Behavioural evidence for a visual and proprioceptive control of head roll in hoverflies (Episyrphus balteatus, Dipteran)

Abstract

The ability of hoverflies to control their head orientation with respect to their body contributes importantly to their agility and their autonomous navigation abilities. Many tasks performed by this insect during flight, especially while hovering, involve a head stabilization reflex. This reflex, which is mediated by multisensory channels, prevents the visual processing from being disturbed by motion blur and maintains a consistent perception of the visual environment. The so-called dorsal light response (DLR) is another head control reflex, which makes insects sensitive to the brightest part of the visual field. In this study, we experimentally validate and quantify the control loop driving the head roll with respect to the horizon in hoverflies. The new approach developed here consisted of using an upside-down horizon in a body roll paradigm. In this unusual configuration, tethered flying hoverflies surprisingly no longer use purely vision-based control for head stabilization. These results shed new light on the role of neck proprioceptor organs in head and body stabilization with respect to the horizon. Based on the responses obtained with male and female hoverflies, an improved model was then developed in which the output signals delivered by the neck proprioceptor organs are combined with the visual error in the estimated position of the body roll. An internal estimation of the body roll angle with respect to the horizon might explain the extremely accurate flight performances achieved by some hovering insects.

Head roll stabilisation in the nocturnal bull ant Myrmecia pyriformis: Implications for visual navigation

“…Viollet and Zeil, 2013;Goulard et al, 2015): firstly, we did not detect delays at least at a temporal resolution of 8 ms (Fig. 4C,D); secondly, ants are able to compensate to some degree even in total darkness (Fig.…”

“…Thus, while vision contributes to head roll stabilisation in M. pyriformis workers, there are also non-visual mechanisms, most likely mechanoreceptors (e.g. Goulard et al, 2015) or an efference copy (e.g. Viollet and Zeil, 2013), that mediate this response.…”

“…The importance of head stabilisation has been recognised in the context of the control of locomotion, heading direction, the reduction of image motion blur and the separation of rotational and translational optic flow (Land, 1999(Land, , 2015Zeil et al, 2008;see also Beatus et al, 2015;Goulard et al, 2015). However, it has only recently been considered in the context of the image (snapshot)-matching process (Ardin et al, 2015) that is thought to underlie the use of route and place memories for navigation (reviewed in Collett et al, 2013;Zeil, 2012).…”

“…Flying insects are able to keep the roll and pitch orientation of the head constant despite large, but predictable, changes of orientation of the thorax associated with flight control (Beatus et al, 2015;Boeddeker et al, 2010;Goulard et al, 2015;Land, 1973;Schilstra and van Hateren, 1998;Viollet and Zeil, 2013). Walking insects, however, face not only the predictable stride-cycle-dependent body oscillations but also unpredictable ground topography-dependent body rotations Egelhaaf, 2012, 2014).…”

It's Not a Bug, It's a Feature: Functional Materials in Insects

“…On the other hand, the hoverfly, Episyphrus balteatus, has a more developed structural and muscular head support than dragonflies, which it is able to manipulate with the help of tactile hair feedback. [209] This feedback acts in combination with visual cues to orient both the head and body of the hoverfly in a horizon-locked position. Head positioning is also important for walking insects, which face disruptions from step movements as well as inconsistent surface topographies.…”