The Mouse Inferior Colliculus Responds Preferentially to Non-Ultrasonic Vocalizations

Abstract

The inferior colliculus (IC), the midbrain auditory integration center, analyzes information about social vocalizations and provides substrates for higher level processing of vocal signals. We used multi-channel recordings to characterize and localize responses to social vocalizations and synthetic stimuli within the IC of female and male mice, both urethane-anesthetized and unanesthetized. We compared responses to ultrasonic vocalizations (USVs) with other vocalizations in the mouse repertoire and related vocal responses to frequency tuning, IC subdivisions, and sex. Responses to lower frequency, broadband social vocalizations were widespread in IC, well represented throughout the tonotopic axis, across subdivisions, and in both sexes. Responses to USVs were much more limited. Although we observed some differences in tonal and vocal responses by sex and subdivision, representations of vocal responses by sex and subdivision were largely the same. For most units, responses to vocal signals occurred only when frequency response areas overlapped with spectra of the vocal signals. Since tuning to frequencies contained within the highest frequency USVs is limited (< 15% of IC units), responses to these vocalizations are correspondingly limited (< 5% of sound-responsive units). These results highlight a paradox of USV processing in some rodents: although USVs are the most abundant social vocalization, their representation and the representation of corresponding frequencies is less than lower frequency social vocalizations. We interpret this paradox in light of observations suggesting that USVs with lower frequency elements (<50 kHz) are associated with increased emotional intensity and engage a larger population of neurons in the mouse auditory system. SIGNIFICANCE STATEMENTThe inferior colliculus (IC) integrates multiple inputs to analyze information about social vocalizations. In mice, we show that the most common type of social vocalization, the ultrasonic vocalization or USV, was poorly represented in IC compared to lower frequency vocalizations. For most neurons, responses to vocal signals occurred only when frequency response areas overlapped with vocalization spectra. These results highlight a paradox of USV processing in some rodent auditory systems: although USVs are the most abundant social vocalization, their representation and representation of corresponding frequencies is less than lower frequency social vocalizations. These results suggest that USVs with lower frequency elements (<50 kHz)--associated with increased emotional intensity--will engage a larger population of neurons in the mouse auditory system.