Cerebellar activity predicts vocalization in fruit bats

Abstract

Echolocating bats exhibit remarkable auditory behaviors, enabled by adaptations both within and outside their auditory system. Yet research on echolocating bats has focused mostly on brain areas that belong to the classic ascending auditory pathway. This study provides direct evidence linking the cerebellum, an evolutionarily ancient and non-classic auditory structure, to vocalization and hearing. We report that in the fruit-eating bat Carollia perspicillata, external sounds can evoke cerebellar responses with latencies below 20 ms. Such fast responses are indicative of early inputs to the bat cerebellum. After establishing fruit-eating bats as a good model to study cerebellar auditory responses, we searched for a neural correlate of vocal production within the cerebellum. We investigated spike trains and field potentials occurring before and after vocalization and found that the type of sound produced (echolocation pulses or communication calls) can be decoded from pre-vocal and post-vocal neural signals, with prediction accuracies that reach above 85%. The latter provides a direct correlate of vocalization in an ancient motor-coordination structure that lies outside of the classic ascending auditory pathway. Taken together, our findings provide evidence of specializations for vocalization and hearing in the cerebellum of an auditory specialist.