Proprioceptive feedback dominates the central oscillator in the patterning of the flight motoneuron output inTipula (Diptera)

Summary

• 1. Action potentials were recorded from units of the indirect power flight muscles dvm1 and dlm of tethered flying crane flies (Tipula paludosa). The normal wingbeat frequencies of the animals were in the range of about 50 to 60 Hz. By mutilating or loading the wings the wingbeat frequencies could be adjusted to any values between 25 Hz and 160 Hz.

• 2. There is a strong tendency for the action potentials to be phase-locked with respect to the wingbeat period at all wingbeat frequencies up to about 120 Hz (Figs. 4, 5). This holds true in spite of the fact that the action potentials do not occur in every wingbeat period (Fig. 6). Thus, wingbeat synchronous afferences influence phasically (trigger) the production of spikes in the output systems. -The dvm1-units and the dlm-units fire at different phase bands within the wingbeat period.

• 3. If both wing nerve afferences are disrupted then in most cases only very short flights can be initiated. It can be concluded that these afferences are involved in the maintenance of flight. Prolonged flights can be elicited only exceptionally. In all cases, however, the tendency of the spikes to accumulate at small phase bands within the wingbeat cycle is drastically reduced (Fig. 8). Thus, wingbeat synchronous afferences travelling along the wing nerves contain important timing cues for the production of the neuromotor output.

• 4. In the absence of wing nerve afferences the motor output systems supplying the flight muscle units of the dvml and the dlm, respectively, fire with their own inherent rhythm; the occurrences of spikes in the dlm are strongly correlated with the occurrences of spikes in the dvm1 and vice versa (Figs. 11B, 12). This demonstrates the existence of a central nervous mechanism which is able to produce a rhythmic motor output autonomously. -Under physiological conditions, however, the endogenous rhythm is overridden by timing cues from wingbeat synchronous afferences.

• 5. The neural output driving the indirect flight muscles inTipula is compared with the neural output supplying the flight muscles in “higher” Diptera on the one hand and in locusts on the other. It is suggested that the tipulid flight motor system represents an early stage in the evolution of the highly specialized systems of the “higher” Diptera. -Some features of the flight motor in Diptera are summarized in a block diagram (Fig. 13).