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A Synchronous Insect Muscle with an Operating Frequency Greater than 500 Hz
1 Department of Psychobiology, University of California, Irvine, California 92717, U.S.A.
2 Department of Zoology, University of Melbourne, Parkville, Victoria 3052, Australia
1. The male cicada, Okanagana vanduzeei, produces a calling song with a pulse repetition frequency of 550 Hz. This sound is produced by a pair of tymbals, each of which is buckled by a large tymbal muscle. Males sing in full sun and the operating temperature of the tymbal muscles is 40-45°C.
2. Analysis of the songs of animals with the tymbal mechanism destroyed on one side, and of the sounds produced by directly manipulating a tymbal, indicates that the two tymbals normally buckle synchronously and that only one sound pulse is produced per tymbal muscle contraction. This implies that the contraction frequency of each tymbal muscle is 550 Hz.
3. Recordings of calling songs from animals with implanted electrodes show that there is usually synchrony between left and right tymbal muscle contractions and that each tymbal muscle can operate at a frequency of about 550 Hz. The recordings also show that there is a 1:1 correlation between muscle electrical and mechanical activity, i.e. these muscles are synchronous and not asynchronous muscles.
4. The ultrastructure of the tymbal muscle is clearly that of a very fast, synchronous muscle: the myofibrils are small, the sarcoplasmic reticulum is extraordinarily well developed, and the T-tubules lie at the 1/4 and 3/4 positions along the sarcomere.
5. When set up for isometric recording, with their nerve supply severed, the tymbal muscles often show spontaneous electrical and mechanical oscillations. The frequency of these oscillations is strongly temperature dependent, and at higher temperatures approaches the normal operating frequency of the muscle. The tendency to oscillate is so strong that single twitches could only very rarely be evoked by electrical stimulation. A twitch duration of under 6 ms was observed at 30°C.
6. We conclude that the tymbal muscle of O. vanduzeei is indeed a synchronous muscle, albeit a highly modified one, capable of operating at 550 Hz. We suggest that the advantages of asynchronous muscles lie chiefly in their greater economy of structure and operation, rather than in an ability to operate at higher frequencies than synchronous muscles.
Note:
This paper is dedicated to the late Professor J. W. S. Pringle who was a pioneer in studies of cicada muscles and a major contributor to our understanding of insect muscle in general. We think he would have enjoyed the new perspective given by the tymbal muscles of Okanagana vanduzeei.
Key words: Insect muscle, tymbal muscle, cicada, sound production, contraction kinetics, muscle ultrastructure
Accepted on April 4, 1985
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