Extraocular Photoreception in Optic Lobes, Suckers, and Skin of Octopus vulgaris.

Abstract

Coleoid cephalopods like octopuses, squids, and cuttlefishes have advanced light-sensing systems crucial for visual perception and survival. Previously, it has been demonstrated that the skin of coleoids contains transcripts encoding rhodopsin and retinochrome, exhibiting a dermal light sense. Moreover, chromatophores in the mantle skin of Octopus bimaculoides expand in response to light when completely isolated from the central nervous system and eyes. In our study combining morphology, gene expression, molecular evolution, 3D modeling of protein structures, and phylogenetic analysis, we demonstrated the presence of photosensitive pigment transcripts in Octopus vulgaris, not only in eyes and skin but also in suckers and even optic lobes. In particular, for the first time, the RNA expression of Ov-Rhodopsin, Ov-retinochrome, and Ov-GRK1 was found and quantified in the skin and also localized in different sucker types and the optic lobes. The obtained results suggest that suckers act as extraocular organs. Each of the approximately 1000 suckers contributes to the distributed light perception system, collectively acquiring environmental information that could support eye vision. Our findings could explain octopuses' extraordinary ability to camouflage. Furthermore, the optic lobes, which are part of the central nervous system, could be directly involved in light detection, in addition to their role in the integration of sensory information.