Insect navigational behaviors including obstacle avoidance, grazing landings, and visual odometry are dependent on the ability to estimate flight speed based only on visual cues. In honeybees, this visual estimate of speed is largely independent of both the direction of motion and the spatial frequency content of the image. Electrophysiological recordings from the motion-sensitive cells believed to underlie these behaviors have long supported spatio-temporally tuned correlation-type models of visual motion detection whose speed tuning changes as the spatial frequency of a stimulus is varied. The result is an apparent conflict between behavioral experiments and the electrophysiological and modeling data. In this article, we demonstrate that conventional correlation-type models are sufficient to reproduce some of the speed-dependent behaviors observed in honeybees when square wave gratings are used, contrary to the theoretical predictions. However, these models fail to match the behavioral observations for sinusoidal stimuli. Instead, we show that non-directional motion detectors, which underlie the correlation-based computation of directional motion, can be used to mimic these same behaviors even when narrowband gratings are used. The existence of such non-directional motion detectors is supported both anatomically and electrophysiologically, and they have been hypothesized to be critical in the Dipteran elementary motion detector (EMD) circuit.
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