Environmental noise affects auditory temporal processing development and NMDA-2B receptor expression in auditory cortex

Abstract

Auditory temporal processing is essential for sound discrimination and speech comprehension. Under normal developmental conditions, temporal processing acuity improves with age. As recent animal studies have shown that the functional development of the auditory cortex (AC) is impaired by early life exposure to environmental noise (i.e., continuous, moderate-level, white noise), here we investigated whether the normal age-related improvement in temporal processing acuity is sensitive to delayed development of the AC. We used a behavioral paradigm, the gap-induced prepulse inhibition of the acoustic startle reflex, to assess the gap detection threshold, and provide a comparison of temporal processing acuity between environmental noise-reared rats and age-matched controls. Moreover, because age-related changes normally occur in the relative expression of different N-methyl-D-aspartate (NMDA) receptor subunits, we assessed the level of protein expression of NMDA-2A and 2B receptors (NR2A and NR2B respectively) in the AC after environmental noise-rearing. As hypothesized, rats reared in environmental noise showed 1) poor temporal processing acuity as adults (i.e., gap detection threshold remained elevated at a juvenile-like level), and 2) an increased level of NR2B protein expression compared to age-matched controls. This poor temporal processing acuity represented delayed development rather than permanent impairment, as moving these environmental noise-reared rats to normal acoustic conditions improved their gap detection threshold to an age-appropriate level. Furthermore, housing normally-reared, adult rats in environmental noise for two months did not affect their already-mature gap detection threshold. Thus, masking normal sound inputs with environmental noise during early life, but not adulthood, impairs temporal processing acuity as assessed with the gap detection threshold.

A Behavioral Framework to Guide Research on Central Auditory Development and Plasticity

“…As adults, these animals actually display poor discrimination at the exposed frequency, yet their discrimination of adjacent frequencies is significantly better than controls (Han et al, 2007). In contrast, when young animals are exposed to noise for days or weeks, behavioral measures typically reveal diminished or delayed capacities (Philbin et al, 1994; Zhang et al, 2008; Zhou and Merzenich, 2009; Sun et al, 2011). Because the tone or noise levels used in these experiments appear to be too low to injure the cochlea, the behavioral impact is likely attributable to central changes (below).…”

Hyperexcitability of inferior colliculus neurons caused by acute noise exposure

“…The physiological function of the IC is largely affected by the excitatory and inhibitory signals mediated by glutamatergic and GABAergic projections. Lack of GABAergic inhibition in the IC is involved in different auditory disorders, including tinnitus, hyperacusis (Brozoski et al, 2007; Dong et al, 2010), and audiogenic seizure (Sun et al, 2011). Previous studies have indicated that a restricted lesion in the cochlea can cause a substantial reduction in GABAergic inhibition within the IC, which may cause increased responsiveness of neurons at the nondamaged frequencies (Gerken, 1996; Felix and Portfors, 2007).…”

The effect of noise exposure during the developmental period on the function of the auditory system

“…Importantly, the degraded spatial hearing could be restored by additional behavioral training. In the work of Sun et al (2011), adult rats reared in environmental noise (starting from P7) exhibited a degraded temporal processing acuity compared to controls. However, in this case, the poorer temporal processing acuity represented not a permanent impairment, but rather a delayed development, as placing the noise-reared animals in normal housing conditions improved their gap detection threshold to a normal level.…”

“…It appears that even a short-time detachment of the developing auditory system from natural and rich auditory experience, resulting from an impaired periphery or anomalous stimulation such as noise or clicks, will often result in altered structural and functional characteristics at various levels of the auditory system. These changes may comprise, for example, a decrease in the number of hair cells and their ribbon synapses Shi et al, 2015), abnormal dendritic trees and cell sizes of neurons in the central auditory system (Gabriele et al, 2000;Ouda et al, 2014;Lu et al, 2014), altered neuronal responsiveness and representation of stimulus frequency and intensity (e.g., Zhang et al, 2001;Gr ecov a et al, 2009;Bure s et al, 2010;Insanally et al, 2010), or deteriorated psychophysical, behavioral and cognitive functions (Rybalko et al, 2011;Sun et al, 2011;Pan et al, 2011;Rybalko et al, 2015;Suta et al, 2015;RuvalcabaDelgadillo et al, 2015). Despite this volume of work, there still exists great uncertainty as to what effect a specific intervention will have: different interventions may have different consequences at various levels of the auditory system, depending also on the type of intervention, stimulus type, exposure levels, or age of exposure (e.g., Sanes and Constantine-Paton, 1985;Zhang et al, 2001;Chang et al, 2005;Gr ecov a et al, 2009;Insanally et al, 2009;Miyakawa et al, 2013).…”