Source identity shapes spatial preference in primary auditory cortex during active navigation

Abstract

Localizing and identifying sensory objects while navigating the environment are fundamental brain functions. However, how individual objects are neuronally represented during unrestricted self-motion is mostly unexplored. We trained gerbils on a behavioral foraging paradigm that required localization and identification of sound-sources during free navigation. Chronic multi-electrode recordings in primary auditory cortex during task performance revealed previously unreported sensory object representations. Strikingly, the egocentric angle preference of the majority of spatially sensitive neurons changed significantly depending on the task-specific identity (outcome association) of the sound-source. Spatial tuning also exhibited larger temporal complexity. Moreover, we encountered egocentrically untuned neurons whose response magnitude differed between source identities. Using a neural network decoder we show that together, these neuronal response ensembles provide spatio-temporally co-existent information about both the egocentric location and the identity of individual sensory objects during self-motion, revealing a novel cortical computation principle for naturalistic sensing. HighlightsO_LILocalization task during free navigation prompts diverse spatial tuning in gerbil A1 C_LIO_LISpatial preference of individual neurons changes with sound-source identity C_LIO_LIEgo- and allocentric information are spatio-temporally coexistent in A1 ensembles C_LIO_LIActive sensing reveals new cortical representations for sensory object identification C_LI