A comparative study of gaze stabilisation in Dipteran flies

Abstract

Flying insects, like many other animals that rely on their sense of vision to guide behaviour, have a tendency to maintain a default orientation of their eyes relative to the environment. During flight, reflexes act to keep the head level and minimise retinal image shifts resulting from rotational steering manoeuvres, or from external perturbations such as wind gusts and turbulent air flow. Gaze stabilisation serves a number of functions, which include: i) simplifying the estimation of translational self-motion, ii) aligning the head-based sensory systems with the inertial vector which facilitates the transformation of sensory signals into motor commands, iii) supporting the tracking of moving targets, and iv) reducing motion blur in the visual input. This thesis reports studies on species-specific adaptations and general principles underlying multisensory gaze stabilisation in a number of different Dipteran flies. A variety of stimulation methods were explored, along with their suitability for a linear systems analysis of the gaze stabilisation system across species. Using results obtained from the well-characterised blowfly for comparison, novel experimental work was performed on the gaze stabilisation behaviour of robberflies, hoverflies and horseflies. Species from each family were shown to stabilise their heads in compensation for body rotations around the roll axis. The performance of the reflex was found to be species-specific and dependent on the sensory modalities involved. Experimental evidence suggests that in contrast to the other families, hoverflies appear to make use of the inertia of the head to maintain a level gaze, a novel finding that has previously been reported only for dragonflies. Finally, the integration of signals in the context of gaze stabilisation obtained by the two visual systems in blowflies - the ocelli and compound eyes - were explored in both behavioural and electrophysiological experiments. This research opens new lines of investigation by identifying behaviours that demonstrate different control strategies employed by the nervous systems of flying insects.