Limit-cycle-based control of the myogenic wingbeat rhythm in the fruit fly Drosophila

TL;DR

This study demonstrates that fruit flies control their wingbeat rhythm through mechanical forcing of a myogenic limit cycle oscillator, involving fast steering muscles, which allows rapid modulation without neural central pattern generator involvement.

Contribution

It provides evidence that Drosophila's wingbeat rhythm is controlled by a mechanically forced limit cycle oscillator, revealing a novel motor control mechanism in insects.

Findings

Flies synchronize wingbeat with stimuli, showing Arnold tongues characteristic of forced oscillators.

Fast steering muscles modulate wingbeat frequency rapidly before locking.

Mechanical forcing enables fast control, bypassing neural central pattern generators.

Abstract

In many animals, rhythmic motor activity is governed by neural limit cycle oscillations under the control of sensory feedback. In the fruit fly Drosophila melanogaster, the wingbeat rhythm is generated myogenically by stretch-activated muscles and hence independently from direct neural input. In this study, we explored if generation and cycle-by-cycle control of Drosophila's wingbeat are functionally separated, or if the steering muscles instead couple into the myogenic rhythm as a weak forcing of a limit cycle oscillator. We behaviourally tested tethered flying flies for characteristic properties of limit cycle oscillators. To this end, we mechanically stimulated the fly's gyroscopic organs, the halteres, and determined the phase relationship between the wing motion and stimulus. The flies synchronized with the stimulus for specific ranges of stimulus amplitude and frequency, revealing the characteristic Arnold tongues of a forced limit cycle oscillator. Rapid periodic modulation of the wingbeat frequency prior to locking demonstrates the involvement of the fast steering muscles in the observed control of the wingbeat frequency. We propose that the mechanical forcing of a myogenic limit cycle oscillator permits flies to avoid the comparatively slow control based on a neural central pattern generator.