Skip to main content
Log in

Reafferent control of optomotor yaw torque inDrosophila melanogaster

  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Summary

In the flight simulator the optomotor response ofDrosophila melanogaster does not operate as a simple feedback loop. Reafferent and exafferent motion stimuli are processed differently. Under open-loop conditions responses to motion are weaker than under closed-loop conditions. It takes the fly less than 100 ms to distinguish reafferent from exafferent motion. In closed-loop conditions, flies constantly generate torque fluctuations leading to small-angle oscillations of the panorama. This reafferent motion stimulus facilitates the response to exafferent motion but does not itself elicit optomotor responses. Reafference control appears to be directionally selective: while a displacement of the patternm by as little as 0.1° against the ‘expected’ direction leads to a fast syndirectional torque response, displacements in the ‘expected’ direction have no comparable effect. Based on the behavior of the mutantrol sol, which under open-loop conditions is directionally motion-blind but in closed-loop conditions still performs optomotor balance, a model is proposed in which the fly's endogenous torque fluctuations are an essential part of the course control process. It is argued that the model may also account for wild type optomotor balance in the flight simulator.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Batschelet E (1981) Circular statistics in biology. In: Sibson R, Cohen JE (eds) Mathematics in biology. Academic, London

    Google Scholar 

  • Bausenwein B, Wolf R, Heisenberg M (1986) Genetic dissection of optomotor behavior inDrosophila melanogaster. Studies on wildtype and the mutantoptomotor-blind H31. J Neurogen 3:87–109

    Google Scholar 

  • Brun R (1914) Die Raumorientierung der Ameisen und das Orientierungsproblem im allgemeinen. Gustav Fischer, Jena

    Google Scholar 

  • Buchner E (1976) Elementary movement detectors in an insect visual system. Biol Cybern 24:85–101

    Google Scholar 

  • Götz KG (1964) Optomotorische Untersuchung des visuellen Systems einiger Augenmutanten der FruchtfliegeDrosophila. Kybernetik 2:77–92

    Google Scholar 

  • Götz KG (1980) Visual guidance inDrosophila. In: Siddiqi O, Babu P, Hall LM, Hall JC (eds) Development and neurobiology ofDrosophila. Plenum, New York, pp 391–407

    Google Scholar 

  • Götz KG (1983) Genetik und Ontogenie des Verhaltens. Genetischer Abbau der visuellen Orientierung beiDrosophila. Verh Dtsch Zool Ges 1983:83–99

    Google Scholar 

  • Götz KG, Buchner E (1978) Evidence for one-way movement detection in the visual system ofDrosophila. Biol Cybern 31:243–248

    Google Scholar 

  • Hausen K (1981) Monocular and binocular computation of motion in the lobula plate of the fly. Verh Dtsch Zool Ges 1981:49–70

    Google Scholar 

  • Heisenberg M (1983) Initiale Aktivität und Willkürverhalten bei Tieren. Naturwissenschaften 70:70–78

    Google Scholar 

  • Heisenberg M, Wolf R (1979) On the fine structure of yaw torque in visual flight orientation ofDrosophila melanogaster. J Comp Physiol 130:113–130

    Google Scholar 

  • Heisenberg M, Wolf R (1984) Vision inDrosophila. Genetics of micro-behavior. In: Braitenberg V (ed) Studies of brain function, vol. XII. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Holst E von, Mittelstaedt H (1950) Das Reafferenzprinzip. Wechselwirkungen zwischen Zentralnervensystem und Peripherie. Naturwissenschaften 37:464–476

    Google Scholar 

  • Kühn A (1919) Die Orientierung der Tiere im Raum. Fischer, Jena

    Google Scholar 

  • Mayer M, Vogtmann K, Bausenwein B, Wolf R, Heisenberg M (1988)Drosophila flight control during ‘free yaw turns’. J Comp Physiol A 163:389–399

    Google Scholar 

  • Mittelstaedt H (1951) Zur Analyse physiologischer Regelungs-systeme. Verh Dtsch Zool Ges, Zool Anz [Suppl]:150

  • Poggio T, Reichardt W (1973) A theory of the pattern induced flight orientation of the flyMusca domestica. Kybernetik 12:185–203

    Google Scholar 

  • Rádl EM (1903) Untersuchungen über den Phototropismus der Tiere. Engelmann, Leipzig

    Google Scholar 

  • Reichardt W (1970) The insect eye as a model for analysis of uptake, transduction and processing of optical data in the nervous system. In: Schmitt FO (ed) The neurosciences. Second study program. Rockefeller University Press, New York, pp 494–511

    Google Scholar 

  • Reichardt W (1973) Musterinduzierte Flugorientierung der FliegeMusca domestica. Naturwissenschaften 60:122–138

    Google Scholar 

  • Reichardt W, Poggio T (1976) Visual control of orientation behaviour in the fly. Part I. A quantitative analysis. Q Rev Biophys 9:311–375

    Google Scholar 

  • Reichardt W, Wenking H (1969) Optical detection and fixation of objects by fixed flying flies. Naturwissenschaften 56:424–425

    Google Scholar 

  • Sperry RW (1950) Neural basis of the spontaneous optokinetic response produced by visual inversion. J Comp Physiol Psychol 43:482–499

    Google Scholar 

  • Wolf R, Heisenberg M (1986) Visual orientation in motion-blind flies is an operant behaviour. Nature 323:154–156

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Heisenberg, M., Wolf, R. Reafferent control of optomotor yaw torque inDrosophila melanogaster . J. Comp. Physiol. 163, 373–388 (1988). https://doi.org/10.1007/BF00604013

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00604013

Keywords

Navigation