Differential adaptation to visual motion allows robust encoding of optic flow in the dragonfly

Abstract

1An important task for any aerial creature is the ability to ascertain their own movement (egomotion) through their environment. Neurons thought to underlie this behaviour have been well-characterised in many insect models including flies, moths and bees. However, dragonfly wide-field motion pathways remain undescribed. Some species of Dragonflies, such as Hemicordulia tau, engage in hawking behaviour, hovering in a single area for extended periods of time whilst also engaging in fast-moving patrols and highly dynamic pursuits of prey and conspecifics. These varied flight behaviours place very different constraints on establishing ego-motion from optic flow cues hinting at a sophisticated wide-field motion analysis system capable of detecting both fast and slow motion.\n\nWe characterised wide-field motion sensitive neurons via intracellular recordings in Hemicordulia dragonflies finding similar properties to those found in other species. We found that the spatial and temporal tuning properties of these neurons were broadly similar but differed significantly in their adaptation to sustained motion. We categorised a total of three different subclasses, finding differences between subclasses in their motion adaptation and response to the broadband statistics of natural images. The differences found correspond well with the dynamics of the varied behavioural tasks hawking dragonflies perform. These findings may underpin the exquisite flight behaviours found in dragonflies. They also hint at the need for the great complexity seen in dragonfly early visual processing.\n\n2 Significance StatementUnderstanding how animals navigate the world is an inherently difficult and interesting problem. Insect models have elucidated the neuronal mechanisms, which underpin this process. Neurons that encode wide-field motion have been studied previously in insects such as flies, hawkmoths and butterflies. Dragonflies exhibit complex aerobatic behaviours such as hovering, patrolling and aerial combat but little is known of their optic physiology. Moreover, dragonflies lack multimodal inputs (such as halteres in flies), which help enable diverse behaviours. The present study characterises wide-field motion sensitive neurons in the dragonfly. We find that wide-field motion sensitive neurons in dragonflies exhibit multiple subtypes, differentiated by their motion adaptation enabling encoding of a broad range of velocities independent of background contrast.