Controlling roll perturbations in fruit flies

Abstract

Owing to aerodynamic instabilities, stable flapping flight requires ever-present fast corrective actions. Here, we investigate how flies control perturbations along their body roll angle, which is unstable and their most sensitive degree of freedom. We glue a magnet to each fly and apply a short magnetic pulse that rolls it in mid-air. Fast video shows flies correct perturbations up to 1008 within 30 + 7 ms by applying a stroke-amplitude asymmetry that is well described by a linear proportional-integral controller. For more aggressive perturbations, we show evidence for nonlinear and hierarchical control mechanisms. Flies respond to roll perturbations within 5 ms, making this correction reflex one of the fastest in the animal kingdom.

Flight mechanics and control of escape manoeuvres in hummingbirds I. Flight kinematics

“…For animals as small as fruit flies, if they were to use similar amounts of change in wing kinematics as hummingbirds, the accelerations generated would quickly destabilize their flight, and their sensorimotor system may not respond rapidly enough to ensure a stable flight (Chang and Wang, 2014). Fruit flies only use subtle wing kinematic changes in free-flight manoeuvres Fry et al, 2003;Muijres et al, 2015) except when being forced into extreme flight conditions with significantly higher body rates than those found in the free-flight manoeuvres (Beatus et al, 2015). Although subtle wing kinematic changes are sufficient for generating rotational moments in fruit flies, this may limit their ability to change the directions of aerodynamic forces.…”

“…These patterns are novel information for hummingbirds; in comparison with insects, whose wing kinematics during various types manoeuvres are available from previous work (Beatus et al, 2015;Cheng et al, 2011;Fry et al, 2003;Muijres et al, 2014;Taylor, 2001). It has been observed that hummingbirds are able to rapidly generate substantial changes of their wing motion for manoeuvring.…”

To crash or not to crash: how do hoverflies cope with free-fall situations and weightlessness?

“…The response latencies recorded here were much longer than those involved in the mechanosensory responses elicited, for example, by stimulated halteres within only 5 ms via a feedforward control pathway (Sandeman and Markl, 1980). In addition, fruit-flies took only 45 ms to reject a yaw perturbation via a heading feedback loop (Ristroph et al, 2010), 5 ms to detect a roll disturbance and elicit counter-torque movements and 30 ms to reject the perturbation (Beatus et al, 2015). If an early gravity perception process was involved in the insects' responses to free-fall situations, similar wingbeat initiation rates could be expected to occur in darkness, and faster mean reaction times would therefore have been recorded than those measured here in the most favourable visual condition (around 110 ms in the presence of stripes), contradicting the existence of an accelerometer-like organ in dipteran.…”

Flight mechanics and control of escape manoeuvres in hummingbirds II. Aerodynamic force production, flight control and performance limitations

“…Coordination of body and wing movements in rapid flight manoeuvres also demands sensorimotor transduction that computes and enforces flight-control algorithms with desired computation complexity and speed (Beatus et al, 2015;Fuller et al, 2014;Ristroph et al, 2013;Roth et al, 2012). For fruit flies (Drosophila), large sensorimotor delay prevents their mechanosensory organs from stabilizing unstable flight dynamics (Chang and Wang, 2014;Elzinga et al, 2012) and results in unstable oscillation of ground-speed regulation under high-gain visual feedback (Fuller et al, 2014).…”

“…A rigorous analysis of insect sensorimotor flight control can be derived from parsimonious modelling of the physics of flight (or mechanical models, Miller et al, 2012) and neural sensing and motor systems in the framework of classical feedback control theory (Cowan et al, 2014;Franklin et al, 1994). This approach has received increasing attention recently, applied to pitching manoeuvres of hawkmoths , flight stabilization of fruit flies under perturbations that induce roll (Beatus et al, 2015), pitch (Ristroph et al, 2013) and yaw (Ristroph et al, 2010), and ground-speed regulation using visual and mechanosensory feedbacks (Fuller et al, 2014).…”