Summary
This paper describes the motor output patterns generated by the flight motor system of the indirect power flight muscles inDrosophila melanogaster, and compares them with motor output patterns in other Diptera. The results are consistent with a model described for other Diptera. The model is also extended forDrosophila to include the following observations:
-
1.
The dorsal longitudinal (wing depressor) muscle which has been described in other Diptera as one muscle having six pairs of motor units, consists inDrosophila of two muscles distinguishable by the temporal pattern of their motor units. The first consists of the five more ventral pairs of motor units, and the second of the single dorsal pair of units.
-
2.
Lateral inhibition between flight motor neurons is mediated directly by axon collaterals of the motor neurons without mediating interneurons.
-
3.
There exists asymmetries in the neural flight oscillator.
-
4.
Motor units in the different muscles show different characteristic frequencies.
-
5.
The three motor units of the most rostral, dorsal ventral (wing elevator) muscle are inhibitorily coupled, and they generate asymmetric motor output patterns. Lateral inhibition between the two motor units of the middle, dorsal ventral muscle, and also between the motor units of the caudal, dorsal ventral muscle was also found. Cases were also observed where a motor unit of the middle, dorsal ventral muscle pair of motor units exhibited reciprocal inhibition with a motor unit of the caudal, dorsal ventral muscle pair.
Analysis of multiple flights indicated that the ability of a specific pair of motor units to change frequency together was more characteristic of two flights of the same animal than in different animals.
Study of flight transients (start bursts and other bursts of motor output near the end of flights), and behavioral studies suggest that there is an internal (non-sensory) driving component of the input to the motor neurons.
Characteristics of the motor neuron discharge inDrosophila show close agreement to the relationships predicted from the size principle, suggesting that the average motor neuron size varies from muscle to muscle but is similar for the motor neurons innervating a given muscle.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Barber, S. B., Pringle, J. W. S.: Functional aspects of flight in belostomatid bugs (Heteroptera). Proc. roy. Soc. B164, 21–39 (1966).
Bennet-Clark, H. C., Ewing, A. W.: The wing mechanism involved in the courtship ofDrosophila. J. exp. Biol.49, 117–128 (1968).
Bullock, T. H., Horridge, G. A.: Structure and function in the nervous systems of invertebrates. New York: Freeman Publ. Co. 1965.
Burton, A. J.: Nervous control of flight orientation in a beetle. Nature (Lond.)204, 1333 (1964).
Darwin, F. W., Pringle, J. W. S.: The physiology of insect fibrillar flight muscle. I. Anatomy and innervation of the basalar muscle of lamellicorn beetles. Proc. roy. Soc. B151, 194–203 (1959).
Davis, W. J.: Functional significance of motor neuron size and soma position in the swimmeret system of the lobster. J. Neurophysiol.35, 274–288 (1971).
Ferris, G. F.: External morphology of the adult. In: M. Demerec ed., The biology ofDrosophila, p. 268–419. New York: Hafner Publ. Co. 1950.
Fraenkel, G.: Untersuchungen über die Koordination von Reflexen und automatisch-nervösen Rhythmen bei Insekten. I. Die Flugreflexe der Insekten und ihre Koordination. Z. vergl. Physiol.16, 371–393 (1932).
Gesteland, R. C., Howland, B., Lettvin, J. Y., Pitts, W. H.: Comments on microelectrodes. Proc. I.R.E.47, 11 (1959).
Harmon, L. D., Lewis, E. R.: Neural modeling. Physiol. Rev.46 (3), 513–591 (1966).
Henneman, E.: Relation between size of neurons and their susceptibility to discharge. Science126, 1345–1347 (1957).
Henneman, E., Somjen, G., Carpenter, D. O.: Functional significance of cell size in spinal motor neurons. J. Neurophysiol.28, 560–580 (1965).
Ikeda, K., Boettiger, E. G.: Studies on the flight mechanisms of insects. II. The innervation of the fibrillar muscles of the bumble bee,Bombus americanorum. J. Insect. Physiol.11, 779–789 (1965).
Ikeda, K., Kaplan, W. D.: Patterned neural activity in a mutantDrosophila melanogaster. Proc. nat. Acad. Sci. (Wash.)66, 765–772 (1969).
Kammer, A.: Motor patterns during flight and warm-up inLepidoptera. J. exp. Biol.48, 89–109 (1968).
Kandel, E. R., Frazier, W. T., Coggeshall, R. E.: Opposite synaptic actions mediated by different branches of an identifiable interneuron inAplysia. Science155, 346–349 (1967).
Keilich, J.: Beiträge zur Kenntnis der Insektenmuskeln. Zool. Jb. Abt. Anat. u. Ontog.40, 515–536 (1918).
Levine, J., Hughes, M.: Cuticular anchorage of the indirect flight muscles and tergal depressor of the trochanter inDrosophila melanogaster. J. Morph. in press.
Machin, K. E., Pringle, J. W. S.: The physiology of insect fibrillar flight muscle. II. Mechanical properties of a beetle flight muscle. Proc. roy. Soc. B151, 204–225 1959).
