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Journal Article

Das Augenmuskelsystem der Stubenfliege Musca domestica. I. Analyse der "clock-spikes" und ihrer Quellen


Hengstenberg,  R
Department Human Perception, Cognition and Action, Max Planck Institute for Biological Cybernetics, Max Planck Society;

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Hengstenberg, R. (1971). Das Augenmuskelsystem der Stubenfliege Musca domestica. I. Analyse der "clock-spikes" und ihrer Quellen. Kybernetik, 9(2), 56-77. doi:10.1007/BF00270852.

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It is possible to record spontaneously occurring impulses in the housefly's optic lobe region. These closely resemble “clock-spikes”, as described for Calliphora by Kuiper and Leutscher-Hazelhoff (1965). The repetition rate of these impulses—here called “C-spikes”—is about 45/s at 20° C and increases with temperature. Between 15 and 35° C the temperature coefficient of the repetition rate is close to Q 10=2. At constant temperature the mean rate is constant for many hours, the individual intervals appear to be gaussian-distributed about the mean interval τˉ . The standard deviation of the interval lengths in samples of >10000 impulses is approximately ±2.5 of the mean. The fluctuation corresponds to a slight modulation of the mean spike frequency by a noise signal, comprising slow as well as fast components. The time course of extracellularly recorded spikes in combination with evidence from simultaneous recordings at different sites shows that typical C-spikes are produced by the subsequent activity of at least two distinct sources: “Prespikes” originate in the midbrain and are centrifugally conducted with about 2 m/s at room temperature to a peripheral site of C-spike-activity, where they induce a strictly event-correlated impulse activity of a “postspike” source. Decapitation shows that all elements that are necessary to produce and to maintain the regular C-spike activity are located within the head. Under constant conditions no interaction is observed between C-spike sources on the left and right side of the head. Intracellular recordings show that the membranes of the postspike sources on either side are of the electrically unexcitable type. Each of the postspike sources is formed by a cluster of at least two cells. Electrophysiological localization experiments indicate that the postspike sources are located outside of the optic lobes, but close to the lower frontal margin of the left-and right-hand medulla. The sources of C-spike activity could be identified by histological localization of the recording sites. The anatomical correlate of the electrophysiologically determined C-spike system has been reconstructed by means of silver impregnated serial sections: In the lateral perikaryon layer on either side of the subesophageal ganglion lies a single large motoneurone, which is spontaneously producing the regular impulses, most probably during the entire life time of the fly. These impulses are centrifugally conducted along a thin peripheral nerve, which only contains a single motor axon of 6 μm diameter. The nerve runs to a very small muscle, consisting of 14–20 tubular skeletal muscle fibres of 7–10 μm diameter. These fibres are innervated by numerous grape-like neuromuscular endings. From this unineuronal, multiterminal innervation it is concluded that the muscle acts as a functional unit. Extracellular and intracellular recordings under microscopic observation prove the identity of the muscle fibres with the source of the postspikes. The muscle has not been previously described for Musca. It is shown that one end of the muscle is inserted at the inner margin of the orbital ridge, i.e. at the base of the frontal ommatidia in the vicinity of the equator of the compound eye. The other end is fixed to an apodeme which originates near the foramen occipitale on the ventral occipital ridge and which most probably is homologous with the tentorium of other insects. Hence the muscle is denoted as Musculus orbitotentorialis. Similar muscles with comparable insertions are found in Calliphora and Drosophila. The orbito-tentorial muscle also exists in Eristalis, where the tentorium is well developed. Here the muscle inserts on the anterior tentorial arm and at the inner margin of the orbital ridge. This muscle also produces continuously regular spikes. The structure of the head skeleton of Musca shows that the tentorial insertion of the muscle is relatively rigid. Since antagonistic muscles are obviously missing, it is concluded that the orbito-tentorial muscle acts against the elastic forces of the eye tissue and of the orbital skeleton. It is conceivable that the muscular action causes displacements of the optic axes of the visual elements in the compound eyes. The physiological meaning of these displacements is still obscure and deserves further investigations.