Integration of social and depth information during affiliative behavior in zebrafish

Social animals need to process information constantly from their social partners and the physical environment. Notably, the distance between conspecifics plays an important role in social decision-making, such as territorial defense and courtship. However, how social and depth information are integrated to control responses to conspecifics remains largely unknown. Here, we have developed a virtual reality (VR) system that systematically manipulates animal behaviors and depth sensation. Our virtual zebrafish expressed naturalistic behaviors that triggered a strong and sustained affiliative response in real zebrafish, outcompeting the response triggered by fish of other species. Biological translocation by virtual animals proved sufficient to trigger affiliative responses. Surprisingly, stationary behaviors, such as orientation changes and tail bending, only triggered affiliative responses in the presence of depth sensation. In addition, unexpected visual motion of conspecifics, either in time or direction, triggered affiliative responses, indicating predictive processing of conspecific visual motion based on depth sensation. Together, our results reveal that depth sensation can either synergize or suppress social information in different contexts. These results also support the necessity of including depth information when designing visual stimuli for investigations of natural behaviors. VIDEO ABSTRACT.