Sensory-evoked locomotion selectively enhances transient and sustained food odor representations in a mushroom body dopaminergic circuit in Drosophila.

Animals must continuously adapt their behavior to dynamic sensory environments and internal motor states. In Drosophila and other invertebrates, the mushroom body is key to this behavioral flexibility, with dopaminergic neurons (DANs) and mushroom body output neurons (MBONs) forming a core circuit for context-dependent action selection. Yet, how olfactory cues and locomotor states are jointly integrated and transformed across the DAN-MBON circuit is unclear. Using single- and dual-color two-photon calcium and dopamine imaging, we found distinct representations in the γ1 compartment. In response to prolonged food odor delivery, γ1 DANs exhibit transient responses tightly locked to odor onset and offset, whereas MBONs maintain a sustained response throughout odor delivery. Moreover, while spontaneous locomotion elicits faithful DAN calcium dynamics and dopamine release without clearly affecting MBONs, odor-evoked locomotion selectively amplifies the transient and sustained olfactory responses in DANs and MBONs, respectively, facilitating context-dependent olfactory-motor integration. Linear encoding models reveal that DANs broadly integrate diverse olfactory and locomotor variables, and exhibit higher variability than MBONs. We propose a model where dopaminergic transients serve as context-switch signals, integrating environmental and locomotor contexts to flexibly modulate sustained MBON output and guide behavior.