The organization and functional properties of interneurons in the flight system of the locust, Locusta migratoria, were investigated by using intracellular recording and staining techniques. Interneurons were found to be distributed within the three thoracic and the first three abdominal ganglia, and they could be subdivided into three organizational categories: (1) members of one of two serially homologous groups controlling either the forewing or the hindwing, (2) unique individuals with no known homologues in other ganglia, and (3) members of a set of serial homologous in the metathoracic and first three abdominal ganglia. Interneurons in the last two categories influenced both forewing and hindwing motoneurons in a similar manner. Thus interneuronal organization is not characterized by two distinct homologous groups of interneurons for the separate control of forewing and hindwing motor activity. Flight interneurons may also form two separate functional categories: (1) those making short latency connections to motoneurons (premotor interneurons), and (2) those which reset the flight rhythm when depolarized by brief current pulses (pattern generator interneurons). None of the ten premotor interneurons we identified influenced the flight rhythm when depolarized and none of the three groups of pattern generator interneurons were found to form short latency connections with motoneurons. This separation of function may allow phase-shifts in motor output for flight control without changes in wingbeat frequency. Pattern generator interneurons influence motor output to both forewings and hindwings. Thus we conclude that the flight rhythm is generated in a distributed neuronal oscillator driving both the pairs of wings. The organization of flight interneurons is considerably more complex than predicted from existing models of the flight system, or anticipated from the relative simplicity of the motor output. Our finding of homologous sets of interneurons in the abdominal ganglia supports the notion that insect flight evoked from a behavior using appendages distributed along the thorax and the abdomen. Thus the organization of flight interneurons may reflect an interneuronal system which controlled the behavior from which flight evolved.
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