Characterization of auditory responsive neurons in the mouse superior colliculus to naturalistic sounds

Abstract

Locating the source of a specific sound in a complex environment and determining its saliency is critical for survival. The superior colliculus (SC), a sensorimotor midbrain structure, plays an important role in sound localization and has been shown to have a topographic map of the auditory space in a range of species. In mice, previous studies using broadband white noise stimuli found that neurons use high-frequency monaural spectral cues and interaural level differences (ILDs) to compute spatially restricted receptive fields (RFs), and that these RFs are organized topographically along the azimuth. However, in a naturalistic environment, the auditory stimuli that an animal encounters may have rich spectral components; however, these sound sources can still be localized efficiently. It remains unknown whether and how the SC neurons respond to naturalistic sounds and, in turn, compute a spatially restricted RF. Here, we show results from large-scale in vivo physiological recordings of SC neurons in response to white noise, naturalistic ultrasonic pup calls and chirps. We find that mouse SC auditory neurons respond to pup calls with distinct temporal patterns and a spatial preference predominantly at [~]60 degrees in contralateral azimuth. In addition, we categorized auditory SC neurons based on their spectrotemporal receptive field patterns and demonstrated that there are at least 4 distinct subtypes of auditory responsive SC neurons. Significance StatementThe superior colliculus (SC) receives visual and auditory information that is used to localize objects. While the organization and composition of visually responsive SC neurons is well described, much less is known about the types and response properties of auditory SC neurons. Here, we presented white noise, ultrasonic mouse pup calls, and chirp stimuli to mice while recording from SC neurons. Analysis of neuronal responses defines 4 distinct classes of auditory neurons. We also show that while auditory neurons respond to naturalistic stimuli, these responses mainly occur when presented from the side but not the front of the animal. These results lead to the hypothesis that mice use different strategies to localize sound depending on the spectral composition of the source.