The flight maintenance mechanism in the cockroachPeriplaneta americana L.

Abstract

1. In order to find the receptors that maintained flight in the cockroachPeriplaneta americana a wind tunnel was used (Fig. 1A). 2. After removal of the antennal flagella prolonged flight was not possible. However, sticking of cut antenna restored flight capability (Table 2a, b). These data showed that for maintenance of cockroach flight antennal flagella were needed as levers acting on pedicel receptors: chordotonal sensilla (including the chordotonal sensilla of Johnston's organ) and sensilla campaniformia. 3. In the laminar airstream passive antennal vibration caused by the wing motor activity was absent and the observed antennal movements in flight were evoked only by antennal muscle activity. Fixation of active antennal movements by immobilization the head-scapus and scapus-pedicel joints leads to cessation of flight. Therefore, pedicel receptors are capable to maintain the cockroach flight only if active antennal movements in the airstream are present. 4. The frequency of active antennal movements with amplitude of more than 1 mm is in the cause of 3–10 Hz (Fig. 3B). Each of these active movements like at instantaneous cessation of\(\bar 1\)1 and\(\overline 1 \overline 1 \)1 antennal joints evoked lash (passive deflection) of its flagellum relatively to the pedicel. To estimate low-amplitude passive deflexions which are defined by high-amplitude active movements due to the inertia, ‘sail-property’ and weight of the flagellum a mathematical model was developed. This model describes the displacements of the cockroach flagellum which are evoked by the active movements in the airstream of different velocity. 5. The application of the constructed mathematical model showed that at active antennal movements in the air current velocity of 1.5–2 m/s (minimum velocity at which the cockroach flight was possible) the angle determined by the flagellum weight (its ‘sagging’) was compensated and the angle of flagellum displacement relative to the pedicel at the active movements upward was increased by 1.5–2 times as compared with the same angles at the same antennal movements in still air (Fig. 4). It seems clear that just the redistribution of the load on the pedicel receptors was that mechanical stimulus which periodically acting with frequency of active antennal movements of 3–10 Hz led to alterate the mosaic of excitation of differently located in pedicel chordotonal and campaniform sensilla (functional asymmetry of the system of pedicel receptors) and ultimate maintenance of prolonged flight. 6. Microelectrode recording of electrical activity of the pedicel sensilla showed that three functional types of receptors (phasic-tonic receptors with slow and incomplete adaptation, phasic-tonic receptors with fast and complete adaptation and phasic receptors) were revealed. These receptors perceived the changes in amplitude (starting from 20–30 μm), the frequency (up to 50 Hz, Fig. 6), the flagellum movement velocity as well as they had directional sensitivity. (The sector of the maximal sensitivity was 90–135° in most receptors.) Thus, redistribution of the load in flight from the ventral to dorsal side of the pedicel evoked electrical activity of a definite group of receptors. The sectors of maximal sensitivity of these receptors were dorsally orientated. 7. The pedicel mechanoreceptors' responses in the cockroach head ganglia went over into the descending interneurons of three functional types including the phasic-tonic type with slow incomplete adaptation, the phasic-tonic type with fast and complete adaptation and phasic interneurons. In the cockroach brain the chiasma of the nervous tracts provides receiving the information about the flagellum deflexion to the left and right sides of the prothoracic ganglia. Interneurons were not able to respond for a long time to flagellum vibration, if its frequency exceeded 10 Hz (Fig. 8). Thus, it was evident that electrical activity maintaining the cockroach flight consisted of the impulse bursts of the pedicel receptors and related interneurons at each deflection of the flagellum with regard to the pedicel at the active antennal movements in the air current.