Summary
To investigate the optomotor leg responses ofDrosophila melanogaster the free walking fly is kept in stationary orientation and position on top of a ball. The stimulus consists of continuous pattern movement in the equatorial zone of the visual field. The rotatory and translatory responses are derived from the signals of a servo-system which maintains the stationary state of the walking fly by appropriate rotations of the ball.
Course control, or the tendency to follow rotatory displacements of the visual surroundings, is established in the wild type and in a behavioural mutant with the eye colour markerw a.The movement detecting systems in the complex eyes on either side respond to the horizontal component of the stimulus and control, predominantly, the thrust of the ipsilateral legs in the wild type, and the thrust of the contralateral legs in the mutant. As a result, front-to-back movement is decreasing the walking speed of the wild type and increasing the walking speed of the mutant, andvice versa.
The course control responses of flying and walking fruitflies depend on the signals of movement detecting systems which are equivalent with respect to the horizontal orientation, the dynamic range, and the resolving power. Leg responses show that the orientation of the movement detecting systems is independent of their position in the eye, and is invariant to the direction and velocity of the stimulus.
The lift control response to the vertical component of the movement stimulus is a quality of the flight system. The response has no counterpart in the optomotor behaviour of the stationarily walking fruitfly.
Functional specialization of the different pairs of legs is not detectable in the present experiments. The rotatory response as well as the translatory propulsion are almost equally accomplished by the fore legs, the middle legs and the hind legs of partially amputated fruitflies.
The optomotor reactions of the fruitfly are accompanied by at least two side-effects of the visual stimulus: The flicker effect acts on the walking speed. The effect is elicited by the temporal sequence of bright and dark stripes in the receptive fields of the visual elements. It is independent of the direction of the pattern movement, and can be produced by a stationarely flickering light source. An after-effect of the pattern movement appears at the end of the visual stimulation. The effect depends on experimental parameters. An initial magnitude of -1/16 of the preceding course control response and a decay time of about 7 min were observed in the present experiments.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Autrum, H., Metschl, N.: Die Arbeitsweise der Ocellen der Insekten. Z. vergl. Physiol.47, 256–273 (1963).
Buchner, E.: Dark activation of the stationary flight of the fruitflyDrosophila. In: Information processing in the visual system of Arthropods, ed. by R. Wehner, p. 141–146. Berlin-Heidelberg-New York: Springer 1972.
Buchner, E.: (unpublished).
Buchner, E., Götz, K. G.: Dunkelanregung des stationären Flugs der FruchtfliegeDrosophila (in preparation).
Davis, W. J., Ayers, J. L.: Locomotion: Control by positive-feedback optokinetic responses. Science177, 183–185 (1972).
Franceschini, N.: Pupil and pseudopupil in the compound eye ofDrosophila. In: Information processing in the visual system of Arthropods, ed. by R. Wehner, p. 75–82, Berlin-Heidelberg-New York: Springer 1972.
Gavel, L. v.: Die „kritische Streifenbreite” als Maß der Sehschärfe beiDrosophila melanogaster. Z. vergl. Physiol.27, 80–135 (1939).
Götz, K. G.: Optomotorische Untersuchung des visuellen Systems einiger Augenmutanten der FruchtfliegeDrosophila. Kybernetik2, 77–92 (1964).
Götz, K. G.: Die optischen Übertragungseigenschaften der Komplexaugen vonDrosophila. Kybernetik2, 215–221 (1965a).
Götz, K. G.: Behavioural analysis of the visual system of the fruitflyDrosophila. In: Information processing in sight sensory systems, ed. by P. W. Nye, p. 85–100. Pasadena: California Institute of Technology 1965b.
Götz, K. G.: Flight control inDrosophila by visual perception of motion. Kybernetik4, 199–208 (1968).
Götz, K. G.: Movement discrimination in insects. In: Processing of optical data by organisms and by machines; Rendiconti S.I.F., Course XLIII, ed. by W. Reichardt, p. 494–509. London-New York: Academic Press 1969.
Götz, K. G.: Fractionation ofDrosophila populations according to optomotor traits. J. exp. Biol.52, 419–436 (1970).
Götz, K. G.: Spontaneous preferences of visual objects inDrosophila.Drosophila Information Service46, 62 (1971).
Götz, K. G.: Processing of cues from the moving environment in theDrosophila navigation system. In: Information processing in the visual system of Arthropods, ed. by R. Wehner, p. 255–263. Berlin-Heidelberg-New York: Springer 1972.
