A dopamine circuit regulates locomotor initiation and persistence in Drosophila

Decisions to initiate or terminate locomotion reflect the commitment of an animal to expend energy and thus must be appropriately regulated. Dopaminergic system has been implicated in locomotor regulation but how it controls these decisions remains unclear. Here we show that a dopamine circuit in Drosophila mushroom body regulates cue-induced locomotor initiation and termination by integrating locomotor history and current motivation. This circuit consists of the locomotor-initiator mushroom body output neurons, MBON09, and the locomotor-terminator MBON21. Previous locomotor initiation by default suppresses the propensity of future initiation through depression of MBON09 activity by locomotion-sensitive dopamine afferents, preventing redundant action. Locomotor persistence is promoted through combined inhibition of MBON21 by MBON09 and by distinct dopamine afferents that receive fluctuating motivational signals. Persistent locomotion under high motivational state, in turn, causes dopamine-dependent MBON09 facilitation, reinvigorating locomotor initiation program. Our results revealed a dopaminergic mechanism to transform recent behavior and current motivation into a moment-by-moment internal state that in turn regulates locomotor decisions.