Abstract

Neuronal representation and extraction of spatial information are essential for behavioral control. For flying insects, a plausible way to gain spatial information is to exploit distance-dependent optic flow that is generated during translational self-motion. Optic flow is computed by arrays of local motion detectors retinotopically arranged in the second neuropile layer of the insect visual system. These motion detectors have adaptive response characteristics, i.e. their responses to motion with a constant or only slowly changing velocity decrease, while their sensitivity to rapid velocity changes is maintained or even increases. We analyzed by a modeling approach how motion adaptation affects signal representation at the output of arrays of motion detectors during simulated flight in artificial and natural 3D environments. We focused on translational flight, because spatial information is only contained in the optic flow induced by translational locomotion. Indeed, flies, bees and other insects segregate their flight into relatively long intersaccadic translational flight sections interspersed with brief and rapid saccadic turns, presumably to maximize periods of translation (80% of the flight). With a novel adaptive model of the insect visual motion pathway we could show that the motion detector responses to background structures of cluttered environments are largely attenuated as a consequence of motion adaptation, while responses to foreground objects stay constant or even increase. This conclusion even holds under the dynamic flight conditions of insects.

Highlights

  • Spatial vision is a fundamental challenge for animals moving in cluttered environments, and there is no exception for flying insects

  • Following the columnar and layered structure of the visual system of flies, our model of the visual motion pathway is composed of successive layers of retinotopic arrays of model photoreceptors (PRs), large monopolar cells (LMCs), elementary motion detector (EMD), and of an lobula plate tangential cells (LPTCs) integrating the output of large arrays of EMDs (Fig 1)

  • Characterization of motion adaptation by modeling the responses to benchmark stimuli The adaptive model of the fly visual motion pathway was first tested with visual stimuli that were used in previous electrophysiological studies on fly LPTCs [26,27,28]

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Summary

Introduction

Spatial vision is a fundamental challenge for animals moving in cluttered environments, and there is no exception for flying insects. During pure rotations the retinal images of surrounding objects are displaced with the same angular velocity irrespective of distance [1] Insects, such as flies and bees, shape their flight into rapid saccadic turns of head and body and translational segments where the gaze is largely kept constant [1,2,3,4,5,6]. This behavioral strategy ‘purifies’ the translational flow by separating it from the rotational one and potentially serves the function of simplifying the computation of depth information

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