Spatially clustered neurons encode vocalization categories in the bat midbrain

Rapid categorization of vocalizations enables adaptive behavior across species. While categorical perception is thought to arise in the neocortex, humans and other animals could benefit from functional organization of ethologically-relevant sounds at earlier stages in the auditory hierarchy. Here, we developed two-photon calcium imaging in the awake echolocating bat (Eptesicus fuscus) to study encoding of sound meaning in the Inferior Colliculus, which is as few as two synapses from the inner ear. Echolocating bats produce and interpret frequency sweep-based vocalizations for social communication and navigation. Auditory playback experiments demonstrated that individual neurons responded selectively to social or navigation calls, enabling robust population-level decoding across categories. Strikingly, category-selective neurons formed spatial clusters, independent of tonotopy within the IC. These findings support a revised view of categorical processing in which specified channels for ethologically-relevant sounds are spatially segregated early in the auditory hierarchy, enabling rapid subcortical organization of call meaning.