Chronic exposure to broadband noise at moderate sound pressure levels spatially shifts tone-evoked responses in the rat auditory 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).
References (57)
- et al.
Music listening engages specific cortical regions within the temporal lobes: differences between musicians and non-musicians
Cortex
(2014) - et al.
Long-term exposure to occupational noise alters the cortical organization of sound processing
Clin. Neurophysiol.
(2005) - et al.
Characterization of the blood-oxygen level-dependent (BOLD) response in cat auditory cortex using high-field fMRI
NeuroImage
(2013) - et al.
Learning-induced neural plasticity associated with improved identification performance after training of a difficult second-language phonetic contrast
NeuroImage
(2003) - et al.
Functional MRI of postnatal visual development in normal and hypoxic–ischemic-injured superior colliculi
NeuroImage
(2010) - et al.
BOLD fMRI investigation of the rat auditory pathway and tonotopic organization
NeuroImage
(2012) - et al.
High fidelity tonotopic mapping using swept source functional magnetic resonance imaging
NeuroImage
(2012) - et al.
The inferior colliculus is involved in deviant sound detection as revealed by BOLD fMRI
NeuroImage
(2014) - et al.
BOLD responses in the superior colliculus and lateral geniculate nucleus of the rat viewing an apparent motion stimulus
NeuroImage
(2011) - et al.
Long-term, passive exposure to non-traumatic acoustic noise induces neural adaptation in the adult rat medial geniculate body and auditory cortex
NeuroImage
(2015)
Distinct pathways involved in sound recognition and localization: a human fMRI study
NeuroImage
Differential contribution of frontal and temporal cortices to auditory change detection: fMRI and ERP results
NeuroImage
The processing of temporal pitch and melody information in auditory cortex
Neuron
Modeling of region-specific fMRI BOLD neurovascular response functions in rat brain reveals residual differences that correlate with the differences in regional evoked potentials
NeuroImage
Comparing BOLD fMRI signal changes in the awake and anesthetized rat during electrical forepaw stimulation
Magn. Reson. Imaging
Voice cells in the primate temporal lobe
Curr. Biol.
Long-term, partially-reversible reorganization of frequency tuning in mature cat primary auditory cortex can be induced by passive exposure to moderate-level sounds
Hear. Res.
Intermittent exposure with moderate-level sound impairs central auditory function of mature animals without concomitant hearing loss
Hear. Res.
Passive exposure of adult cats to moderate-level tone pip ensembles differentially decreases AI and AII responsiveness in the exposure frequency range
Hear. Res.
Passive exposure of adult cats to bandlimited tone pip ensembles or noise leads to long-term response suppression in auditory cortex
Hear. Res.
Effects of passive, moderate-level sound exposure on the mature auditory cortex: spectral edges, spectrotemporal density, and real-world noise
Hear. Res.
Dose-response hearing-loss for white noise in the Sprague–Dawley rat
Fundam. Appl. Toxicol.
Spatiotemporal properties of the BOLD response in the songbirds' auditory circuit during a variety of listening tasks
NeuroImage
A fully noninvasive and robust experimental protocol for longitudinal fMRI studies in the rat
NeuroImage
Direct imaging of macrovascular and microvascular contributions to BOLD fMRI in layers IV–V of the rat whisker–barrel cortex
NeuroImage
Functional magnetic resonance imaging of sound pressure level encoding in the rat central auditory system
NeuroImage
Auditory map reorganization and pitch discrimination in adult rats chronically exposed to low-level ambient noise
Front. Syst. Neurosci.
Functional magnetic resonance imaging of the ascending stages of the auditory system in dogs
BMC Vet. Res.
Cited by (24)
The effects of exposure to road traffic noise at school on central auditory pathway functional connectivity
2023, Environmental ResearchHow low must you go? Effects of low-level noise on cochlear neural response
2020, Hearing ResearchCitation Excerpt :However, at 1-week post-exposure response amplitudes were within the normal range. Many studies have employed passive exposure to long-duration, low-level noise to elucidate the neuroplastic changes occurring in the central auditory pathway of adult and developing animals (Chang and Merzenich, 2003; de Villers-Sidani et al., 2007; Eggermont and Komiya, 2000; Lau et al., 2015b; Munguia et al., 2013; Pienkowski and Eggermont, 2010b; Zheng, 2012). A fundamental assumption of these studies is that low-intensity exposures do not disrupt the neural output of the cochlea because the exposure did not induce a threshold shift or because the intensity was too low to do so.
BOLD-fMRI in the mouse auditory pathway
2018, NeuroImageCitation Excerpt :Thus, despite its indirect nature, BOLD can still be very useful for mapping spatial locations of neural activity, and in some cases, also reflect some of its dynamics. In rodents, BOLD is typically easier to detect in rats than mice using fMRI (Jonckers et al., 2015), and fMRI in the rat was indeed widely used for studying disorders such as stroke (Canazza et al., 2014), epilepsy (Blumenfeld, 2007), ischemia (Chan et al., 2010), or to study plasticity (Lau et al., 2015), e.g., after nerve deafferentation. Global brain function arising from tactile stimulation (fore/hind paws, whiskers) was extensively studied in normal animals (Shih et al., 2013); in addition, activation patterns arising from visual (Bailey et al., 2013; Lau et al., 2011a, b; Matthew C. Murphy et al., 2016a,b; Niranjan et al., 2016; Pawela et al., 2008; Tambalo et al., 2015; Van Camp et al., 2006), olfactory (Matthew C Murphy et al., 2016a,b) and, recently, auditory stimuli (Cheung et al., 2012a) were reported.
Prolonged low-level noise-induced plasticity in the peripheral and central auditory system of rats
2017, NeuroscienceCitation Excerpt :Interestingly, these neuroplastic changes have all been reported in absence of peripheral hearing loss. Additional studies have indicated that similar neuroplasticity likely occurs at more peripheral auditory loci such as the medial geniculate body and inferior colliculus (IC) (Lau et al., 2015a, 2015b). At the level of the peripheral auditory system, low-level noise has been shown to alter auditory function.