Coupling of flight initiation to the jump in locusts

Summary

• 1. In adult locusts' wing opening for flight occurs soon after a jump is triggered. Previous studies have shown that the interval between the triggering of a jump and the initial wing movement (or the start of elevator muscle activity) is often too short for either the loss of tarsal contact with the ground or the self-generated air stream on the head to be responsible for the onset of wing opening. Thus it has been postulated that the system generating the motor program for the jump is directly linked to the system generating flight motor activity. To investigate this proposal we have recorded activity in flight motoneurons and interneurons during bilateral kicks of the hindlegs.

• 2. The preparation was arranged to allow intracellular recording from flight motoneurons and interneurons during hindleg kicks. Kicks were readily evoked by mechanical stimulation of the abdomen, and the motor activity associated with the kicks was similar to that for a jump in unrestrained animals.

• 3. Short sequences of flight activity were often associated with hindleg kicks. The time of onset of flight activity relative to the time kicks were triggered was variable, and often flight activity commencedbefore the kicks were triggered. The probability of flight activity being initiated increased throughout the co-contraction phase with the peak probability being close to the time kicks were triggered. Thus it appears that the flight system receives a progressively increasing excitatory input during the co-contraction phase of the kick, and that the onset of flight activity isnot tightly linked to the system triggering the kick.

• 4. Intracellular recordings from flight motoneurons showed that wing elevator motoneurons often received an excitatory input during the co-contraction phase, whereas wing depressor motoneurons either showed no change in membrane potential or were slightly hyperpolarized during co-contraction. These recordings failed to reveal any significant input to flight motoneurons at the time a kick was triggered.

• 5. The lack of any influence of the trigger system on the flight system was also apparent in recordings from identified flight interneurons. None consistently showed a synaptic response timelocked to triggering but many received synaptic input during the co-contraction phase. Those receiving excitatory input were also those excited by wind on the head, while those receiving inhibitory input were hyperpolarized by wind on the head.

• 6. We conclude that the flight system receives an excitatory input during the co-contraction phase of the kick, and that this input produces many of the same changes in membrane potential in interneurons and motoneurons as does a wind stream to the head (a stimulus known to readily evoke flight activity). None of our data indicates that the system triggering the kick is responsible for exciting the flight system. We propose that in an intact animal the initiation of flight activity following a jump is facilitated by an excitatory input to the flight system during the co-contraction phase of the jump. The origin of this input has not been determined.