Intermittent exposure with moderate-level sound impairs central auditory function of mature animals without concomitant hearing loss

https://doi.org/10.1016/j.heares.2009.12.025Get rights and content

Abstract

Long-term, passive, continuous exposure of mature animals to moderate-level, band-limited sounds can profoundly decrease neural activity in primary auditory cortex (AI) to sounds in the exposure frequency range, and increase activity to sounds outside the exposure range. The resulting reorganization of the AI tonotopic map resembles that following a restricted lesion of the cochlear epithelium. Here we show qualitatively similar effects of passive exposure when it is limited to 12 h/day, simulating a noisy-work/quiet-living environment, albeit at substantially lower intensity levels (68 dB SPL) than are considered harmful to hearing. Compared to continuous exposure at the same SPL and over a similar duration (6–12 weeks), this intermittent exposure produced a smaller decrease in AI spike and LFP (local field potential) activity in response to sound frequencies in the exposure range, and an increase in activity only for frequencies above the exposure range. As expected at these exposure levels, cortical changes occurred in the absence of concomitant hearing loss (i.e., absolute threshold shifts). Our results have implications for occupational noise exposure standards, which presently may not prevent changes in central auditory function that cannot be detected on the standard behavioral audiogram.

Introduction

The normal development of the brain can be delayed or even irreversibly altered by sensory deprivation or other manipulations of natural sensory environments, giving rise to the notion of “critical periods” (e.g., Hubel and Wiesel, 1970, Knudsen, 1985, Stanton and Harrison, 1996, Chang and Merzenich, 2003, Hooks and Chen, 2007). However, the mature brain is also susceptible to large-scale reorganization following long-term changes in the patterns of sensory input. In adult mammals, partial lesion of the cochlea (Robertson and Irvine, 1989), retina (Kaas et al., 1990) or hand (Merzenich et al., 1984) ultimately leads to the re-activation of the corresponding region of primary sensory cortex by inputs originating from the nearest functioning areas of sensory epithelium. Exposure of adult mammals to various experimental acoustic environments had been shown to affect stimulus representations in primary auditory cortex (AI) (e.g., Recanzone et al., 1993, Weinberger et al., 1993, Bao et al., 2003, Engineer et al., 2004, Polley et al., 2006), but always in conjunction with behavioral training or stimulation of the basal forebrain system (which is implicated in associative learning). However, we recently demonstrated that long-term (6–20 wk) passive exposure of adult cats to moderate-level (68–80 dB SPL), band-limited (4–20 kHz) tone pip ensembles could profoundly decrease AI responsiveness to sounds in the exposure frequency range, and increase responsiveness to sounds outside that range (Noreña et al., 2006, Pienkowski and Eggermont, 2009). The resulting reorganization of the AI tonotopic map resembled that following partial lesion of the cochlea, although no absolute threshold shifts could be detected either in the auditory periphery or central pathways. Following the cessation of exposure, these changes were slow to reverse, and the tonotopic map remained abnormal after up to 3 months of recovery in a quiet environment (Pienkowski and Eggermont, 2009).

Here we show qualitatively similar albeit weaker effects of long-term (6–12 wk), moderate-level (68 dB SPL) passive exposure when it was limited to 12 h/day (followed by 12 h of quiet). Our intent was to simulate the alteration of noisy-work/quiet-living environments, albeit at substantially lower intensity levels than are considered harmful to hearing (90 dBA for 8 h/day; OSHA, Standard 1926.52). We find that such acoustic environments can profoundly alter the sound frequency representation in AI without affecting hearing sensitivity.

Section snippets

Exposure stimulus

The exposure stimulus was the same as used previously (Noreña et al., 2006, Pienkowski and Eggermont, 2009). Briefly, it was constructed from a set of 50 ms-long gamma-shaped tone pips, with 38 frequencies logarithmically-spaced between 4 and 20 kHz. Each frequency was randomly and independently generated at a mean rate of 3 s−1, so that the average aggregate pip presentation rate was 114 s−1. The average A-weighted, linearly-integrated level, measured at various locations in the cat room ∼10 cm off

Sound exposure did not cause hearing loss due to cochlear trauma

As expected, the intermittent, moderate-level (68 dB SPL) sound exposure did not cause hearing loss. In no exposed cat did ABR thresholds exceed mean control values at any sound frequency (Fig. 1a). Threshold was determined using cat ABR wave IV (equivalent to wave V in humans), which effectively measures evoked potentials at the level of the lateral lemniscus. Since there were no threshold changes at the level of the generator of wave IV, there could be none at more peripheral stations.

Discussion

We have shown that long-term, intermittent exposure to band-limited, moderate-level tone pip ensembles leads to a reorganization of frequency tuning in AI and presumably in thalamus, given the similarity of the spike and LFP data. Changes induced by continuous exposure to the same frequency band and level were reversible (at least in part) after a relatively long period (12 weeks) of quiet recovery (Pienkowski and Eggermont, 2009). Since there is some overlap in the amount of change in neural

References (36)

  • C.D. Condon et al.

    Habituation produces frequency-specific plasticity of receptive fields in the auditory cortex

    Behav. Neurosci.

    (1991)
  • 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)
  • E. de Villers-Sidani et al.

    Manipulating critical period closure across different sectors of the primary auditory cortex

    Nat. Neurosci.

    (2008)
  • J.J. Eggermont

    The Correlative Brain; Theory and Experiment in Neural Interaction

    (1990)
  • N.D. Engineer et al.

    Environmental enrichment improves response strength, threshold, selectivity, and latency of auditory cortex neurons

    J. Neurophysiol.

    (2004)
  • C. Formby et al.

    Adaptive plasticity of loudness induced by chronic attenuation and enhancement of the acoustic background

    J. Acoust. Soc. Am.

    (2003)
  • M.J. Gardner et al.

    Confidence intervals rather than P values: estimation rather than hypothesis testing

    Br. Med. J. (Clin. Res. Ed.)

    (1986)
  • Y.K. Han et al.

    Early experience impairs perceptual discrimination

    Nat. Neurosci.

    (2007)
  • Cited by (50)

    • How low must you go? Effects of low-level noise on cochlear neural response

      2020, Hearing Research
      Citation Excerpt :

      Prolonged low-level noise exposures have often been used in animal studies to investigate the types of neuroplastic changes that can occur at different stages of the central auditory pathway. Many studies have identified significant functional alternations (e.g., spontaneous activity, sound evoked hyperactivity or hypoactivity, tonotopic map reorganization, abnormal temporal processing) in the auditory cortex as well as the medial geniculate body and inferior colliculus after prolonged (4–8 weeks) noise exposures presented at ostensibly “safe” exposure levels typically between 65 and 85 dB SPL (Eggermont and Komiya, 2000; Lau et al., 2015a, 2015b; Munguia et al., 2013; Pienkowski and Eggermont, 2010a, 2010b; Zheng, 2012). These sound-induced neuroplastic changes in the central auditory pathway have been reported occur in absence of any measureable noise-induced hearing loss generally assessed by measuring auditory brainstem response (ABR) thresholds.

    View all citing articles on Scopus
    View full text