Clustered representation of vocalizations in the auditory midbrain of the echolocating bat

Categorical perception of sensory inputs, including human speech, enables adaptive behavior and is thought to emerge in the sensory cortex. There would be significant computational advantages, however, to functional specialization before cortical processing. To what extent do categorical representations emerge earlier in the auditory hierarchy? To address this, we reasoned that the ideal species would exhibit expert auditory sensing and a rich repertoire of vocalizations, akin to human listening and speech. The big brown bat, Eptesicus fuscus, stands out in the animal kingdom for its acoustic communication for self-navigation (through echolocation) and for social interactions (with conspecifics). Eptesicus fuscus move in three dimensions through their environment and must rapidly distinguish between vocalizations intended for navigation and those intended for social interaction. Here, we used two-photon calcium imaging in the awake big brown bat, to enable large-scale (7,868 neurons in three bats), spatially resolved recordings in the inferior colliculus (IC) during auditory playback. We discovered a novel, superficial tonotopy in the IC that was orthogonal to spatially clustered representations of social and navigation vocalizations. Population decoding revealed sharp boundaries across, but not within, these categories. Auditory models for perceptual categorization rely on the idea that the periphery and midbrain possess mostly a feedforward and filter-bank role. Our data support a revised view of categorical perception in which ethologically relevant sensory streams are spatially segregated early in the auditory hierarchy and provide parallel channels of organized information to downstream regions.