Maynard, D. M., Atwood, H. A.: Divergent post-synaptic effects produced by single motor neurons of the lobster stomatogastric ganglion. Amer. Zool.9, 1107 (1969).
McCann, F., Boettiger, E. G.: Studies of the flight mechanisms of inscets. I. The electrophysiology of fibrillar flight muscle. J. gen. Physiol.45, 125–142 (1961).
Mulloney, B.: Interneurons in the central nervous system of flies and the start of flight. Z. vergl. Physiol.64, 243–253 (1969).
Mulloney, B.: Impulse patterns in the flight motor neurons ofBombus californicus andOncopeltus fasciatus. J. exp. Biol.52, 59–77 (1970a).
Mulloney, B.: Organization of flight motor neurons of Diptera. J. Neurophysiol.33, 86–95 (1970b).
Neville, A. C.: Motor unit distribution of the dorsal longitudinal muscles in locusts. J. exp. Biol.40, 123–136 (1963).
Pringle, J. W. S.: The excitation and contraction of the flight muscles of insects. J. Insect Physiol.108, 226–232 (1949).
Pringle, J. W. S.: Comparative physiology of the flight motor. Advanc. Insect Physiol.5, 163–227 (1968).
Renshaw, B.: Central effects of centripetal impulses in axons of spinal ventral roots. J. Neurophysiol.9, 191 (1946).
Roeder, K. D.: Movement of the thorax and potential changes in the thoracic muscles in insects during flight. Biol. Bull. Woods Hole,100, 95–106 (1951).
Tiegs, O. W.: The flight muscles of insects—their anatomy and histology; with some observations on the structure of striated muscle in general. Phil. Trans. B238, 221–359 (1955).
Waldron, I.: Mechanisms for the production of motor output pattern in flying locust. J. exp. Biol.47, 201–212 (1967).
Waldron, I., Wilson, D. M.: Latency relationships between loosely co-ordinated locust flight motor neurons. J. exp. Zool.170, 293–300 (1969).
Wilson, D. M.: The central nervous control of flight in locust. J. exp. Biol.38, 471–490 (1961).
Wilson, D. M.: Relative refractoriness and patterned discharge of locust flight motor neurons. J. exp. Biol.41, 191–205 (1964).
Wilson, D. M.: Central nervous mechanisms for the generation of rhythmic behavior in arthropods. XXth Symp. Soc. exp. Biol.20, 199–228 (1966).
Wilson, D. M.: The nervous control of insect flight and related behavior. Advanc. Insect Physiol.5, 289–338 (1968).
Wilson, D. M., Waldron, I.: Models for the generation of the motor output pattern in flying locust. Proc. I.E.E.E.56, 1058–1064 (1968).
Wilson, D. M., Wyman, R. J.: Phasically unpatterned nervous control of dipteran flight. J. Insect Physiol.9, 859–865 (1963).
Wyman, R. J.: Probabilistic characterization of simultaneous nerve impulse sequences controlling dipteran flight. Biophys. J.5 (4), 447–471 (1965).
Wyman, R. J.: Multistable firing patterns among several neurons. J. Neurophysiol.29, 807–833 (1966).
Wyman, R. J.: Lateral inhibition in a motor output system. I. Reciprocal inhibition in a dipteran flight motor system. J. Neurophysiol.32, 297–306 (1969a).
Wyman, R. J.: Lateral inhibition in a motor output system. II. Diverse forms of patterning. J. Neurophysiol.32, 307–314 (1969b).
Wyman, R. J.: Patterning of frequency variation in dipteran flight motor units. J. Comp. Biochem. Physiol.35, 1–16 (1970).
Zalokar, M.: Anatomie du thorax duDrosophila melanogaster. Rev. Suisse Biol.54 (2), 18–53 (1947).
Author information
Authors and Affiliations
Additional information
I would like to acknowledge the importance to the present work of interacting with the following people. Alphabetically they are: Roger Abbott, David Bently, George Gerstein, Leon Harmon, Earl Mayeri, Brian Mulloney, Donald Poulson, John Pringle, Robert Socolow, Noni Smith (Harcombe), Alan Steinbach, Curt Stern, Ingrid Waldron, David White, Donald Wilson, Robert Wyman, and Malcolm Zaretsky.
Parts of this work were carried out while the author was: guest research investigator in the A.R.C. unit of Insect Physiology at Oxford University, graduate student at Yale University, and guest investigator at Stanford University.
This research was supported by N.I.H., N.S.F. and, N.A.S.A. predoctoral fellowships to Jon Levine, grants N.I.H.-N.B. 07314 and N.A.S.A. NGR-07-004-090 to Dr. Robert Wyman, and Professor J. W. S. Pringle and Donald M. Wilson for facilities for some of the experimental work.
Rights and permissions
About this article
Cite this article
Levine, J. Properties of the nervous system controlling flight inDrosophila melanogaster . J. Comp. Physiol. 84, 129–166 (1973). https://doi.org/10.1007/BF00697603
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF00697603