Phonotactic steering and representation of directional information in the ascending auditory pathway of a cricket

Abstract

Directional hearing is crucial for animals depending on acoustic signals to locate a mate. We focused on crickets to explore the reliability of directional information forwarded to the brain by the ascending auditory interneuron AN1, which is crucial for phonotactic behavior. We presented calling song from −45° to +45° in steps of 3° and compared the phonotactic steering of females walking on a trackball with the directional responses of AN1. Forty percent of females showed good steering behavior and changed their walking direction when the speaker passed the body’s longitudinal axis. The bilateral latency difference between right and left AN1 responses was small and may not be reliable for auditory steering. In respect to spike count, all AN1 recordings presented significant bilateral differences for angles larger than ±18°, yet 35% showed a mean significant difference of 1–3 action potentials per chirp when the frontal stimulus deviated by 3° from their length axis. For small angles, some females had a very similar AN1 activity forwarded to the brain, but the accuracy of their steering behavior was substantially different. Our results indicate a correlation between directional steering and the response strength of AN1, especially for large angles. The reliable steering of animals at small angles would have to be based on small bilateral differences of AN1 activity, if AN1 is the only source providing directional information. We discuss whether such bilateral response difference at small angles can provide a reliable measure to generate auditory steering commands descending from the brain, as pattern recognition is intensity independent. NEW & NOTEWORTHY The ascending auditory interneuron AN1 has been implicated in cricket auditory steering, but at small acoustic stimulation angles, it does not provide reliable directional information. We conclude that either the small bilateral auditory activity differences of the AN1 neurons are enhanced to generate reliable descending steering commands or, more likely, directional auditory steering is mediated via a thoracic pathway, as indicated by the reactive steering hypothesis.