Experience dependent modulation of collective behavior in larval zebrafish
Collective behaviors such as schooling in fish and flocking in birds are crucial for animal survival, providing protraction form predators, and improving foraging and navigation abilities. These large-scale group patterns were shown to emerge from simple and local inter-individual interactions. Commonly, these interactions are considered static and hardwired, and little is known about how experience and learning affect collective group behavior. Previously, we mapped the sensory-motor transformations that govern collective swimming behavior in larval zebrafish throughout their development and described the neural circuits involved in these computations (Harpaz et al., 2021). Here, we explored how groups of animals dynamically modify their collective behaviors to adapt to changing social conditions. We found that larval zebrafish modulate their inter-individual interactions and resulting collective behaviors in response to acute changes in their population density. Using naturalistic and virtual reality experiments we show that fish swimming in a specific group density will exhibit weaker (stronger) interactions if they were previously exposed to higher (lower) neighbor densities. These adaptations develop slowly over tens of minutes. Mechanistically, we show that larvae estimate their group density by temporally integrating changes in visual occupancy and couple the strength of their interactions to that estimate. A time-varying state-space model that modulates agents’ social interactions based on their previous social experiences, accurately describes our behavioral observations, and predicts novel aspects of behavior that were confirmed in subsequent experiments. These findings provide concrete evidence that inter-individual interactions are not static, but rather continuously evolve based on experience and current environmental demands. The underlying neurobiological mechanisms of experiences dependent modulation of collective behavior can now be explored in this species.