Elsevier

NeuroImage

Volume 122, 15 November 2015, Pages 44-51
NeuroImage

Chronic exposure to broadband noise at moderate sound pressure levels spatially shifts tone-evoked responses in the rat auditory midbrain

https://doi.org/10.1016/j.neuroimage.2015.07.065Get rights and content

Highlights

  • fMRI was applied on a chronic and moderate intensity acoustic exposure model.

  • IC responses to tones shifted to regions that normally respond to lower frequencies.

  • Shifts quantified by ROI and center of responsive region analyses.

  • Results suggest that high frequency regions above exposure bandwidth spatially expand.

Abstract

Noise-induced hearing disorders are a significant public health concern. One cause of such disorders is exposure to high sound pressure levels (SPLs) above 85 dBA for eight hours/day. High SPL exposures occur in occupational and recreational settings and affect a substantial proportion of the population. However, an even larger proportion is exposed to more moderate SPLs for longer durations. Therefore, there is significant need to better understand the impact of chronic, moderate SPL exposures on auditory processing, especially in the absence of hearing loss. In this study, we applied functional magnetic resonance imaging (fMRI) with tonal acoustic stimulation on an established broadband rat exposure model (65 dB SPL, 30 kHz low-pass, 60 days). The auditory midbrain response of exposed subjects to 7 kHz stimulation (within exposure bandwidth) shifts dorsolaterally to regions that typically respond to lower stimulation frequencies. This shift is quantified by a region of interest analysis that shows that fMRI signals are higher in the dorsolateral midbrain of exposed subjects and in the ventromedial midbrain of control subjects (p < 0.05). Also, the center of the responsive region in exposed subjects shifts dorsally relative to that of controls (p < 0.05). A similar statistically significant shift (p < 0.01) is observed using 40 kHz stimulation (above exposure bandwidth). The results suggest that high frequency midbrain regions above the exposure bandwidth spatially expand due to exposure. This expansion shifts lower frequency regions dorsolaterally. Similar observations have previously been made in the rat auditory cortex. Therefore, moderate SPL exposures affect auditory processing at multiple levels, from the auditory cortex to the midbrain.

Introduction

Acoustic noise exposure can lead to numerous health disorders. One of the most prominent disorders is noise-induced hearing loss. According to the National Institute on Deafness and Other Communication Disorders of the United States, approximately 15% of Americans between the ages of 20 and 69 have noise exposure related hearing loss (NIDCD, 2014). This may well be an underestimate as not all hearing loss is easily detected using the current gold standard of pure tone audiometry (Plack et al., 2014). Further, 16% of teenagers from 12 to 19 years of age may have noise exposure related hearing loss. This suggests the prevalence of hearing disorders will increase in the coming years. The noise exposures leading to hearing loss can come from occupational and recreational settings. To help protect hearing, the National Institute for Occupational Safety and Health has set a recommended exposure limit of 85 dBA averaged over 8 hr/day (NIOSH, 1998).

Unfortunately, a significant proportion of the population still receives acoustic exposures exceeding the 85 dBA limit. Furthermore, a potentially much larger proportion receives more moderate sound pressure level (SPL) exposures, in the 60–80 dBA range, for a longer duration. Chronic and moderate SPL exposures can come from noise sources such as transportation vehicles, construction equipment, and crowded restaurants. The potential impact of such exposures on auditory health is not well understood. Therefore, there is significant need to better understand the impact, especially in the absence of clinically significant hearing loss. Chronic exposures at moderate SPLs may be related to hearing disorders that affect central auditory processing. Recent human studies have observed auditory abnormalities in noise exposed subjects without hearing loss. For example, Stamper et al. studied subjects with a range of chronic noise exposure backgrounds, 67–83 dBA (Stamper and Johnson, 2015). They observed that the auditory brainstem response wave I amplitude decreased with noise exposure background, which could suggest a loss of afferent nerve terminals and cochlear nerve degeneration (Kujawa and Liberman, 2009). Kujala et al. studied subjects with noisy occupations (shipyards, daycare centers) and subjects with quiet occupations (Kujala et al., 2004). The noise levels in a shipyard ranged from 95 to 100 dBA (workers wore ear protection) and in a daycare center ranged from 67 to 75 dB. The investigators found that noisy occupation subjects had impaired speech-sound discrimination compared with quiet occupation subjects. Also, noisy occupation subjects were more easily distracted by irrelevant sounds. Brattico et al. studied subjects from the armchair industry and subjects with quiet occupations (Brattico et al., 2005). The background noise level in the armchair industry was 70–80 dB. The mismatch negativity results to deviant and speech sounds of armchair subjects differed from those of quiet occupation subjects, again suggesting impaired speech–sound discrimination.

