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Activation phase ensures kinematic efficacy in flight-steering muscles of Drosophila melanogaster

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Abstract

During tethered flight in Drosophila melanogaster, spike activity of the second basalar flight-control muscle (M.b2) is correlated with an increase in both the ipsilateral wing beat amplitude and the ipsilateral flight force. The frequency of muscle spikes within a burst is about 100 Hz, or 1 spike for every two wing beat cycles. When M.b2 is active, its spikes tend to occur within a comparatively narrow phase band of the wing beat cycle. To understand the functional role of this phase-lock of firing in the control of flight forces, we stimulated M.b2 in selected phases of the wing beat cycle and recorded the effect on the ipsilateral wing beat amplitude. Varying the phase timing of the stimulus had a significant effect on the wing beat amplitude. A maximum increase of wing beat amplitude was obtained by stimulating M.b2 at the beginning of the upstroke or about 1 ms prior to the narrow phase band in which the muscle spikes typically occur during flight. Assuming a delay of 1 ms between the stimulation of the motor nerve and muscle activation, these results indicate that M.b2 is activated at an instant of the stroke cycle that produces the greatest effect on wing beat amplitude.

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References

  • Batschelet E (1981) Circular statistics in biology. Academic Press, London New York

    Google Scholar 

  • Bergmann-Erb D, Heide G (1990) Kontraktionsmodus direkter Flugsteuermuskeln von Calliphora. In: Eisner N, Roth G (eds) Brain-Perception-Cognition. Thieme, Stuttgart, p 41

    Google Scholar 

  • Dickinson MH, Lehmann F-O, Götz KG (1993) The active control of wing rotation by Drosophila. J Exp Biol 182: 173–189

    Google Scholar 

  • Egelhaaf M (1989) Visual afferences to flight steering muscles controlling optomotor responses of the fly. J Comp Physiol A 165: 719–730

    Google Scholar 

  • Ewing AW (1977) The neuromuscular basis of courtship song in Drosophila: The role of the indirect flight muscles. J Comp Physiol 119: 249–265

    Google Scholar 

  • Ewing AW (1979a) The neuromuscular basis of courtship song in Drosophila: The role of the direct and axillary wing muscles. J Comp Physiol 130: 87–93

    Google Scholar 

  • Ewing AW (1979b) The role of feedback during singing and flight in Drosophila melanogaster. Physiol Entomol 4: 329–337

    Google Scholar 

  • Friedrich RW, Spatz H-C, Bausenwein B (1994) Visual control of wing beat frequency in Drosophila. J Comp Physiol A 175: 587–596

    Google Scholar 

  • Götz KG (1968) Flight control in Drosophila by visual perception of motion. Kybernetik 4: 199–208

    Google Scholar 

  • Götz KG (1983a) Genetic defects of visual orientation in Drosophila. Verb Dtsch Zool Ges 1983: 83–99

    Google Scholar 

  • Götz KG (1983b) Bewegungssehen und Flugsteuerung bei der Fliege Drosophila. In: Nachtigall W (ed) Insect flight II. Biona report 2. Fischer, Stuttgart, pp 21–34

    Google Scholar 

  • Götz KG (1987) Course-control, metabolism and wing interference during ultralong tethered flight in Drosophila melanogaster. J Exp Biol 128: 35–46

    Google Scholar 

  • Götz KG (1989) Search and choice in Drosophila. In: Singh RN, Strausfeld NJ (eds) Neurobiology of sensory systems. Plenum Press, New York, pp 139–153

    Google Scholar 

  • Götz KG, Hengstenberg B, Biesinger R (1979) Optomotor control of wing beat and body posture in Drosophila. Biol Cybern 35: 101–112

    Google Scholar 

  • Heide G (1971a) Die Funktion der nicht-fibrillären Flugmuskeln bei der Schmeißfliege Calliphora. I. Lage, Insertionsstellen und Innervierungsmuster der Muskeln. Zool Jb Physiol 76: 87–98

    Google Scholar 

  • Heide G (1971b) Die Funktion der nicht-fibrillären Flugmuskeln bei der Schmeißfliege Calliphora. II. Muskuläre Mechanismen der Flugsteuerung und ihre nervöse Kontrolle. Zool Jb Physiol 76: 99–137

    Google Scholar 

  • Heide G (1975) Properties of a motor output system involved in the optomotor response of the flies. Biol Cybern 20: 99–112

    Google Scholar 

  • Heide G (1978) Proprioceptorische Beeinflussung der Impulsmusterbildung in neuromotorischen System fliegender Dipteren. Verh Dtsch Zool Ges 1978: 256

    Google Scholar 

  • Heide G (1979) Proprioceptive feedback dominates the central oscillator in the patterning of the flight motoneuron output in Tipula (Diptera). J Comp Physiol 134: 177–189

    Google Scholar 

  • Heide G (1983) Neural mechanism of flight control in Diptera. In: Nachtigall W (ed) Insect flight II. Biona report 2. Fischer, Stuttgart, pp 35–52

