Journal of Comparative Physiology A

, Volume 164, Issue 1, pp 15–24 | Cite as

Visual steering under closed-loop conditions by flying locusts: flexibility of optomotor response and mechanisms of correctional steering

  • Daniel Robert


  1. 1.

    Tethered locusts,Locusta migratoria, flying in a laminar air flow react to motion of the visual world with compensatory steering.

  2. 2.

    Vertical gratings surrounding the animal and rotating around the yaw axis elicit an optomotor yaw response. At the low light level used, gratings of spatial periods (λ) below 10° or of contrast frequency (CF) above 15 Hz are less effective.

  3. 3.

    In a flight simulator which converts torque into angular velocity of the vertical grating, the locust can control the motion of its visual surroundings. When the negative feedback loop is closed, locusts stabilize a vertical grating by modulation of their yaw torque. This indicates that the correctional steering behaviour described under open loop conditions is functionally relevant.

  4. 4.

    Under the same conditions, the optomotor reactions lead to the stabilization of a single vertical stripe in the frontal visual area (fixation).

  5. 5.

    With positive feedback (i.e. the pattern turns in the same direction as the torque), no corresponding inversion of steering is observed, and stabilization around the yaw axis fails.

  6. 6.

    Under similar negative feedback conditions, locusts stabilize the position of the visual horizon around the roll axis by modulating their roll torque. Positive feedback leads, however, to the stabilization of the horizon in the inverted position (reverse albedo).

  7. 7.

    The results suggest the existence of two steering strategies, one based on the parameters of visual movement and the other on position in the visual field and relative luminance. The use of these strategies is discussed.



Torque Flight Simulator Vertical Grating Roll Torque Optomotor Response 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