Recent animal model studies of the auditory system have begun to investigate behavioral and neuronal changes following chronic exposures at moderate SPLs (Pienkowski and Eggermont, 2010a, Zhou and Merzenich, 2012). These studies have shown considerable functional changes in the auditory cortex. Our group has recently used blood oxygenation level dependent (BOLD) functional magnetic resonance imaging (fMRI) to investigate the impact of acoustic exposure in animal models (Cheung et al., 2012b, Lau et al., 2015). BOLD fMRI exploits the different magnetic properties of oxyhemoglobin and deoxyhemoglobin in blood to indirectly measure neuronal activity (Ogawa et al., 1990). It is well suited to investigating the impact of acoustic exposures because measurements are noninvasive, simultaneously investigate the entire central auditory system, and have relatively good spatial resolution. fMRI has been employed extensively to investigate the central auditory system in both human and animal subjects (Bach et al., 2013, Baumann et al., 2011, Boemio et al., 2005, Boumans et al., 2008, Brown et al., 2013, Maeder et al., 2001, Opitz et al., 2002, Patterson et al., 2002, Perrodin et al., 2011, Van Meir et al., 2005). Our group and others have extended fMRI methods to perform investigations of rodent models, including of the auditory system (Chan et al., 2010, Cheung et al., 2012a, Cheung et al., 2012b, Duong et al., 2000, Gao et al., 2014, Hyder et al., 2002, Lau et al., 2011a, Lau et al., 2011b, Lau et al., 2013, Lau et al., 2015, Pawela et al., 2008, Peeters et al., 2001, Shih et al., 2009, Sicard et al., 2003, Silva and Koretsky, 2002, Weber et al., 2006, Yu et al., 2012, Zhang et al., 2013, Zhou et al., 2012).

In this study, we used BOLD fMRI with tonal acoustic stimulation to investigate the central auditory system of adult rats following chronic noise exposure at moderate SPLs. fMRI images were analyzed using conventional methods and custom methods tailored to this study.

Section snippets

Animal subjects

All aspects of this study were approved by the animal research ethics committees of the City University of Hong Kong and the University of Hong Kong. Ninety day old female Sprague Dawley rats (N = 13) were employed in this study. Female subjects were chosen to reduce size increase during the course of the study. Male rats increase in size considerably faster than females and large size increase can complicate functional magnetic resonance imaging (fMRI) experiments. One subject was used to

Results

Figs. 2 shows the group-averaged activation maps for control and noise exposed subjects during 7 kHz tonal acoustic stimulation. Activated voxels are observed in the contralateral (left) lateral lemniscus (LL) and inferior colliculus (IC). Contralateral activation is expected and had been observed in our earlier rat auditory functional magnetic resonance imaging (fMRI) studies (Cheung et al., 2012a, Cheung et al., 2012b, Gao et al., 2014, Lau et al., 2013, Lau et al., 2015, Zhang et al., 2013).

Discussion

Functional magnetic resonance imaging (fMRI) with tonal acoustic stimulation was performed on an established rat model of chronic exposure to moderate sound pressure level (SPL) noise. The inferior colliculus (IC) response of noise exposed subjects to 7 kHz stimulation (within the noise exposure bandwidth) shifted dorsolaterally to regions that typically respond to lower frequency sound. This shift was quantified by a region of interest (ROI) analysis which showed that fMRI signals were higher

Conclusion

Functional magnetic resonance imaging was used to investigate rat subjects receiving chronic, moderate sound pressure level (SPL) noise exposure. The inferior colliculus (IC) responses of noise exposed subjects to tonal acoustic stimuli both within and above the exposure bandwidth shifted dorsolaterally to regions that typically respond to lower stimulation frequencies. These results support the spatial expansion of high frequency IC regions above the exposure bandwidth, shifting lower

Acknowledgments

This research was supported by the Hong Kong General Research Fund (#661313 and #17103015), the Hong Kong Health and Medical Research Fund (#11122581), and start-up funding from the City University of Hong Kong (#7200414).

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