Like many adaptive behaviors, acoustic communication often requires rapid modification of motor output in response to sensory cues. However, little is known about the sensorimotor transformations that underlie such complex natural behaviors. In this study, we examine vocal exchanges in Alston’s singing mouse (Scotinomys teguina). We find that males modify singing behavior during social interactions on a subsecond time course that resembles both traditional sensorimotor tasks and conversational speech. We identify an orofacial motor cortical region and, via a series of perturbation experiments, demonstrate a hierarchical control of vocal production, with the motor cortex influencing the pacing of singing behavior on a moment-by-moment basis, enabling precise vocal interactions. These results suggest a systems-level framework for understanding the sensorimotor transformations that underlie natural social interactions.

To navigate towards a food source, animals frequently combine odor cues about source identity with wind direction cues about source location. Where and how these two cues are integrated to support navigation is unclear. Here we describe a pathway to the Drosophila fan-shaped body that encodes attractive odor and promotes upwind navigation. We show that neurons throughout this pathway encode odor, but not wind direction. Using connectomics, we identify fan-shaped body local neurons called h∆C that receive input from this odor pathway and a previously described wind pathway. We show that h∆C neurons exhibit odor-gated, wind direction-tuned activity, that sparse activation of h∆C neurons promotes navigation in a reproducible direction, and that h∆C activity is required for persistent upwind orientation during odor. Based on connectome data, we develop a computational model showing how h∆C activity can promote navigation towards a goal such as an upwind odor source. Our results suggest that odor and wind cues are processed by separate pathways and integrated within the fan-shaped body to support goal-directed navigation.

Highlights d Walking flies require both antennae for robust olfactory navigation behavior d The difference between antennal displacements generates a linear code for wind direction d Second-order APN neurons encode ipsilateral antenna deflections d Higher-order WPNs encode wind direction by integrating information from the two antennae