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Abstract

The brain has persistent internal states that can modulate every aspect of an animal’smental experience. In complex tasks such as foraging, internal state is dynamic. C.elegans alternate between local search and global dispersal. Rodents and primates ex-hibit trade-offs between exploitation and exploration. However, fundamental questionsremain about how persistent states are maintained in the brain, which upstream net-works drive state transitions, and how state-encoding neurons exert neuromodulatoryeffects on sensory perception and decision making to govern appropriate behavior. Usingtracking microscopy in larval zebrafish, we can monitor whole brain neuronal activityat cellular resolution in a freely moving animal across spontaneous internal state transi-tions. We show that larval zebrafish alternate between two persistent behavioral statesduring foraging for live prey (paramecia). In the exploitation state, the animal inhibitslocomotion and promotes hunting, generating small localized trajectories. In the explo-ration state, the animal promotes locomotion and suppresses hunting, generating longranging trajectories that enhance spatial dispersion. We uncover a dorsal raphe sub-population with persistent activity that robustly encodes the exploitation state. Theexploitation state-encoding neurons, together with a multimodal trigger network thatis associated with state transitions, form a stochastically activated nonlinear dynamicalsystem. The activity of this oscillatory network correlates with a global re-tuning ofsensorimotor transformations during foraging that leads to dramatic changes in boththe 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 ofmotivation and decision making.