Gaze stabilization in mantis shrimp in response to angled stimuli

Abstract

Gaze stabilization is a fundamental aspect of vision and almost all animals shift their eyes to compensate for any self-movement relative to the external environment. When it comes to mantis shrimp, however, the situation becomes complicated due to the complexity of their visual system and their range of eye movements. The stalked eyes of mantis shrimp can independently move left and right, and up and down, whilst simultaneously rotating about the axis of the eye stalks. Despite the large range of rotational freedom, mantis shrimp nevertheless show a stereotypical gaze stabilization response to horizontal motion of a wide-field, high-contrast stimulus. This response is often accompanied by pitch (up-down) and torsion (about the eye stalk) rotations which, surprisingly, have no effect on the performance of yaw (side-to-side) gaze stabilization. This unusual feature of mantis shrimp vision suggests that their neural circuitry for detecting motion is radially symmetric and immune to the confounding effects of torsional self-motion. In this work, we reinforce this finding, demonstrating that the yaw gaze stabilization response of the mantis shrimp is robust to the ambiguous motion cues arising from the motion of striped visual gratings in which the angle of a grating is offset from its direction of travel.

Keywords: Eye movements; Gaze stabilisation; Motion detection; Optokinesis; Stomatopod.

Fig. 1

a The three degrees of rotational freedom in the stomatopod eye; yaw (side-to-side, blue arrow), pitch (up-down, green) and torsion (rotation about the eye axis, red). b We define ‘yaw’ as the rotation about the z-axis, in the x–y plane of the real-world coordinate system. Similarly, c ‘pitch’ is defined as the rotation about the x-axis, in the y–z plane and d torsion as the rotation about the y-axis, in the x–z plane of the real world. Calculation of pitch and torsion assumes alignment with the real-world axis, and, therefore, require compensation for the yaw pose. The pitch pose is independent of the torsion angle; it is the elevation of the eye regardless of its torsional pose. e The rotating drum and aquarium set-up including the positioning of the animal and the stereo cameras used during the experiment. Figure adapted from Fig. 2 in (Daly et al. 2017)

Fig. 2

a Three orientations of grating (φ) were presented to each animal: (i) 0°, (ii) 10°, and (iii) 20° in both directions in the horizontal plane; b (i–iii) clockwise (purple) and anticlockwise (orange). The angular offset (δ) between the stripe axis and motion direction (φ_M) is dependent on the direction of rotation (clockwise φ_M = 90°; clockwise φ_M = − 90°) and on the orientation of the grating; the values of δ for each stripe orientation during clockwise rotation are shown to the right (underlined; purple angle measure) and during anticlockwise rotation to the left (not underlined; orange angle measure). c The direction of the apparent motion in the ‘real-world’ coordinate system (calculated using the model of How and Zanker 2014) for each grating orientation during (i–iii) clockwise and (iv–vi) anticlockwise rotation at each grating orientation is represented by the blue arrow. The actual direction of motion (horizontal in all cases) is represented by the black arrow. When φ = 0°, the apparent motion of the grating is purely horizontal, whilst when φ = 10° or φ = 20°, the apparent motion has a vertical component

Fig. 3

a Examples of the stereotypical yaw optokinesis in an eye of three individual stomatopods in response to the motion of the grating rotating in the clockwise direction when the grating was oriented at 0°(top), 10° (middle) and 20° (bottom). The dotted lines indicate the progress of points on the surface of the drum, rotating in the yaw plane, but these lines do not necessarily represent specific stripe boundaries. b The yaw optokinesis (blue line) in response to the motion of the grating (φ = 20° in this example) is accompanied by pitch (green) and torsion (red) rotations, as demonstrated in the rotation of the left eye of a single individual. c The frequency distributions of the median relative velocity ratios recorded in all trials during both the slow and fast phases of yaw optokinesis across both eyes of all six individuals when the grating is oriented at φ = 0°(top), φ = 10°(middle) and φ = 20°(bottom). The dashed vertical lines indicate ‘perfect’, idealized gaze stabilisation (S_y = 1). S_y > 0 when the eye is yawing in the same direction as the drum and S_y < 0 when yawing in the opposite direction (dark blue region), as occurs during fast resets (n = 6, error bars are standard deviation across all animals in each 0.5 interval)

Fig. 4

a The frequency distributions of the median torsional angles measured in all trials during periods of drum rotation, across both eyes of all six individuals, when the grating is oriented at φ = 0° (yellow), φ = 10° (orange) and φ = 20° (red). b Gaze stabilization performance is unaffected by torsion angle at all three grating orientations [φ = 0° (yellow), φ = 10° (orange) and φ = 20° (red)], as shown by the uniform distribution of relative velocity ratios across the range of torsion rotation (n = 6, error bars are 95% confidence intervals across all animals in each 10° interval). c There is no significant cross-correlation between the angle of torsional pose and relative speed ratio (S_Y) at any grating orientation (n = 6). d Similarly, there is no significant cross-correlation between the velocity of torsional rotation and the relative speed ratio (n = 6)

Fig. 5

a The velocity of the pitch rotations shows no strong dependence on stripe orientation when the drum is rotating in the clockwise direction. Median pitch velocity across all animals shown in black, with the responses of the left (solid grey) and right (dashed grey) eye of each individual across all trials (n = 6, error bars are 95% confidence intervals across all animals in each 10° interval). b The median distribution of the pitch relative velocity during clockwise rotation of the drum when the grating is oriented at φ = 10° (top) and φ = 20° (bottom). Dashed vertical line indicates ‘perfect’, idealized gaze stabilisation (S_P = 1). S_P > 0 when the eye is pitching in the same direction as the apparent motion of the grating and S_P < 0 when yawing in the opposite direction (dark green region) (n = 6, error bars are standard deviation across all animals in each 0.5 interval). c, d Similar results are seen in response to anticlockwise rotation of the drum. The similarity in the overall distribution of the pitch speed in response to clockwise and anticlockwise rotation indicates that the mantis shrimp visual system is unaffected by the apparent downward (clockwise rotation) or upward (anticlockwise) motion generated by the horizontal movement of the tilted gratings. Note that the relative differences in the width of the distributions of S_P in response to gratings oriented at 10° and 20° is due to the calculation of S_P; the magnitude of the vertical component of apparent motion (ω_P, Eq 2, Table 2) is greater for 20° than for 10°. Since the values of the pitch speed a, c are not significantly different, when the 20 data is divided by ω_P, the resulting distribution is smaller, with a higher proportion of the S_P data in the bins closest to 0