    Google Scholar 

  • Heide G, Götz KG (1996) Optomotor control of course and altitude in Drosophila is correlated with distinct activities of at least three pairs of flight steering muscles. J Exp Biol (in press)

  • 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, Berlin, pp 215–222

    Google Scholar 

  • Heisenberg M, Wolf R (1984) Vision in Drosophila. Genetics of microbehavior. In: Braitenberg V, Barlow HB, Bullock TH, Florey E, Grüsser OJ, Peters A (eds) Studies of brain function. Springer, Berlin, pp 1–250

    Google Scholar 

  • Hengstenberg R (1971) Das Augenmuskelsystem der Stubenfliege Musca domestica. Kybernetik 2: 56–77

    Google Scholar 

  • Josephson RK (1984) Contraction dynamics of flight and stridulatory muscles of tettigoniid insects. J Exp Biol 114: 493–512

    Google Scholar 

  • King DG, Tanouye MA (1983) Anatomy of motor axons to direct flight muscles in Drosophila. J Exp Biol 105: 231–239

    Google Scholar 

  • Lehmann F-O (1994) Aerodynamische, kinematische und elektrophysiologische Aspekte der Flugkrafterzeugung und Flugkraftsteuerung bei der Fliege Drosophila melanogaster. Thesis, University of Tübingen, Germany

    Google Scholar 

  • Lehmann F-O, Götz KG (1990) Electrical Stimulation of a flight control muscle in Drosophila. In: Elsner N, Roth G (eds) Brainperception-cognition. Thieme, Stuttgart, p 77

    Google Scholar 

  • Lehmann F-O, Götz KG (1992) Efficiency of a flight control muscle in Drosophila depends on the phase of its spikes in the wingbeat cycle. Europ J Neurosci [Suppl] 5: 3218

    Google Scholar 

  • Nachtigall W, Wilson DM (1967) Neuro-muscular control of dipteran flight. J Exp Biol 47: 77–97

    Google Scholar 

  • Nalbach G (1989) The gear change mechanism of the blowfly (Calliphora erythrocephala) in tethered flight. J Comp Physiol A 165: 321–331

    Google Scholar 

  • Pringle JWS (1949) The excitation and contraction of the flight muscles of insects. J Physiol (Lond) 108: 226–232

    Google Scholar 

  • Pringle JWS (1965) Locomotion: Flight. In: Rockstein M (ed) The physiology of insects, vol. 2. Academic Press, New York, pp 238–329

    Google Scholar 

  • Schrage D, Heide G (1990) Elektrische Eigenschaften von Fasern eines Flugsteuermuskels von Calliphora. In: Elsner N, Roth G (eds) Brain-Perception-Cognition. Thieme, Stuttgart, p 42

    Google Scholar 

  • Smith DS (1965) Flight muscles in insects. Sci Amer 212(6): 76–88

    Google Scholar 

  • Spüler M (1980) Erregende und hemmende Wirkungen visueller Bewegungsreize auf das Flugsteuersystem von Fliegen — Elektrophysiologische and verhaltensphysiologische Untersuchungen an Musca and Calliphora. Thesis, University of Düsseldorf, Germany

    Google Scholar 

  • Tu MS, Dickinson MH (1994) Modulation of the negative work output from a steering muscle of the blowfly Calliphora vicina. J Exp Biol 192: 207–224

    Google Scholar 

  • Tu, MS, Dickinson MH (1996) The control of wing kinematics by two steering muscles of the blowfly (Calliphora vicina) J Comp Physiol A 179: 813–830

    Google Scholar 

  • Waldvogel F-M (1992) Flugsteuerung bei der Fliege Drosophila melanogaster: Anatomie, Muskulatur und Physiologie des Flugapparats. Thesis, University of Freiburg, Germany

    Google Scholar 

  • Waldvogel F-M, Bausenwein B (1990) Activity of flight steering muscles in Drosophila. In: Elsner N, Roth G (eds) Brain-Perception-Cognition. Thieme, Stuttgart, p 82

    Google Scholar 

  • Wisser A, Nachtigall W (1983) Funktionelle Gelenkmorphologie und Flügelantrieb bei der Schmeissfliege. In: Nachtigall W (ed) Insect flight I. Biona Report 1. Fischer, Stuttgart, pp 29–34

    Google Scholar 

  • Wisser A, Nachtigall W (1984) Functional-morphological investigations on the flight muscles and their insertion points in the blowfly Calliphora erythrocephala (Insecta, Diperta). Zoomorphology 104: 188–195

    Google Scholar 

  • Wyman R (1965) Probabilistic characterization of simultaneous nerve impulse sequences controlling dipteran flight. Biophys J 5: 447–471

    Google Scholar 

  • Zarnack W, Möhl B (1977) Activity of the direct downstroke flight muscles of Locusta migratoria (L.) during steering behavior in flight. J Comp Physiol 118: 215–233

    Google Scholar 

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Lehmann, F.O., Götz, K.G. Activation phase ensures kinematic efficacy in flight-steering muscles of Drosophila melanogaster . J Comp Physiol A 179, 311–322 (1996). https://doi.org/10.1007/BF00194985

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