Inverse Control of Turning Behavior by Dopamine D1 Receptor Signaling in Columnar and Ring Neurons of the Central Complex in Drosophila

Action selection is a prerequisite for decision-making and a fundamental aspect to any goal-directed locomotion; it requires integration of sensory signals and internal states to translate them into action sequences. Here, we introduce a novel behavioral analysis to study neural circuits and mechanisms underlying action selection and decision-making in freely moving Drosophila. We discovered preferred patterns of motor activity and turning behavior. These patterns are impaired in FoxP mutant flies, which present an altered temporal organization of motor actions and turning behavior, reminiscent of indecisiveness. Then, focusing on central complex (CX) circuits known to integrate different sensory modalities and controlling premotor regions, we show that action sequences and turning behavior are regulated by dopamine D1-like receptor (Dop1R1) signaling. Dop1R1 inputs onto CX columnar ellipsoid body-protocerebral bridge gall (E-PG) neuron and ellipsoid body (EB) R2/R4m ring neuron circuits both negatively gate motor activity but inversely control turning behavior. Although flies deficient of D1 receptor signaling present normal turning behavior despite decreased activity, restoring Dop1R1 level in R2/R4m-specific circuitry affects the temporal organization of motor actions and turning. We finally show EB R2/R4m neurons are in contact with E-PG neurons that are thought to encode body orientation and heading direction of the fly. These findings suggest that Dop1R1 signaling in E-PG and EB R2/4 m circuits are compared against each other, thereby modulating patterns of activity and turning behavior for goal-directed locomotion. •Freely moving Drosophila present preferred patterns of activity and turning behavior•FoxP mutations affect temporal distribution of motor actions and turning behavior•Central complex columnar E-PG and R2/4 m ring neurons inversely regulate turning•Dopamine D1-like receptor signaling in R2/R4m ring neurons modulates behavior Kottler et al. use a novel behavioral paradigm to show that dopamine D1-like receptor Dop1R1 signaling in columnar E-PG and ellipsoid body R2/R4m ring neurons mediate temporal patterns of activity and inversely control turning, suggesting that Dop1R1 levels between interconnected central complex circuitry modulate behavioral performance in flies.