Unilateral Conductive Hearing Loss Disrupts the Developmental Refinement of Binaural Processing in the Rat Primary Auditory Cortex.

Jing Liu,Jiping Zhang,Xinyi Huang

doi:10.3389/fnins.2021.762337

Abstract

Binaural hearing is critically important for the perception of sound spatial locations. The primary auditory cortex (AI) has been demonstrated to be necessary for sound localization. However, after hearing onset, how the processing of binaural cues by AI neurons develops, and how the binaural processing of AI neurons is affected by reversible unilateral conductive hearing loss (RUCHL), are not fully elucidated. Here, we determined the binaural processing of AI neurons in four groups of rats: postnatal day (P) 14–18 rats, P19–30 rats, P57–70 adult rats, and RUCHL rats (P57–70) with RUCHL during P14–30. We recorded the responses of AI neurons to both monaural and binaural stimuli with variations in interaural level differences (ILDs) and average binaural levels. We found that the monaural response types, the binaural interaction types, and the distributions of the best ILDs of AI neurons in P14–18 rats are already adult-like. However, after hearing onset, there exist developmental refinements in the binaural processing of AI neurons, which are exhibited by the increase in the degree of binaural interaction, and the increase in the sensitivity and selectivity to ILDs. RUCHL during early hearing development affects monaural response types, decreases the degree of binaural interactions, and decreases both the selectivity and sensitivity to ILDs of AI neurons in adulthood. These new evidences help us to understand the refinements and plasticity in the binaural processing of AI neurons during hearing development, and might enhance our understanding in the neuronal mechanism of developmental changes in auditory spatial perception.

Highlights

The central auditory system receives, integrates, and analyses inputs from the two ears
We compared the data of auditory cortex (AI) neurons between the reversible UCHL (RUCHL) group (n = 138) and the adult group to investigate the effects of RUCHL at young age on the monaural response types and the binaural processing of AI neurons in adulthood
Whereas early age bilateral conductive hearing loss impairs sound loudness perception (Sun et al, 2011) and spatial memory (Zhao et al, 2018), unilateral conductive hearing loss (UCHL) during development impair performance on tasks such as sound localization and spatial release from masking that rely on binaural processing (Kumpik and King, 2019)

Summary

Introduction

The central auditory system receives, integrates, and analyses inputs from the two ears. This binaural processing contributes to localizing the sound source (Middlebrooks, 2015), separating the target sound from competing noisy background (Middlebrooks and Waters, 2020), and improving speech perception in noise (Hawley et al, 2004). The perception of acoustic space in humans exhibits developmental changes in sound localization accuracy and auditory spatial discrimination (Van Deun et al, 2009; Kuhnle et al, 2013), and it develops from an initially imprecise representation of spatial positions in infants and young children to a concise representation in young adults (Kuhnle et al, 2013; Freigang et al, 2015). The neural mechanism for the normal development of binaural processing is still not fully understood

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