Abstract

In many animal phyla, eyes are small and provide only low-resolution vision for general orientation in the environment. Because these primitive eyes rarely have a defined image plane, traditional visual-optics principles cannot be applied. To assess the functional capacity of such eyes we have developed modelling principles based on ray tracing in 3D reconstructions of eye morphology, where refraction on the way to the photoreceptors and absorption in the photopigment are calculated incrementally for ray bundles from all angles within the visual field. From the ray tracing, we calculate the complete angular acceptance function of each photoreceptor in the eye, revealing the visual acuity for all parts of the visual field. We then use this information to generate visual filters that can be applied to high resolution images or videos to convert them to accurate representations of the spatial information seen by the animal. The method is here applied to the 0.1 mm eyes of the velvet worm Euperipatoides rowelli (Onychophora). These eyes of these terrestrial invertebrates consist of a curved cornea covering an irregular but optically homogeneous lens directly joining a retina packed with photoreceptive rhabdoms. 3D reconstruction from histological sections revealed an asymmetric eye, where the retina is deeper in the forward-pointing direction. The calculated visual acuity also reveals performance differences across the visual field, with a maximum acuity of about 0.11 cycles/deg in the forward direction despite laterally pointing eyes. The results agree with previous behavioural measurements of visual acuity, and suggest that velvet worm vision is adequate for orientation and positioning within the habitat.

Highlights

  • A detailed mapping of an animal’s visual performance across its entire visual field is extremely informative for revealing the roles vision may have in that species [1,2,3]

  • It is difficult to understand the roles that vision may have in animals with visual performance very different to our own

  • Many invertebrates such as flatworms, polychaetes, onychophorans, gastropod molluscs and numerous arthropods have tiny eyes with unknown visual abilities

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Summary

Introduction

A detailed mapping of an animal’s visual performance across its entire visual field is extremely informative for revealing the roles vision may have in that species [1,2,3]. Signal-to-noise ratios, and photoreceptor temporal properties, all determine what an animal can see, but perhaps the most informative measures are the retinal sampling matrix (pixel density) and the angular sensitivity of each photoreceptor. It is the latter types of information that determines the spatial visual performance (visual acuity) and how it varies over the visual field. Mapping of ommatidial axes in compound eyes or measurements of retinal ganglion cell densities in vertebrate eyes are examples of approaches aimed at revealing the “pixel density” of vision

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