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

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 stretchactivated 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 Arnol'd 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.

Neural control and precision of flight muscle activation in Drosophila

“…The complexity of this feedback control loop, including all its facets, is still under investigation and understanding the integration process of signals coming from the compound eyes, ocelli, antennae, campaniform sensilla on wings and body, and the gyroscopic halteres remains a challenge. Thus, there is a continuing debate on which sensory feedback is needed for flight and how sensory information, for example, from halteres and eyes are temporally encoded to provide the desired precision for body posture, flight course control, and equilibrium reflexes (Sherman and Dickinson 2003, 2004; Frye and Dickinson Michael 2004; Bender and Dickinson 2006a; Huston and Krapp 2009; Frye 2010; Bartussek et al 2013; Bartussek and Lehmann 2016). A fairly comprehensive review on sensory control of insect flight was previously published by Taylor and Krapp (2007).…”

Fog and dense gas disrupt mosquito flight due to increased aerodynamic drag on halteres

“…1(a) and (b)). Halteres provide proprioceptive feedback by detecting Coriolis forces and play a crucial role in the neuromuscular circuit generating the wingbeat rhythm in Dipterans (Bartussek et al, 2013;Bender and Dickinson, 2006). By activating the motor neurons of minuscule steering muscles, halteres help regulate wing motion through a reflexive feedback loop with these muscles.…”

Motor output and control input in flapping flight: a compact model of the deforming wing kinematics of manoeuvring hoverflies

“…Other indirect steering muscles act by modifying the deformation of the thorax. Besides the obvious function of the direct steering muscles in changing the trajectory of the wing tip, or altering the amplitude and phase of the wing's pitching rotation and torsional deformation, indirect steering muscle activity may be important in controlling the frequency of the limit cycle oscillations of the stretchactivated power muscles [4]. In summary, the power muscles can be thought of as driving a limit cycle oscillation of the wing; the form and frequency of which is controlled by the steering muscles [6], [4].…”