Eye-specific detection and a multi-eye integration model of biological motion perception

Abstract

‘Biological motion’ refers to the distinctive kinematics observed in many living organisms, where visually-observable points on the animal move at fixed distances from each other. Across the animal kingdom, many species have developed specialized visual circuitry to recognize such biological motion and to discriminate it from other patterns. Recently, this ability has been observed in the distributed visual system of jumping spiders. These eight-eyed animals usesix eyes to perceive motion, while the remaining two (the principal anterior-medial eyes) are shifted across the visual scene to further inspect detected objects. When presented with a biologically moving stimulus and a random one, jumping spiders turn to face the latter, clearly demonstrating the ability to discriminate between them. However, it remains unclear if the principal eyes are necessary for this behavior, whether all secondary eyes can perform this discrimination, or if a single eye-pair is specialized for this task. Here, we systematically tested the ability of jumping spiders to discriminate between biological and random visual stimuli by testing each eye-pair alone. Spiders were able to discriminate stimuli only when the anterior-lateral eyes were unblocked, and performed at chance levels in other configurations. Interestingly, spiders showed a preference for biological motion over random stimuli—unlike in past work. We therefore propose a new model describing how specialization of the anterior-lateral eyes for detecting biological motion contributes to multi-eye integration in this system. This integration generates more complex behavior through the combination of simple, single-eye responses. We posit that this in-built modularity may be a solution to the limited resources of these invertebrates’ brains—constituting a novel approach to visual processing.