Gravity-Dependent Animacy Perception in Zebrafish

Biological motion (BM), depicted by a handful of point lights attached to the major joints, conveys rich animacy information, which is significantly disrupted if BM is shown upside down. This well-known inversion effect in BM perception is conserved in terrestrial vertebrates and is presumably a manifestation of an evolutionarily endowed perceptual filter (i.e., life motion detector) tuned to gravity-compatible BM. However, it remains unknown whether aquatic animals, living in a completely different environment from terrestrial animals, perceive BM in a gravity-dependent manner. Here, taking advantage of their typical shoaling behaviors, we used zebrafish as a model animal to examine the ability of teleosts to discriminate between upright (gravity-compatible) and inverted (gravity-incompatible) BM signals. We recorded their swimming trajectories and quantified their preference based on dwelling time and head orientation. The results obtained from three experiments consistently showed that zebrafish spent significantly more time swimming in proximity to and orienting towards the upright BM relative to the inverted BM or other gravity-incompatible point-light stimuli (i.e., the non-BM). More intriguingly, when the recorded point-light video clips of fish were directly compared with those of human walkers and pigeons, we could identify a unique and consistent pattern of accelerating movements in the vertical (gravity) direction. These findings, to our knowledge, demonstrate for the first time the inversion effect in BM perception in simple aquatic vertebrates and suggest that the evolutionary origin of gravity-dependent BM processing may be traced back to ancient aquatic animals.