Abstract

Accurate sound localization requires normal binaural input and precise auditory neuronal representation of sound spatial locations. Previous studies showed that unilateral hearing loss profoundly impaired the sound localization abilities. However, the underlying neural mechanism is not fully understood. Here, we investigated how chronic unilateral conductive hearing loss (UCHL) affected the neural tuning to sound source azimuth in the primary auditory cortex (AI). The UCHL was manipulated by the removal of tympanic membrane and malleus in the right ear of young (P14) rats and adult (P57) rats. We recorded the azimuth tuning of neurons in the left AI contralateral to the operated ear in the two groups of rats that experienced 2 months of UCHL, and in the left AI of age-matched control rats. We found that AI neurons in control rats showed predominant preference to sound from contralateral azimuths. However, UCHL weakened the cortical neuronal representation of contralateral azimuths on the operated ear side and strengthened the cortical neuronal representation of ipsilateral azimuths on the intact ear side. This effect was stronger in rats with UCHL at young age than in rats with UCHL in adulthood. Moreover, UCHL degraded the azimuth selectivity and azimuth sensitivity of AI neurons, and this effect was stronger in rats with UCHL in adulthood than in rats with UCHL at young age. These findings highlight a remarkable age-related experience-dependent plasticity of neural tuning to sound source azimuth in AI, and imply a neural mechanism for the impacts of chronic UCHL on sound localization abilities.

Highlights

  • The ability to accurately localize and segregate different sound sources is a fundamental acoustical process for human and animals in analyzing signal sounds, monitoring acoustical environment, and guiding subsequent behavioral responses

  • The data of the azimuth functions from 278 neurons were obtained in the auditory cortex (AI) of the four groups of rats, including 78 neurons in the young control (YCon) group, 73 neurons in the young unilateral conductive hearing loss (YUCHL) group, 61 neurons in the adult control (ACon) group, and 66 neurons in the adult unilateral conductive hearing loss (AUCHL) group

  • The characteristic frequency (CF) ranges of these AI neurons were 4.0–44.0 kHz in the YCon group, 5.0–41.0 kHz in the YUCHL group, 8.0–41.0 kHz in the ACon group, and 4.2–35.0 kHz in the AUCHL group

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Summary

Introduction

The ability to accurately localize and segregate different sound sources is a fundamental acoustical process for human and animals in analyzing signal sounds, monitoring acoustical environment, and guiding subsequent behavioral responses. Most of the neurons in AI preferred sound stimuli from the contralateral field, and only a small proportion of neurons preferred the sound stimuli from midline or ipsilateral field This has been demonstrated in cats (Imig et al, 1990; Rajan et al, 1990; Barone et al, 1996; Eggermont and Mossop, 1998), rats (Yao et al, 2013; Gao et al, 2018), and monkeys (Woods et al, 2006). Studies showed that many azimuth-sensitive neurons in the AI of adult cats determined in binaural conditions immediately became insensitive to sound source azimuth when determined with one ear plugged (Samson et al, 1994), demonstrating the importance of normal binaural input in the spatial sensitivity of AI neurons

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