Complex gaze stabilization in mantis shrimp.

Ilse M Daly,Nicholas W Roberts,Julian C Partridge,Martin J How

doi:10.1098/rspb.2018.0594

Abstract

Almost all animals, regardless of the anatomy of the eyes, require some level of gaze stabilization in order to see the world clearly and without blur. For the mantis shrimp, achieving gaze stabilization is unusually challenging as their eyes have an unprecedented scope for movement in all three rotational degrees of freedom: yaw, pitch and torsion. We demonstrate that the species Odontodactylus scyllarus performs stereotypical gaze stabilization in the yaw degree of rotational freedom, which is accompanied by simultaneous changes in the pitch and torsion rotation of the eye. Surprisingly, yaw gaze stabilization performance is unaffected by both the torsional pose and the rate of torsional rotation of the eye. Further to this, we show, for the first time, a lack of a torsional gaze stabilization response in the stomatopod visual system. In the light of these findings, we suggest that the neural wide-field motion detection network in the stomatopod visual system may follow a radially symmetric organization to compensate for the potentially disorientating effects of torsional eye movements, a system likely to be unique to stomatopods.

Highlights

Moving animals are confronted with a visual trade-off: their eyes are more efficient at detecting salient features of a scene and local motion cues when they are fixed relative to the outside world and yet, for many tasks, having movable eyes provides an adaptive advantage
We investigate the role of torsional eye movements during gaze stabilization in the stomatopod Odontodactylus scyllarus and ask three questions: do the eyes rotate torsionally during optokinetic responses to a horizontally displaced field of view? Do torsional rotations affect the yaw gaze stabilization performance? Is there evidence for gaze stabilization in the torsional degree of freedom?
Overall the median maximum cross-correlation coefficient was not significantly different from 0 for yaw and torsion rotation, yaw and pitch rotations or pitch and torsion rotation (Wilcoxon signed-rank test, n 1⁄4 17, V 1⁄4 117, p . 0.05, full statistics in electronic supplementary material, S3; figure 2e). These findings demonstrate that stomatopods are able to independently rotate their eyes in the three degrees of rotational freedom, but that these rotations can become coupled in some instances, such as the yaw and torsion rotation during optokinesis shown in figure 2a,b

Summary

Introduction

Moving animals are confronted with a visual trade-off: their eyes are more efficient at detecting salient features of a scene and local motion cues when they are fixed relative to the outside world and yet, for many tasks, having movable eyes provides an adaptive advantage Overcoming this problem is a visual challenge that has resulted in the evolution of systems that steady the retinal projection of the external visual scene for periods of time. Without adequate visual compensation for rotational and translational movements of the body, an animal’s egocentric coordinate system can become misaligned with real-world coordinates, so body posture and equilibrium may become compromised [4] To counteract these degrading visual effects, animals make compensatory movements with their eyes, head or body depending on their individual anatomy to reduce movement of the retinal image [2]. This is known as gaze stabilization, and is common to both vertebrates and arthropods

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