Götz, K. G., Gambke, C.: Zum Bewegungssehen des MehlkäfersTenebrio molitor. Kybernetik4, 225–228 (1968).
Hassenstein, B.: Wie sehen Insekten Bewegungen? Naturwissenschaften48, 207–214 (1961).
Hecht, S., Wald, G.: The visual acuity and intensity discrimination ofDrosophila. J. genr. Physiol.17, 517–547 (1934).
Heisenberg, M.: Isolation of mutants lacking the optomotor response.Drosophila Information Service46, 68 (1971).
Heisenberg, M.: Comparative behavioural studies of two visual mutants ofDrosophila. J. comp. Physiol.80, 119–136 (1972).
Hughes, M.: Locomotion: terrestrial. In: The physiology of insecta, vol. II, ed. by M. Rockstein, p. 227–254. New York-London: Academic Press 1965.
Hunter, W. S.: Retinal factors in visual after-movement. Psychol. Rev.22, 479–489 (1915).
Kalmus, H.: The optomotor responses of some eye mutants ofDrosophila. J. Genet.45, 206–213 (1943).
Kalmus, H.: Optomotor responses inDrosophila andMusca. Physiol. Comp. (s' Grav.)1, 127–147 (1949).
Kalmus, H.: Animals as mathematicians. Nature (Lond.)202, 1156–1160 (1964).
Kirschfeld, K.: The visual system ofMusca: studies on optics, structure and function. In: Information processing in the visual system of Arthropods, ed. by R. Wehner, p. 61–74. Berlin-Heidelberg-New York: Springer 1972.
Kramer, U.: (unpublished).
Maffei, L.: (unpublished).
Nachtigall, W., Wilson, D.: Neuro-muscular control of dipteran flight. J. exp. Biol.47, 77–97 (1967).
Pak, W.: (unpublished).
Reichardt, W.: Musterinduzierte Flugorientierung, Verhaltens-Versuche an der FliegeMusca domestica. Naturwissenschaften60, 122–138 (1973).
Schneider, P.: Vergleichende Untersuchungen zur Steuerung der Fluggeschwindigkeit beiCalliphora vicinia. Z. wiss. Zool.173, 114–173 (1965).
Smyth, T., Yurkiewicz, W. J.: Visual reflex control of indirect flight muscles in the sheep blowfly. Comp. Biochem. Physiol.17, 1175–1180 (1966).
Varjú, D.: Übertragungseigensohaften im Auswertesystem für das Bewegungssehen (Wirksamkeit und biologische Signifikanz des optomotorischen Regelkreises). In: Nova Acta Leopoldina, hrsg. von K. Mothes, Bd. 208, S. 173–193. Leipzig: Joh. Ambr. Barth 1973.
Wehner, R.: Spontaneous pattern preferences ofDrosophila melanogaster to black areas in various parts of the visual field. J. Insect. Physiol.18, 1531–1543 (1972).
Wehner, R., Wehner, S.: Calculation of visual receptor spacing inDrosophila melanogaster by pattern recognition experiments. J. comp. Physiol.82, 165–177 (1973).
Wehrhahn, C., Reichardt, W.: Visual orientation of the flyMusca domestica towards a horizontal stripe. Naturwissenschaften60, 203–204 (1973).
Zimmermann, G., Götz, K. G.: Der Einfluß stehender und bewegter Musteranteile auf die optomotorische Reaktion der FliegeDrosophila (in preparation).
Author information
Authors and Affiliations
Additional information
We gratefully acknowledge the contributions of our colleagues and coworkers. Mr. H. Braun, Mr. M. Herre, Mr. K. Stahl, Dipl. Phys. U. Tietze, Mr. U. Wandel and Mr. D. Wirth have worked on the assembling and the maintenance of the mechano-electric device. Mrs. B. Hengstenberg and Miss A. Huth helped with the preparation and evaluation of the experiments. Numerous suggestions and comments were contributed by Dipl. Phys. E. Buchner, Dr. M. Heisenberg, Dr. R. Hengstenberg, Dr. K. Kirschfeld, Dr. W. Pak, Dr. T. Poggio, Dr. W. Reichardt and Dr. N. Strausfeld who have read the manuscript, and discussed the results, in different stages of the work. The drawings were elaborated by Mr. E. Freiberg and the typing was done by Mrs. E. Abelt and Mrs. I. Geiss.
Rights and permissions
About this article
Cite this article
Götz, K.G., Wenking, H. Visual control of locomotion in the walking fruitflyDrosophila . J. Comp. Physiol. 85, 235–266 (1973). https://doi.org/10.1007/BF00694232
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF00694232