Abstract
Complex schooling behaviors result from local interactions among individuals. Yet, how sensory signals from neighbors are analyzed in the visuomotor stream of animals is poorly understood. Here, we studied aggregation behavior in larval zebrafish and found that over development larvae transition from overdispersed groups to tight shoals. Using a virtual reality assay, we characterized the algorithms fish use to transform visual inputs from neighbors into movement decisions. We found that young larvae turn away from virtual neighbors by integrating and averaging retina-wide visual occupancy within each eye, and by using a winner-take-all strategy for binocular integration. As fish mature, their responses expand to include attraction to virtual neighbors, which is based on similar algorithms of visual integration. Using model simulations, we show that the observed algorithms accurately predict group structure over development. These findings allow us to make testable predictions regarding the neuronal circuits underlying collective behavior in zebrafish.
Highlights
Complex schooling behaviors result from local interactions among individuals
Understanding how sensory signals coming from surrounding neighbors guide fast and accurate movement decisions is central to the understanding of emergent collective behavior and is of great interest from both computational and neurobiological perspectives[7]
Older larvae (17–26 dpf) and adults were shown to be attracted to projected moving objects that exhibit movement dynamics of real fish[31,46]. Extending these studies to 7 dpf larvae in our virtual reality (VR) assay, we found that fish turn away from projected dots that mimic the motion of real neighbors (Fig. S2a–c, “Methods”), capturing both the group structure and response tendencies observed in our group swimming experiments (Fig. 1c, f)
Summary
Group structure in larval zebrafish depends on visual social interactions. To understand how social interactions shape group structure over development, we studied collective swimming behavior in groups of 5 or 10 larval zebrafish at the ages 7, 14, and. We used the VR assay to explore the way 14 and 21 dpf larvae integrate and respond to visual occupancy, as fish at these ages begin turning towards their neighbors as opposed to the purely repulsive interactions at 7 dpf (Fig. 1d, f) For both these older age groups, we observed the emergence of attraction to projected stimuli of small angular size, in combination with repulsion from larger stimuli (Fig. 3a, b, “Methods”). Simulated groups, based on the visual integration algorithms observed in VR at 7 dpf, showed an increase in group dispersion compared to the non-social model, which exhibited dispersion values that were at chance levels (Fig. 4c) These results capture well the behavior of groups of 7 dpf larvae swimming in the light and in the dark (Fig. 4c). The specific elements in this hypothesized model, e.g. units that represent integrated vertical occupancy and averaged horizontal occupancy in visual areas, excitation/inhibition of units in the contra/ipsilateral side in the hindbrain and even the emergence of additional modules over development can be readily tested, rejected or refined using whole-brain imaging and connectivity data from real fish[66,67]
Sign-in/Register to view highlights & summary Sign-in/Register to access full text options 
Free) 
Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have
Schedule a call