contrast frequency


negative feedback


positive feedback


spatial period


angular velocity


descending neurone


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Arbas EA (1986) Control of hindlimb posture by wind-sensitive hairs and antennae during locust flight. J Comp Physiol A 159:849–857Google Scholar
  2. Baker PS (1979) The wing movements of flying locusts during steering behaviour. J Comp Physiol 131:49–58Google Scholar
  3. Baker PS, Cooler RJ (1979) The natural flight of the migratory locust,Locusta migratoria L. J Comp Physiol 131:79–87Google Scholar
  4. Camhi JM (1970) Yaw-correcting postural changes in locusts. J Exp Biol 52:519–531Google Scholar
  5. Cooler RJ (1979) Visually induced yaw movements in the flying locustSchistocera gregaria (Forsk). J Comp Physiol 131:67–78Google Scholar
  6. Dugard JJ (1967) Directional change in flying locusts. J Insect Physiol 13:1055–1063Google Scholar
  7. Forman R, Brumbley D (1980) An improved capacitive position transducer for biological systems. J Exp Biol 88:399–402Google Scholar
  8. Gewecke M, Philippen J (1978) Control of the horizontal flight-course by air-current sense organs inLocusta migratoria. Physiol Entomol 3:43–52Google Scholar
  9. Götz KG (1984) Optomotorische Untersuchungen des visuellen Systems einiger Augenmutanten der FruchtfliegeDrosophila. Kybernetik 2:77–92Google Scholar
  10. Götz KG (1975) The optomotor equilibrium of theDrosophila navigation system. J Comp Physiol 99:187–210Google Scholar
  11. Götz KG (1983) Genetik und Ontogenie des Verhaltens: Genetischer Abbau der visuellen Orientierung beiDrosophila. Verh Dtsch Zool Ges 76:83–99Google Scholar
  12. Götz KG (1987) Course-control, metabolism and wing interference during ultralong tethered flight inDrosophila melanogaster. J Exp Biol 128:35–46Google Scholar
  13. Goodman LJ (1965) The role of certain optomotor reactions in regulating stability in the rolling plane during flight in the desert locust,Schistocerca gregaria. J Exp Biol 42:385–407Google Scholar
  14. Heisenberg M, Wolf R (1979) On the fine structure of yaw torque in visual flight orientation ofDrosophila melanogaster. J Comp Physiol 130:113–130Google Scholar
  15. Heisenberg M, Wolf R (1984) Vision inDrosophila. Genetics of microbehavior. Springer, Berlin Heidelberg New YorkGoogle Scholar
  16. Hengstenberg R, Sandeman DC, Hengstenberg B (1986) Compensatory head roll in the blowflyCalliphora during flight. Proc R Soc Lond B 227:455–482Google Scholar
  17. Hensler K (1987) Flight steering in locusts: parallel encoding of deviations from straight flight and head movements in the same deviation detector neuron and its functional significance. In: Elsner N, Creutzfeld O (eds) New frontiers in brain research: Proc 15. Göttingen Neurobiol Conf. Thieme, Stuttgart, p 51Google Scholar
  18. Kunze P (1961) Untersuchung des Bewegungssehens fixiert fliegender Bienen. Z Vergl Physiol 44:656–684Google Scholar
  19. Möhl B (1988) Short-term learning during flight control inLocusta migratoria. J Comp Physiol A 163:803–812Google Scholar
  20. Pick B, Buchner E (1979) Visual movement detection under light and dark-adaptation in the fly,Musca domestica. J Comp Physiol 134:45–54Google Scholar
  21. Reichardt W, Poggio T (1976) Visual control of orientation behaviour in the fly. Part 1. Q Rev Biophys 9:311–375Google Scholar
  22. Reichardt W, Wenking H (1969) Optical detection and fixation of objects by fixed flying flies. Naturwissenschaften 56:424–425Google Scholar
  23. Reichert H, Rowell CHF (1985) Integration of non-phase-locked exteroceptive information in the control of rhythmic flight in the locust. J Neurophysiol 53:1216–1233Google Scholar
  24. Reichert H, Rowell CHF, Griss C (1985) Course correction circuitry translates feature detection into behavioural action in locusts. Nature 315:142–144Google Scholar
  25. Rowell CHF (1988) Mechanisms of flight steering in locusts. In: Camhi J (ed) Neuroethology: a multiauthor review. Experientia 44:389–395Google Scholar
  26. Rowell CHF, Reichert H (1986) Three descending interneurons reporting deviation from course in the locust. II. Physiology. J Comp Physiol A 158:775–794Google Scholar
  27. Rowell CHF, O'Shea M, Williams JLD (1977) The neuronal basis of a sensory analyser, the acridid movement detector system. IV. The preference for small field stimuli. J Exp Biol 68:157–185Google Scholar
  28. Schmidt J, Zarnack W (1987) The motor pattern of locusts during visually induced rolling in long-term flight. Biol Cybern 56:397–410Google Scholar
  29. Taylor CP (1981) Contribution of compound eyes and ocelli to steering of locusts in flight. I. Behavioural analysis. J Exp Biol 93:1–18Google Scholar
  30. Thorson J (1966) Small-signal analysis of a visual reflex in the locust. I: Input parameters. Kybernetik 3:41–53Google Scholar
  31. Thüring DA (1986) Variability of the motor output during flight steering in locusts. J Comp Physiol A 156:655–664Google Scholar
  32. Wagner H (1986) Flight performance and visual control of flight of the free-flying housefly (Musca domestica). I: Organization of the flight motor. Phil Trans R Soc Lond B 312:527–551Google Scholar
  33. Wilson DM (1968) Inherent asymmetry and reflex modulation of the locust flight motor pattern. J Exp Biol 48:631–641Google Scholar
  34. Wilson M (1978) The functional organization of the locust ocelli. J Comp Physiol 124:297–316Google Scholar
  35. Wolf R, Heisenberg M (1986) Visual orientation in motion-blind flies is an operant behaviour. Nature 323:154–156Google Scholar
  36. Zaretsky M (1982) Quantitative measurements of centrally and retinally generated saccadic suppression in a locust movement detector neurone. J Exp Biol 328:521–533Google Scholar
  37. Zarnack W, Möhl B (1977) Activity of the direct downstroke flight muscles ofLocusta migratoria (L.) during steering behaviour in flight. I. Patterns of time shift. J Comp Physiol 118:215–233Google Scholar

Copyright information

© Springer-Verlag 1988

Authors and Affiliations

  • Daniel Robert
    • 1
  1. 1.Zoologisches InstitutUniversität BaselBaselSwitzerland

Personalised recommendations