Abstract
The present study shows that the wing beat frequency of Drosophila is visually controlled and modulated in response to different optomotor stimuli.
Whereas rotational large field stimuli do not appear to modulate wing beat frequency, single rotating vertical stripes increase or decrease wing beat frequency when moving back-to-front or front-to-back, respectively. Maximal modulations occur at lateral stripe positions.
Expansion stimuli eliciting the landing response cause a marked increase in wing beat frequency. Parameters of this frequency response depend in a graded fashion on certain stimulus properties, and the frequency response co-habituates with the landing response. Several results indicate that the frequency response is an integral component of the landing response, although it can also occur when the characteristic front leg extension is not observed. The complex spatial input integration underlying the frequency response and other motor components of the landing response cannot easily be explained by a system of large field integration units, but might indicate the existence of local expansion detectors.
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References
Baader A, Schäfer M, Rowell CHF (1992) The perception of the visual flow field by flying locusts: a behavioural and neuronal analysis. J Exp Biol 165:137–160
Bausenwein B, Wolf R, Heisenberg M (1986) Genetic dissection of optomotor behavior in Drosophila melanogaster. Studies in wild-type and the mutant optomotor-blind H31. J Neurogenetics 3:87–109
Bausenwein B, Friedrich RW, Waldvogel FM, Spatz HC (1993) Visual control of wing-beat frequency in Drosophila. In: Elsner N, Heisenberg M (eds) Gene-brain-behavior. Thieme, Stuttgart New York, p 170
Belton P (1986) Sounds of insect flight. In: Danthanarayana W (ed) Insect flight. Springer, Berlin Heidelberg New York, pp 60–70
Blondeau J, Heisenberg M (1982) The 3-dimensional optomotor torque system of Drosophila melanogaster. Studies on wild-type and the mutant optomotor-blind H31. J Comp Physiol 145:321–329
Boettiger EG (1957) The machinery of insect flight. In: Scheer BT (ed) Recent advances in invertebrate physiology. Univ Oregon Publ, Eugene, pp 117–142
Borst A (1989) Temporal processing of excitatory and inhibitory motion stimuli in the fly's landing system. Naturwissenschaften 76:531–534
Borst A, Bahde S (1988) Spatio-temporal integration of motion. Naturwissenschaften 75:265–267
David CT (1978) The relationship between body angle and flight speed in free-flying Drosophila. Physiol Entomol 3:191–195
David CT (1985) Visual control of the partition of flight force between lift and thrust in free-flying Drosophila. Nature 313:48–50
Egelhaaf M (1985a) On the neuronal basis of figure-ground discrimination by relative motion in the visual system of the fly. I. Behavioural constraints imposed on the neuronal network and the role of the optomotor system. Biol Cybern 52:123–140
Egelhaaf M (1985b) On the neuronal basis of figure-ground discrimination by relative motion in the visual system of the fly. II. Figure-detection cells, a new class of visual interneurones. Biol Cybern 52:195–209
Egelhaaf M (1989) Visual afferences to flight steering muscles controlling optomotor responses of the fly. J Comp Physiol A 165:719–730
Egelhaaf M, Hausen K, Reichardt W, Wehrhahn C (1988) Visual course control in flies relies on neuronal computation of object and background motion. Trends Neurosci 11:351–358
Fischbach KF (1981) Habituation and sensitization of the landing response of Drosophila melanogaster. Naturwissenschaften 68:332
Fischbach KF, Bausenwein B (1988) Habituation and sensitization of the landing response of Drosophila melanogaster. II: Receptive field size of habituating units. In: Hertting G, Spatz HC (eds) Modulation of synaptic transmission and plasticity in nervous systems. Springer, Berlin Heidelberg New York, pp 369–389
Goodman J (1960) The landing responses of insects. The landing response of the fly Lucilia sericata and other Calliphorinae. J Exp Biol 37:854–878
Götz KG (1964) Optomotorische Untersuchungen des visuellen Systems einiger Augenmutanten der Fruchtfliege Drosophila. Kybernetik 2:77–92
Götz KG (1968) Flight control in Drosophila by visual perception of motion. Kybernetik 4:199–208
Götz KG (1983) Bewegungssehen und Flugsteuerung bei der Fliege Drosophila. In: Nachtigall W (ed) Biona-report 2. Akademie der Wissenschaften und der Literatur Mainz. G. Fischer, Stuttgart New York, pp 21–34
