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

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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.

Research highlights

▶ Environmental noise can delay temporal processing acuity development. ▶ Environmental noise increased NMDA-R2B protein expression in the auditory cortex. ▶ Noise affects auditory cortex maturation and thus affects auditory temporal processing. ▶ Noise shows no effect on temporal processing in adult rats. ▶ There exists a critical period for the functional development of temporal processing acuity.

Introduction

During normal development neurons in the mammalian auditory cortex (AC) undergo a progressive refinement of their excitatory response properties [1], [2] which coincides with a maturation of inhibitory neurotransmission [3], [4], [5]. In addition, normal development is marked by a reduction in the degree to which AC neurons demonstrate experience-dependent synaptic plasticity [6]. This greater resistance to plasticity in the adult brain may result from age-related changes in the relative expression of different subunits of N-methyl-d-aspartate (NMDA) receptors (e.g., NR2A and NR2B) [7]. Juvenile brains have a relatively greater level of NR2B subunit expression [8], which is thought to facilitate plasticity and long-term potentiation (LTP) induction [9].

It is well established that brief exposure to intense noise during early development can result in impaired neural processing in the central auditory system in adulthood [10], [11], [12], and that the normal maturation of the AC can be dramatically delayed by prolonged exposure to an abnormal sound environment during the formative developmental epoch, termed the critical period [1], [6], [13]. For example, rearing rats, whose critical period normally extends ∼50 days after birth, in environmental noise (i.e., continuous, moderate-level, white noise) results in poor spatial tuning in AC neurons [14], as well as an overall lack of tonotopic refinement [13] and enhancement of NR2B-dependent LTP in the AC [9]. Furthermore, young rats exposed to moderate-level interrupted white noise for 8 h/day for 2 weeks during their critical period showed impaired sound level processing in AC neurons [15] and deficits in sound localization behavior as adults [16]. Ultimately, it has been suggested that environmental noise may contribute to language-related developmental delays in children [13].

Language processing requires the central auditory system to detect rapid changes of speech sounds in temporal and spectral domains [17], [18]. Proper maturation of a child's temporal processing ability is essential for their speech comprehension and language development [19], [20]. In both humans and laboratory animals, temporal processing acuity can be monitored with a behavioral assessment of the subject's ability to detect short gaps in sound [21]. Under normal developmental conditions, temporal processing acuity improves such that the gap detection threshold in adults is shorter than that for infants (5.2 ms vs. 11 ms, respectively) [22]. At present, it is uncertain whether this normal age-related improvement in temporal processing acuity is sensitive to delayed development of the AC.

In the present study, we investigated the effect of environmental noise on (1) the maturation of temporal processing acuity in rats, and (2) the protein expression of NMDA receptor subunits (NR2A and NR2B) in their AC. We used a behavioral paradigm, the gap-induced prepulse inhibition of the acoustic startle reflex (Gap-PPI), to assess the gap detection threshold [23], and provide a comparison of temporal processing acuity between environmental noise-reared rats and controls. In addition, using standard laboratory techniques described in our recent study [24], we compared the level of NR2A and NR2B subunit protein expression in the AC between groups. Because the absence of normal sound input during early life retards the functional development of the AC [1], [9], [13], we hypothesized that environmental noise-rearing would delay the normal maturation of temporal processing acuity (i.e., gap detection threshold would fail to decrease). Furthermore, based on a previous report [9], we expected the relative level of protein expression of NR2B in the AC to remain elevated in the environmental noise-reared rats, indicative of developmental arrest in an immature state.

Section snippets

Animals and noise environment

A total of 30 male Sprague–Dawley rats (Harlan) were used in this study. All experimental procedures were approved by the Institutional Animal Care and Use Committee (IACUC) of University at Buffalo, and conform to the guidelines issued by the National Institutes of Health. At postnatal day-7, rat pups and their breeding mothers were randomly assigned into one of two groups: an environmental noise-exposed group, or control group. For environmental noise-rearing, rat pups and their mother were

Behavioral testing of temporal processing acuity

To determine the effect of masking normal sound inputs on temporal processing acuity development, the Gap-PPI paradigm was performed on the environmental noise-exposed rats and age-matched controls. Compared to the control group, rats reared in the environmental noise showed much lower Gap-PPI% at 2 months old (P-2m, Fig. 2A, significant, two-way ANOVA, F(8, 45) = 15, P < 0.0001) and 3 months old (P-3m, Fig. 2B, significant, two-way ANOVA, F(9, 60) = 11.3, P < 0.0001), indicative of impaired temporal

Discussion

The present study provides an investigation of the effect of environmental noise-rearing (i.e., continuous, moderate-level, white noise) on (1) temporal processing acuity assessed behaviorally, and (2) NMDA receptor subunit (NR2A and NR2B) protein expression in the AC. As hypothesized, rats exposed to environmental noise during early postnatal life (from 7 days to 2 or 3 months old) showed poor temporal processing acuity as adults (i.e., gap detection threshold remained elevated at a

Acknowledgements

We thank Drs. Ison and Allen from the University at Rochester for generously sharing the custom software for acoustic startle reflex testing. This project is supported by grants from National Institute of Health (R03 DC008685-03) and National Organization for Hearing Research.

References (31)

  • E. de Villers-Sidani et al.

    Critical period window for spectral tuning defined in the primary auditory cortex (A1) in the rat

    J Neurosci

    (2007)
  • V.C. Kotak et al.

    Hearing loss prevents the maturation of GABAergic transmission in the auditory cortex

    Cereb Cortex

    (2008)
  • A.E. Takesian et al.

    Presynaptic GABA(B) receptors regulate experience-dependent development of inhibitory short-term plasticity

    J Neurosci

    (2010)
  • A.L. Dorrn et al.

    Developmental sensory experience balances cortical excitation and inhibition

    Nature

    (2010)
  • Y. Cui et al.

    Early auditory experience-induced composition/ratio changes of N-methyl-d-aspartate receptor subunit expression and effects of d-2-amino-5-phosphonovaleric acid chronic blockade in rat auditory cortex

    J Neurosci Res

    (2009)
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