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

Abstract

The term biological motion refers to the peculiar kinematics of living organisms. Their interconnected joints move at a fixed distance from each other, a pattern that is common among all locomotive, rigid animals. Across the animal kingdom, many species have developed specialized circuitry to visually recognize biologically moving stimuli and discriminate them from other patterns. Recently, this skill has also been observed in the distributed visual system of jumping spiders. These eight-eyed animals use three of their eye pairs to perceive motion. Then, the gaze of the remaining pair is shifted towards the detected object for further inspection. When presented with a biologically moving stimulus and a random one, jumping spiders turn to face the latter, demonstrating discrimination. In the current paper, we systematically tested the ability of jumping spiders to discriminate biological from random displays using every single eye-pair, by blocking the others with paint. The animals were able to discriminate the stimuli only when the anterior-lateral eyes were unblocked, performing at chance level with the other pairs. Crucially, the spiders preferred the biological stimulus, not the random one. To explain this preference reversal we hypothesized a model, describing how the anterior-lateral eyes specialization in detecting biological motion feeds into a multi-eye integration system, generating more complex behavior from the combination of the simple, single-eye responses. We propose that this in-built modularity may be a solution to the limited resources of these invertebrates brains, constituting a novel approach to visual processing.