Spatially clustered neurons in the bat midbrain encode vocalization categories

Abstract

Rapid categorization of vocalizations enables adaptive behavior across species. While categorical perception is thought to arise in the neocortex, humans and animals could benefit from a functional organization tailored to ethologically relevant sound processing earlier in the auditory pathway. Here we developed two-photon calcium imaging in the awake echolocating bat (Eptesicus fuscus) to study the representation of vocalizations in the inferior colliculus, which is as few as two synapses from the inner ear. Echolocating bats rely on 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. When social calls were morphed into navigation calls in equidistant step-wise increments, individual neurons showed switch-like properties and population-level response patterns sharply transitioned at the category boundary. Strikingly, category-selective neurons formed spatial clusters, independent of tonotopy within the dorsal cortex of the inferior colliculus. 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 into categorical primitives.