google Scholar
  22. Hausen, K.: Motion sensitive interneurons in the optomotor system of the fly. I. The horizontal cells: structure and signals. Biol. Cybern.45, 143–156 (1982)Google Scholar
  23. Hausen, K., Wehrhahn, C.: The role of the horizontal cells in the optomotor yaw torque response in flies (in preparation) (1982)Google Scholar
  24. Heide, G.: Properties of a motor output system involved in the optomotor responses of flies. Biol. Cybern.20, 99–112 (1975)Google Scholar
  25. Heisenberg, M., Wonneberger, R., Wolf, R.: Optomotor-blind — aDrosophila mutant of the lobula plate giant neurons. J. Comp. Physiol.124, 287–296 (1978)Google Scholar
  26. Hengstenberg, R.: Spike responses of non-spiking visual interneurone. Nature270, 338–340 (1977)Google Scholar
  27. Hengstenberg, R.: Common visual response properties of giant vertical cells in the lobula plate of the blowflyCalliphora. J. Comp. Physiol. (in press) (1982)Google Scholar
  28. Mastebroek, H.A.K., Zaagman, W.H., Lenting, B.P.M.: Movement detection: performance of a wide-field element in the visual system of the blowfly. Vision Res.20 467–474 (1980)Google Scholar
  29. McCann, G.D., Dill, J.C.: Fundamental properties of intensity, form, and motion perception in the visual nervous system ofCalliphora phaenicia andMusca domestica. J. Gen. Physiol.53, 355–371 (1969)Google Scholar
  30. McCann, G.D., Foster, S.F.: Binocular interactions of motion detection fibers in the optic lobes of flies. Kybernetik8, 193–203 (1971)Google Scholar
  31. Pick, B.: Visual pattern discrimination as an element of the fly's orientation behaviour. Biol. Cybern.23, 171–180 (1976)Google Scholar
  32. Poggio, T., Reichardt, W., Hausen, K.: A neuronal circuitry for relative movement discrimination by the visual system of the fly. Naturwissenschaften68, 443–446 (1981)Google Scholar
  33. Reichardt, W., Poggio, T., Hausen, K.: Figure-ground discrimination by relative movement in the visual system of the fly. Part II: Towards the neural circuitry (in preparation) (1982)Google Scholar
  34. Soohoo, S.L., Bishop, L.G.: Intensity and motion response of giant vertical neurons in the fly eye. J. Neurobiol.11, 159–177 (1980)Google Scholar
  35. Spüler, M.: Erregende und hemmende Wirkungen visueller Bewegungsreize auf das Flugsteuersystem von Fliegen —Elektrophysiologische und verhaltensphysiologische Untersuchungen anMusca andCalliphora. Dissertation, Universität Düsseldorf 1980Google Scholar
  36. Wehrhahn, C., Hausen, K.: How is tracking and fixation accomplished in the nervous of the fly? Biol. Cybern.38, 179–186 (1980)Google Scholar
  37. Zaagman, W.H., Mastebroek, H.A.K., Kuiper, J.W.: On the correlation model: processing of continuously moving patterns by a movement detecting neural element in the fly visual system. Biol. Cybern.31, 163–168 (1978)Google Scholar

Copyright information

© Springer-Verlag 1982

Authors and Affiliations

  • Klaus Hausen
    • 1
  1. 1.Max-Planck-Institut für biologische KybernetikTübingenFederal Republic of Germany

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