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

Abstract

Visual cues provide an important means for aerial creatures to ascertain their self-motion through the environment. In many insects including flies, moths and bees, wide-field motion-sensitive neurons in the 3rd optic ganglion are thought to underlie such motion encoding, however these neurons can only respond robustly over limited speed ranges. The task is more complicated for some species of dragonflies that switch between extended periods of hovering flight and fast-moving pursuit of prey and conspecifics, requiring motion detection over a broad range of velocities. Since little is known about motion processing in these insects, we performed intracellular recordings from hawking, emerald dragonflies (Hemicordulia spp.) and identified a diverse group of motion sensitive neurons that we named Lobula Tangential Cells (LTCs). Following prolonged visual stimulation with drifting gratings, we observed significant differences in both temporal and spatial tuning of LTCs. Cluster analysis of these changes confirmed several groups of LTCs with distinctive spatiotemporal tuning. These differences were associated with variation in velocity tuning in response to translated, natural scenes.LTCs with differences in velocity tuning ranges and optima may underlie how a broad range of motion velocities are encoded. In the hawking dragonfly, changes in LTCs tuning over time are therefore likely to support their extensive range of behaviours, from hovering to fast speed pursuits.SIGNIFICANCE STATEMENTUnderstanding how animals navigate the world is an inherently difficult and interesting problem. Insects are useful models for understanding neuronal mechanisms underlying these activities, with neurons that encode wide-field motion previously identified in insects such as flies, hawkmoths and butterflies. Like some Dipteran flies, dragonflies exhibit complex aerobatic behaviours such as hovering, patrolling and aerial combat. However, dragonflies lack halteres that support such diverse behaviour in flies. To understand how dragonflies might address this problem using only visual cues, we recorded from their wide-field motion sensitive neurons. We found these differ strongly in the ways they respond to sustained motion, allowing them collectively to encode the very broad range of velocities experienced during diverse behaviour.