Pilifers provide rapid mechanosensory feedback during floral tracking in hawkmoths

Hawkmoths expertly hover over flowers during feeding, accurately tracking floral movements even as flowers gently sway in the wind. They use visual and mechanosensory feedback to adjust their position, while their long, flexible mouthpart, the proboscis, stays inserted inside the nectar spur. Although much is known about how hawkmoths detect and process visual motion, far less is understood about how hawkmoths detect mechanical motion cues. Pilifers are hair bundles at the proboscis-head joint, well-positioned to provide feedback about floral motion. Here, we tested if pilifers could provide mechanosensory feedback essential for successful floral tracking. We computed bending at the proboscis base during floral tracking in freely flying hawkmoths and found that floral movements induce small yet significantly correlated lateral bending. Recordings from pilifer afferents showed that they respond to lateral motions of amplitudes similar to those seen in natural floral tracking behaviors. They respond to different directions and speeds of proboscis motion with an average latency of 1.9 ms. Neural tracing revealed extensive sensory arborizations in the sub-esophageal ganglion of the brain and ventral nerve cord, indicating a feedback pathway to the neck and flight motor system that enables rapid coordination of appendages and body for successful feeding.