Reverse engineering the control law for schooling in zebrafish using virtual reality

Abstract Revealing the evolved mechanisms that give rise to collective behavior is a central objective in the study of cellular and organismal systems1-12. In addition, understanding the algorithmic basis of social interactions in a causal and quantitative way offers an important foundation for subsequently quantifying social deficits13-16. Here, we employ immersive Virtual Reality (VR)17 to reverse-engineer the sensory-motor control of social response during schooling in a vertebrate model: juvenile zebrafish (Danio rerio). In addition to providing a highly-controlled means to understand how zebrafish translate visual input to movement decisions, networking our systems allows real fish to swim and interact together in the same virtual world. Together, this allows us to directly test models of social interactions in situ. A key feature of social response is shown to be single- and multi-target-oriented pursuit. This is based on a quasi-2D egocentric representation of the positional information of conspecifics, and is highly robust to incomplete sensory input. We demonstrate, including with a 'Turing test' for pursuit behavior, that all key features of this behavior are accounted for by individuals following a simple experimentally-derived proportional derivative control law, which we term 'BioPD'. Since target pursuit is key to effective control of autonomous vehicles, we evaluate—as a proof of principle—the potential utility of this simple evolved control law for human-engineered systems. In doing so, we find close-to-optimal performance in autonomous vehicles (terrestrial, airborne, and watercraft) pursuit, while requiring limited system-specific tuning or optimization.