Emergent Behavior in a Dish: Discovery of Bi-directional Spiraling as a Population Phenomenon in C. elegans Enables In-Depth Dissection of Mechanisms Underlying Group Behaviors

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Project Summary/Abstract Emergent behaviors arise when individuals follow rules about how to interact with one another and their environment to produce a group entity with new properties or abilities1,2. Common examples include a school of fish, a flock of birds, and a colony of ants. In an emergent behavior, individuals often simultaneously communicate with multiple other individuals while processing sensory cues from the environment2,3. All this information is integrated to produce a behavioral response that is remarkably cohesive across the group. Though complex information integration is a hallmark of how humans process the world, the mechanisms underlying communication in groups have been difficult to probe experimentally. I have discovered the first example of emergent group behavior in C. elegans in which individuals coordinate motion without being in physical contact: in response to a simple environmental cue, a population of several hundred individuals will synchronously perform an inward bidirectional spiral that eventually concentrates the initially dispersed population at a central point. The behavior occurs when a lid is placed on an open dish containing a sufficient density of worms in the absence of food and is dependent on intact sensory systems. Furthermore, I have demonstrated that a cue from a high density population can be sensed across a shared airspace to induce spiral-like behavior in individual worms that would not otherwise show spiral motion. I therefore propose that C. elegans uses a volatile cue to gauge population density, and spiraling behavior is triggered by concentration of this cue when the dish is closed. However, I also demonstrate that accumulation of a cue is not sufficient to induce spiraling if inter-worm distance is too great indicating that local cues between neighboring worms are also involved in coordinating spiraling. In Aim 1, I will elucidate the cues that individuals produce and perceive to facilitate emergent spiraling in C. elegans including both long-range density cues and short-range cues from nearby individuals. In Aim 2, I will take advantage of the tractability of C. elegans to ask how brain activity produces emergent spiraling behavior. C. elegans are transparent, and the brain activity of individuals can be directly visualized by following calcium transients in freely moving worms4. I will explore the hypothesis that neural networks reduce the noise of inputs to produce maximally coherent behavior across individuals in the collective. Together these findings will illuminate principles underlying emergent behavior at unprecedented resolution which may allow us to identify similar processes occurring in other systems or design artificial systems which exhibit spiral behavior.