Stability of neural representations in the auditory midbrain across the lifespan despite age-related brainstem delays

Abstract

The extent to which aging of the central auditory pathway impairs auditory perception in the elderly independent of peripheral cochlear decline is debated. To cause auditory deficits in normal hearing elderly, central aging needs to degrade neural sound representations at some point along the auditory pathway. However, inaccessible to psychophysical methods, the level of the auditory pathway at which aging starts to effectively degrade neural sound representations remains poorly differentiated. Here we tested how potential age-related changes in the auditory brainstem affect the stability of spatiotemporal multiunit complex speech-like sound representations in the auditory midbrain of old normal hearing CBA/J mice. Although brainstem conduction speed slowed down in old mice, the change was limited to the sub-millisecond range and only minimally affected temporal processing in the midbrain (i.e. gaps-in-noise sensitivity). Importantly, besides the small delay, multiunit complex temporal sound representations in the auditory midbrain did not differ between young and old mice. This shows that although small age-related neural effects in simple sound parameters in the lower brainstem may be present in aging they do not effectively deteriorate complex neural population representations at the level of the auditory midbrain when peripheral hearing remains normal. This result challenges the widespread belief of pure central auditory decline as an automatic consequence of aging. However, the stability of midbrain processing in aging emphasizes the role of undetected 'hidden' peripheral damage and accumulating effects in higher cortical auditory-cognitive processing explaining perception deficits in 'normal hearing' elderly.