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Abstract

The motivational state of an animal sets its behavioral priorities and modulates its motor performance. In complex tasks such as foraging, internal state is dynamic, and behavior alternates between local search (exploitation) and global dispersal (exploration). It is unclear whether exploitation and exploration states are maintained by a specific set of master regulatory neurons or are emergent from large-scale population activity. Using tracking microscopy, we simultaneously imaged behavior and whole brain neural activity at cellular resolution in freely swimming zebrafish for hours during foraging behavior. We uncover a dorsal raphe subpopulation with persistent activity that encodes the exploitation state. The exploitation state-encoding neurons, together with a multimodal trigger network that is associated with state transitions, forms a stochastic nonlinear relaxation oscillator. The activity of this oscillatory network correlates with a global re-tuning of sensorimotor transformations during foraging that leads to dramatic changes in both the motivation to hunt for prey and the accuracy of motor sequences during hunting. This work reveals an important hidden variable that shapes the temporal structure of motivation and decision making.