Spectral cues are necessary to encode azimuthal auditory space in the mouse superior colliculus

Shinya Ito,Alan M Litke,Yufei Si,David A Feldheim

doi:10.1038/s41467-020-14897-7

Shinya Ito, Alan M Litke + Show 2 more

Open Access

https://doi.org/10.1038/s41467-020-14897-7

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Journal: Nature Communications	Publication Date: Feb 27, 2020
Citations: 20	License type: open-access

Affiliation: University of California, Santa Cruz

Abstract

Sound localization plays a critical role in animal survival. Three cues can be used to compute sound direction: interaural timing differences (ITDs), interaural level differences (ILDs) and the direction-dependent spectral filtering by the head and pinnae (spectral cues). Little is known about how spectral cues contribute to the neural encoding of auditory space. Here we report on auditory space encoding in the mouse superior colliculus (SC). We show that the mouse SC contains neurons with spatially-restricted receptive fields (RFs) that form an azimuthal topographic map. We found that frontal RFs require spectral cues and lateral RFs require ILDs. The neurons with frontal RFs have frequency tunings that match the spectral structure of the specific head and pinna filter for sound coming from the front. These results demonstrate that patterned spectral cues in combination with ILDs give rise to the topographic map of azimuthal auditory space.

Highlights

Sound localization plays a critical role in animal survival
We found that the mouse superior colliculus (SC) contains a topographic map of auditory space along the azimuthal axis; spectral cues and interaural level differences (ILDs) are used to compute localized auditory receptive fields (RFs), but interaural timing differences (ITDs) are not; the relative importance of spectral cues and ILDs depends on the azimuthal position of the RF; and the spectral tuning properties of neurons with frontal RFs match well with the spectral structure of the frontal head-related transfer functions (HRTFs)
We first measured a set of HRTFs, the modulation of sound by the physical structure of the head and pinnae, that contains each of the three sound localization cues: ITDs, ILDs, and spectral cues (Supplementary Fig. 1)

Summary

Introduction

Sound localization plays a critical role in animal survival. Three cues can be used to compute sound direction: interaural timing differences (ITDs), interaural level differences (ILDs) and the direction-dependent spectral filtering by the head and pinnae (spectral cues). We found that frontal RFs require spectral cues and lateral RFs require ILDs. The neurons with frontal RFs have frequency tunings that match the spectral structure of the specific head and pinna filter for sound coming from the front. The neurons with frontal RFs have frequency tunings that match the spectral structure of the specific head and pinna filter for sound coming from the front These results demonstrate that patterned spectral cues in combination with ILDs give rise to the topographic map of azimuthal auditory space. Unlike vision or touch, where the receptor position along the sensory detector encodes spatial information, the incident direction of the sound source must be computed This calculation is based on three cues: interaural timing differences (ITDs), interaural level differences (ILDs), and the spectral modification of the sound as it enters the ear (spectral cues). These results demonstrate an unexpectedly important role for spectral cues in the formation of the azimuthal sound map, lending new insights into how mice perform sound localization

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