Evidence of Hyperacusis in Adult Rats Following Non-traumatic Sound Exposure.

Maryse E Thomas,Kristina M Drudik,Gerson D Guercio,Étienne De Villers-Sidani

doi:10.3389/fnsys.2019.00055

Abstract

Manipulations that enhance neuroplasticity may inadvertently create opportunities for maladaptation. We have previously used passive exposures to non-traumatic white noise to open windows of plasticity in the adult rat auditory cortex and induce frequency-specific functional reorganizations of the tonotopic map. However, similar reorganizations in the central auditory pathway are thought to contribute to the generation of hearing disorders such as tinnitus and hyperacusis. Here, we investigate whether noise-induced reorganizations are accompanied by electrophysiological or behavioral evidence of tinnitus or hyperacusis in adult Long-Evans rats. We used a 2-week passive exposure to moderate-intensity (70 dB SPL) broadband white noise to reopen a critical period for spectral tuning such that a second 1-week exposure to 7 kHz tone pips produced an expansion of the 7 kHz frequency region in the primary auditory cortex (A1). We demonstrate for the first time that this expansion also takes place in the ventral auditory field (VAF). Sound exposure also led to spontaneous and sound-evoked hyperactivity in the anterior auditory field (AAF). Rats were assessed for behavioral evidence of tinnitus or hyperacusis using gap and tone prepulse inhibition of the acoustic startle response. We found that sound exposure did not affect gap-prepulse inhibition. However, sound exposure led to an improvement in prepulse inhibition when the prepulse was a 7 kHz tone, showing that exposed rats had enhanced sensorimotor gating for the exposure frequency. Together, our electrophysiological and behavioral results provide evidence of hyperacusis but not tinnitus in sound-exposed animals. Our findings demonstrate that periods of prolonged noise exposure may open windows of plasticity that can also be understood as windows of vulnerability, potentially increasing the likelihood for maladaptive plasticity to take place.

Highlights

As recent decades of neuroscience research have revealed the brain’s lifelong capacity for plastic change (Hofer et al, 2006; de Villers-Sidani and Merzenich, 2011), the goal of reopening critical periods (CPs) in order to stimulate learning and recovery in adulthood has become an important area of study
We documented the effects of 2 weeks of passive exposure to white noise followed by 1 week of 7 kHz tone pip exposure on electrophysiological response properties in 13 rats (Exposed Group) and compared them to 11 rats that were housed in a standard acoustic environment (Naïve Group; Figure 1A)
Responsive sites were classified as belonging to A1, anterior auditory field (AAF), ventral auditory field (VAF), or posterior auditory field (PAF) based on the published functional characteristics of each field (Polley et al, 2007; Profant et al, 2013), reversal of tonotopic gradients, onset latencies, threshold, and peri-stimulus time histograms (PSTHs) morphologies (Supplementary Figure S1)

Summary

Introduction

As recent decades of neuroscience research have revealed the brain’s lifelong capacity for plastic change (Hofer et al, 2006; de Villers-Sidani and Merzenich, 2011), the goal of reopening critical periods (CPs) in order to stimulate learning and recovery in adulthood has become an important area of study. The inevitable quest for lifelong adaptability, should not be undertaken without considering the potential risks of opening windows of vulnerability on the brain One such vulnerability is the opportunity for maladaptive plasticity, which refers to structural or functional nervous system changes that disrupt normal function. In the central auditory system, maladaptive plasticity is thought to underlie the generation of auditory disorders including chronic tinnitus and hyperacusis, the uncomfortable sensations of ringing in the ears and sound hypersensitivity. These potentially debilitating conditions usually emerge late in life comorbid with hearing loss and affect between 6% to 15% of the general population (Brozoski and Bauer, 2016). Some evidence links spontaneous and sound-evoked hyperactivity to tinnitus or hyperacusis in humans (Adjamian et al, 2009; Gu et al, 2010), but neuroimaging studies have yet to demonstrate macroscopic tonotopic reorganization in patients with tinnitus (Langers et al, 2012; Elgoyhen et al, 2015), illustrating that much remains to be understood in the etiology of both conditions

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