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.

Akin to all damselflies, Calopteryx (family Calopterygidae), commonly known as jewel wings or demoiselles, possess dichoptic (separated) eyes with overlapping visual fields of view. In contrast, many dragonfly species possess holoptic (dorsally fused) eyes with limited binocular overlap. We have here compared the neuronal correlates of target tracking between damselfly and dragonfly sister lineages and linked these changes in visual overlap to premotor neural adaptations. While dragonflies attack prey dorsally, we show that demoiselles attack prey frontally. We identify demoiselle Target Selective Descending Neurons (TSDNs) with matching frontal visual receptive fields, anatomically and functionally homologous to the dorsally-positioned dragonfly TSDNs. By manipulating visual input using eyepatches and prisms, we show that moving target information at the premotor level depends on binocular summation in demoiselles. Consequently, demoiselles encode directional information in a binocularly fused frame of reference such that information of a target moving towards the midline in the left eye is fused with information of the target moving away from the midline in the right eye. This contrasts with dragonfly TSDNs where receptive fields possess a sharp midline boundary, confining responses to a single visual hemifield in a sagittal frame of reference (i.e. relative to the midline). Our results indicate that although TSDNs are conserved across Odonata, their neural inputs, and thus the upstream organization of the target tracking system, differs significantly and match divergence in eye design and predatory strategies.

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