Humans, macaque monkeys, cats, horses, sheep, owls, falcons, & toads have stereopsis; in cuttlefish, stereopsis. works differently to vertebrates (extract stereopsis cues from anticorrelated stimuli)

Cuttlefish use stereopsis to strike at prey. R. C. Feord et al. Science Advances  Jan 08 2020: Vol. 6, no. 2, eaay6036. DOI: 10.1126/sciadv.aay6036

Abstract: The camera-type eyes of vertebrates and cephalopods exhibit remarkable convergence, but it is currently unknown whether the mechanisms for visual information processing in these brains, which exhibit wildly disparate architecture, are also shared. To investigate stereopsis in a cephalopod species, we affixed “anaglyph” glasses to cuttlefish and used a three-dimensional perception paradigm. We show that (i) cuttlefish have also evolved stereopsis (i.e., the ability to extract depth information from the disparity between left and right visual fields); (ii) when stereopsis information is intact, the time and distance covered before striking at a target are shorter; (iii) stereopsis in cuttlefish works differently to vertebrates, as cuttlefish can extract stereopsis cues from anticorrelated stimuli. These findings demonstrate that although there is convergent evolution in depth computation, cuttlefish stereopsis is likely afforded by a different algorithm than in humans, and not just a different implementation.

DISCUSSION

To ensure that cuttlefish hit their prey successfully, they must acquire information about its location before the strike. Here, we show that cuttlefish use the disparity between their left and right eyes to perceive depth (Fig. 1). Cuttlefish use this information to aid in prey capture, as animals with intact binocular vision take less time to strike at prey and do so from farther away (Fig. 2.). In animals tested with quasi-monocular stimuli, the significant difference in latency, travel distance, and strike location during the positioning phase is consistent with Messenger’s study (7), as he found that attack success in unilaterally blinded animals decreased to 56% (versus 91% in binocular animals). Nonetheless, binocular cues cannot be the only depth perception mechanism used by the cuttlefish, as many quasi-monocularly and binocularly stimulated animals behaved equally well, both in Messenger’s study and ours. The absence of pictorial cues in our stimulus (the shrimp silhouette lacks any shadowing, shading, or occlusion) leads us to conclude that for monocular but not binocular depth perception, cuttlefish may rely on motion cues such as parallax (13) and/or motion in depth (19).

Before our investigation, cuttlefish were not known to use stereopsis (i.e., calculate depth from disparity between left and right eye views). They had been shown only to have a variable range of binocular overlap (7). Using anaglyph glasses and this 3D perception assay, we provide strong support that cuttlefish have and use stereopsis during the positioning to prey seizure phases of the hunt. However, as suggested by Messenger (7), other depth estimation strategies, such as oculomotor proprioceptive cues provided by the vergence of the two eyes (20, 21), could be at play. Accommodation cues, as used by chameleons to judge distance (22), could also provide an additional explanation as lens movements have been observed in cuttlefish (23). However, if proprioceptive or accommodation cues were being used by cuttlefish for depth estimation, it should not fail as it did when presented with a completely uncorrelated stimulus, i.e., each eye should still fixate and converge on the moving target without requiring correspondence between the images (Fig. 3). We observed that cuttlefish consistently engaged and reached the positioning phase when presented with uncorrelated stimuli, but they quickly aborted and never advanced to the striking phase of the hunt (movie S4). Because they could not solve the uncorrelated stimuli test, we conclude that cuttlefish rely on interocular correspondence to integrate binocular cues and not simply use binocular optomotor cues (vergence) or accommodation to estimate depth. This also indicates that cuttlefish stereopsis is different from praying mantis (also known as mantids) stereopsis, because mantids can resolve targets based on “kinetic disparity” (the difference in the location of moving object between both eyes) (16). Mantids can do this in the absence of “static disparity” provided by the surrounding visual scene, something which humans are unable to do (16).

To see how binocular overlap may play a role in stereopsis, we investigated eye convergence. A disparity difference of up to 10° between the left and right eye angular positions at the moment when they strike may seem large (Fig. 4). However, cuttlefish have a relatively low-resolution retina, 2.5° to 0.57° per photoreceptor (24). Thus, cuttlefish image disparity relative to their eye resolution is comparable to the relative magnitudes observed for these measures in vertebrates. Cuttlefish’s lower spatial resolution makes it plausible that they may also have neurons that encode disparity across a larger array of visual angles, as known to be the case in mice (25). To coordinate the relative positions of the left and right receptive fields for object tracking, cuttlefish may have evolved similar circuits as those used by chameleons for synchronous and disconjugate saccades (26, 27) and by rats for a greater overhead binocular field (28).

The evidence presented here establishes that cuttlefish make use of stereopsis when hunting and that this improves hunting performance by reducing the distance traveled, the time taken to strike at prey, and allowing it to strike from farther away. Further investigation is required to uncover the neural mechanisms underlying the computation of stereopsis in these animals.