Biological motion as an innate perceptual mechanism driving social affiliation

Abstract

Collective behavior, such as shoaling in teleost fish, is driven by the perceptual recognition of conspecific animals. Because social interactions are mutual, it has been difficult to disentangle the exact sensory cues that trigger affiliation in the first place from those that are emitted by receptive and responsive shoal mates. Here we overcome this challenge in a virtual reality assay in zebrafish. We discovered that simple visual features of conspecific biological motion provide an irresistible shoaling cue. Individual juvenile fish interact with circular black dots projected onto a screen, to the same extent as they do with real conspecifics, provided these virtual objects mimic the characteristic kinetics of zebrafish swim bouts. Other naturalistic cues previously implicated in shoaling, such as fish-like shape, pigmentation pattern, or non-visual sensory modalities are not required. During growth, the animals stimulus preferences shift gradually, matching self-like kinetics, even in fish raised in isolation. Virtual group interactions and our multi-agent model implementation of this perceptual mechanism demonstrate sufficiency of kinetic cues to drive assortative shoaling, a phenomenon commonly observed in field studies. Coordinated behavior can emerge from autonomous interactions, such as collective odor avoidance in Drosophila, or from reciprocal interactions, such as the codified turn-taking in wren duet singing. We found that individual zebrafish shoal autonomously without evidence for a reciprocal choreography. Our results reveal individual-level, innate perceptual rules of engagement in mutual affiliation and provide experimental access to the neural mechanisms of social recognition. (239/250 words max)\n\nSignificance StatementSocial affiliation is ubiquitous in the animal kingdom, but fundamental sensory cues driving group formation remain elusive. During swarm behavior, for example, individuals dynamically exchange sensory cues with their neighbors, presenting an intertwined choreography opaque to formal analysis of causal stimulus-response relationships. Using a virtual interaction assay for psychophysical analysis, we solved this issue and identify biological motion as the irresistible trigger of social affiliation in zebrafish, Danio rerio. Given that many species form groups including shoals, flocks and herds, perceptual mechanisms of social recognition and their underlying neural circuits are likely shared across vertebrates. The identification of fundamental affiliation-inducing cues is a prerequisite for relating individual-level sensory-motor transformations to collective behavior. (112/120 words max)