Götz KG (1987) Course-control, metabolism and wing interference during ultralong tethered flight in Drosophila melanogaster. J Exp Biol 128:35–46
Götz KG, Wandel U (1984) Optomotor control of the force of flight in Drosophila and Musca. II. Covariance of lift and thrust in still air. Biol Cybern 51:135–139
Götz KG, Hengstenberg B, Biesinger R (1979) Optomotor control of wing beat and body posture. Biol Cybern 35:101–112
Heide G (1971a) Die Funktion der nicht-fibrillären Flugmuskeln von Calliphora. I. Lage, Insertionsstellen und Innervierungsmuster der Muskeln. Zool Jahrb Physiol 76:87–98
Heide G (1971b) Die Funktion der nicht-fibrillären Flugmuskeln von Calliphora. II. Muskuläre Mechanismen der Flugsteuerung und ihre nervöse Kontrolle. Zool Jahrb Physiol 76:99–137
Heide G (1983) Neural mechanisms of flight control in Diptera. In: Nachtigall W (ed) Biona-report 2. Akademie der Wissenschaften und der Literatur Mainz. G. Fischer, Stuttgart New York, pp 21–34
Heide G, Spüler M, Götz KG, Kamper K (1985) Neural control of asynchronous flight muscles in flies during induced flight manoeuvres. In: Gewecke M, Wendler G (eds) Insect locomotion. Parey, Hamburg, pp 215–222
Heisenberg M, Wolf R (1979) On the fine structure of yaw torque in visual flight orientation of Drosophila melanogaster. J Comp Physiol 130:113–130
Heisenberg M, Wolf R (1984) Vision in Drosophila. Genetics of Microbehavior. Springer, Berlin Heidelberg New York
Nachtigall W (1966) Die Kinematik der Schlagflügelbewegungen von Dipteren. Methodische und analytische Grundlagen zur Biophysik des Insektenflugs. Z Vergl Physiol 52:155–211
Nachtigall W (1968) Gläserne Schwingen. Aus einer Werkstatt biophysikalischer Forschung. Moos, München
Nachtigall W, Roth W (1983) Correlations between stationary measurable parameters of wing movement and aerodynamic force production in the blowfly (Calliphora vicina R.-D.). J Comp Physiol 150:251–260
Pringle JWS (1949) The excitation and contraction of flight muscles of insects. J Physiol (Lond) 108:226–232
Pringle JWS (1978) Stretch activation of muscle: function and mechanism. Proc R Soc Lond B 201:107–130
Reichardt W, Poggio T (1976) Visual control of orientation behaviour in the fly. Part I. A quantitative analysis. Quart Rev Biophys 9:311–375
Reichert H, Rowell CHF, Griss C (1985) Course correction circuitry translates feature detection into behavioural action in locusts. Nature 315:142–144
Robertson RM, Pearson KG (1985) Neural networks controlling locomotion in locusts. In: Selverston AI (ed) Model neural networks and behaviour. Plenum Press, New York, pp 21–35
Robertson RM, Reye DN (1992) Wing movements associated with collision avoidance manouvres during flight in the locust Locusta migratoria. J Exp Biol 163:231–258
Smyth T, Yurkiewicz WJ (1966) Visual reflex control of indirect flight muscles in the sheep blowfly. Comp Biochem Physiol 17:1175–1180
Wagner H (1982) Flow-field variables trigger landing in flies. Nature 297:147–148
Waldvogel FM (1992) Flugsteuerung bei der Fliege Drosophila melanogaster: Anatomie, Muskulatur und Physiologie des Flugapparates. Dissertation, University of Freiburg, Germany
Waldvogel FM, Fischbach KF (1991) Plasticity of the landing response of Drosophila melanogaster. J Comp Physiol A 169:323–330
Warnke R, Spatz HCh (1977) Der Flügelschlag einer Fliege. Biologie in unserer Zeit 6:188–190
Wendler G (1974) The influence of proprioreceptive feedback on locust flight co-ordination. J Comp Physiol 88:173–200
Wittekind WC, Spatz HCh (1988) Habituation of the landing response of Drosophila. In: Hertting G, Spatz HC (eds) Modulation of synaptic transmission and plasticity. Springer, Berlin Heidelberg New York, pp 351–368
Zalokar M (1947) Anatomie du thorax de Drosophila melanogaster. Rev Suisse Zool 54:17–53
Zanker JM (1988) How does lateral abdomen deflection contribute to flight control of Drosophila melanogaster? J Comp Physiol A 162:581–588
Zanker JM (1990) The wing beat of Drosophila melanogaster I. Kinematics. Phil Trans R Soc Lond 327:1–18
Zanker JM, Götz KG (1990) The wing beat of Drosophila melanogaster II. Dynamics. Phil Trans R Soc Lond 327:45–64
Zanker JM, Egelhaaf M, Warzecha AK (1991) On the coordination of motor output during visual flight control of flies. J Comp Physiol A 169:127–134
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Friedrich, R.W., Spatz, H.C. & Bausenwein, B. Visual control of wing beat frequency in Drosophila . J Comp Physiol A 175, 587–596 (1994). https://doi.org/10.1007/BF00199480
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DOI: https://doi.org/10.1007/BF00199480