Lateralization of retinal structure correlated with behavioral lateralization in the oval squid Sepioteuthis lessoniana

Abstract Background Cephalopods, including Sepioteuthis lessoniana , preferentially orient either the left or right eye toward visual targets during various visually guided behaviors, as most of their visual field is monocular. Such visual lateralization is widely observed in the animals whose eyes are positioned laterally on the head. However, the neural mechanisms underlying visual lateralization remain largely unclear. In this study, we investigated whether lateralization of retinal structures is correlated with behavioral lateralization toward conspecifics in the oval squid S. lessoniana . We analyzed lateralization in juvenile S. lessoniana reared in a container from eggs for 86 days, when they were maintained at a density of 0.15 individuals/L and exhibited a normal schooling behavior, one of the social behaviors in this species. Visual lateralization was quantified by analyzing which eye animals preferentially faced toward conspecifics and by calculating its laterality index. Lateralization of each retina was assessed by measuring focal length, photoreceptor cell density in the posterior retina, and the proportion of photoreceptor cells containing a single chromocenter in their nuclei. The optical properties of the eye were also examined by testing whether light passing through the retina was reflected by the argentea, the outer reflective layer of the eye. In addition, three-dimensional finite-difference time-domain simulations were performed to investigate how the number of chromocenters affects light collection in photoreceptor cells. Results Among the retinal parameters examined, only the lateralization of the proportion of photoreceptor cells containing a single chromocenter showed a significant correlation with visual lateralization toward conspecifics. Optical experiments demonstrated that light passing through the retina was reflected from the inner surface of the argentea. Simulations further indicated that photoreceptor cells containing a single chromocenter collect reflected light onto the outer segment more efficiently than those containing multiple chromocenters. Conclusions These findings suggest that the dominant eye in S. lessoniana may achieve higher contrast sensitivity because it contains a higher proportion of photoreceptor cells containing a single chromocenter, which more efficiently collects light on the outer segment. Such lateralization in retinal structure may enhance the detection of weak visual signals from conspecifics and contribute to visual lateralization during social interactions.