Shaping the aging brain: role of auditory input patterns in the emergence of auditory cortical impairments

Brishna Kamal,Etienne De Villers-Sidani,Constance Holman

doi:10.3389/fnsys.2013.00052

Abstract

Age-related impairments in the primary auditory cortex (A1) include poor tuning selectivity, neural desynchronization, and degraded responses to low-probability sounds. These changes have been largely attributed to reduced inhibition in the aged brain, and are thought to contribute to substantial hearing impairment in both humans and animals. Since many of these changes can be partially reversed with auditory training, it has been speculated that they might not be purely degenerative, but might rather represent negative plastic adjustments to noisy or distorted auditory signals reaching the brain. To test this hypothesis, we examined the impact of exposing young adult rats to 8 weeks of low-grade broadband noise on several aspects of A1 function and structure. We then characterized the same A1 elements in aging rats for comparison. We found that the impact of noise exposure on A1 tuning selectivity, temporal processing of auditory signal and responses to oddball tones was almost indistinguishable from the effect of natural aging. Moreover, noise exposure resulted in a reduction in the population of parvalbumin inhibitory interneurons and cortical myelin as previously documented in the aged group. Most of these changes reversed after returning the rats to a quiet environment. These results support the hypothesis that age-related changes in A1 have a strong activity-dependent component and indicate that the presence or absence of clear auditory input patterns might be a key factor in sustaining adult A1 function.

Highlights

Perceptual decline represents a universal component of the aging process across species, yet remains a poorly understood phenomenon
Noise exposure caused a significant receptive fields (RF) broadening, as measured with BW10 of neurons across the frequency spectrum (18% increase in BW10 compared to young naïve, p = 0.02–0.04, Figure 1C), with neurons tuned to low frequencies being slightly more affected
Based on the results of our experiments, it appears that a prolonged masking of auditory input patterns with low-grade noise may be sufficient to cause numerous alterations in A1 normally associated with aging, such as tonotopic re-organization of A1 previously demonstrated by Zheng (2012) in a similar paradigm with younger animals

Summary

Introduction

Perceptual decline represents a universal component of the aging process across species, yet remains a poorly understood phenomenon. For example, deficits in auditory processing have been linked to reduced inhibitory signaling (Seidman et al, 2002; Caspary et al, 2005), GABAergic transmission (Ling et al, 2005; Burianova et al, 2009), and parvalbumin positive (PV+) neurons (Ouda et al, 2008; Del Campo et al, 2012), and myelin (de Villers-Sidani et al, 2010; Tremblay et al, 2012). A recent upswing in research on cognitive training as therapy for age-related deficits has shown that many of these changes are reversible via targeted training paradigms (de VillersSidani et al, 2010). The plastic nature of this inhibitory signaling, is unlikely to be the fundamental mechanism underlying age-related cognitive decline, and instead could represent a side effect of other complex neurological processes

Methods

Results

Conclusion