Long-term, passive exposure to non-traumatic acoustic noise induces neural adaptation in the adult rat medial geniculate body and auditory cortex
Introduction
Exposure to high sound pressure levels (SPLs) can permanently damage the sensory apparatus of the inner ear (Liberman and Kiang, 1978). The resulting hearing loss (i.e., increase of the minimum detectible SPL, or hearing threshold) can produce extensive reorganization of the central auditory system (Gold and Bajo, 2014). For example, following a high-frequency hearing loss, neurons in the auditory cortex (AC) that were formerly sensitive to high frequencies become sensitive to neighboring mid-frequencies (Rajan et al., 1993, Robertson and Irvine, 1989), i.e., the mid-frequencies become “over-represented” as a consequence of the high-frequency hearing loss. Some of these central effects of deafness can be reversed following the restoration of hearing, as in cochlear implantation (Pantev et al., 2006, Seghier et al., 2005). Exposure to somewhat lower SPLs may lead to only temporary elevations of hearing thresholds, followed by recovery. Such exposures are presently permitted by occupational noise standards (NIOSH, 1998, OSHA, 2002). However, recent studies found that such exposures can result in a permanent loss of inner hair cell synaptic terminals and degeneration of auditory nerve fibers, even if hearing thresholds are (initially) only temporarily affected (Kujawa and Liberman, 2009, Wang and Ren, 2012). In light of these findings, there is a serious need to further assess the potential impact of acoustic exposures that do not permanently elevate hearing thresholds.
Traditionally, research on more moderate acoustic exposures (well within present occupational limits) has focused on the more plastic developing brain (Hensch, 2004). In mature subjects, after “critical” or “sensitive” developmental periods have closed, conventional wisdom held that moderate-level acoustic exposure could not, under passive conditions (not paired with conditioned learning or stimulated neuromodulator release from the forebrain), have any long-term impact on the auditory brain (Pienkowski and Eggermont, 2011). However, the impact of long-term, passive exposure at moderate SPL in adulthood has recently gained renewed attention (Brattico et al., 2005, Gourévitch et al., 2014, Kujala et al., 2004, Noreña et al., 2006, Pienkowski and Eggermont, 2009, Pienkowski and Eggermont, 2010a, Pienkowski and Eggermont, 2010b, Pienkowski et al., 2011, Pienkowski et al., 2013, Zhou and Merzenich, 2012, Zhou et al., 2011). Eggermont et al. exposed adult cats for several weeks to months to various types of noise at levels of 68–80 dB SPL (Noreña et al., 2006, Pienkowski and Eggermont, 2009, Pienkowski and Eggermont, 2010a, Pienkowski and Eggermont, 2010b, Pienkowski et al., 2011, Pienkowski et al., 2013). The general finding was that the auditory cortical representation of sound frequencies within the noise band was profoundly suppressed, and the representation of frequencies outside of the noise band was enhanced. This is reminiscent of the effects of restricted hearing loss (Rajan et al., 1993, Robertson and Irvine, 1989), although the moderate-level exposures produced no observable signs of cochlear damage. Zhou and Merzenich extended this work to show that moderate exposure of adult rats led to behavioral deficits on an auditory temporal discrimination task (Zhou and Merzenich, 2012). Prior to this animal work, Kujala et al. had observed impaired syllable discrimination (as assessed electrophysiologically, using the mismatch negativity response) in eight shipyard workers and two preschool teachers (23– 36 years old), with an average six years of moderate occupational noise exposure but no elevation of hearing threshold (Kujala et al., 2004). Brattico et al. extended this work by comparing the effects of moderate occupational exposure on the cortical representation of speech and non-speech sounds (Brattico et al., 2005).
Previous studies on the effects on the mature auditory brain of persistent exposure to moderate-level noise have employed primarily electrophysiological testing. However, electrophysiology does not allow easy study of functional changes across the entire central auditory system, and is limited to poorly localized far-field recordings in human subjects. To advance this direction of research, including opening avenues for future measurements in humans, we here employ functional magnetic resonance imaging (fMRI) to simultaneously examine the entire central auditory system of moderate noise-exposed rats.
Blood oxygenation level dependent (BOLD) fMRI is a noninvasive neuroimaging technique (Ogawa et al., 1990) that offers a whole brain field of view with relatively high spatial resolution. fMRI has been applied extensively to study the auditory system (Binder et al., 1996, De Martino et al., 2013, Saenz and Langers, 2014), helping to show that music and language training alter response patterns in the hippocampus, AC, and other cortical and subcortical regions (Angulo-Perkins et al., 2014, Callan et al., 2003, Herdener et al., 2010, Rauschecker et al., 2008, Wang et al., 2003). fMRI has also been used to confirm that the AC of cochlear implant users is activated by electrical stimulation (Seghier et al., 2005), and that hearing loss and tinnitus alter auditory system responses (Adjamian et al., 2009, Bilecen et al., 2000, Langguth et al., 2012, Melcher et al., 2000, Middleton and Tzounopoulos, 2012). fMRI has been applied in animal models (Bach et al., 2013, Baumann et al., 2011, Brown et al., 2014, Jin and Kim, 2008, Van Ruijssevelt et al., 2013), including rats (Pawela et al., 2008, Sicard et al., 2003, Smith et al., 2002, Van Camp et al., 2006). We and others have recently developed rat auditory fMRI capabilities (Cheung et al., 2012a, Cheung et al., 2012b, Gao et al., 2014, Lau et al., 2013, Yu et al., 2009, Zhang et al., 2013).
In this study, adult rats were passively exposed for two months to pulsed noise at 65 dB SPL. Following the cessation of exposure, control (unexposed) and exposed subjects underwent fMRI with acoustic stimulation pulsed at two different rates. Region of interest analysis was performed on fMRI signals measured from the contralateral superior olivary complex, lateral lemniscus, inferior colliculus, medial geniculate body, and auditory cortex of the central auditory system. The amplitudes of fMRI signals from the different brain structures, subject groups, and stimulation rates were compared.
Section snippets
Animals and housing
All aspects of this study were approved by the Committee on Research Practices of the Hong Kong University of Science and Technology and the Committee on the Use of Live Animals in Teaching and Research of the University of Hong Kong. Normal female Sprague–Dawley rats (three months of age, N = 24) were used in this study. Twelve were randomly assigned to receive continuous acoustic exposure while the remaining 12 were assigned to standard housing. Exposed and control subjects were housed in
Results
Fig. 3 shows the fMRI activation map of control and exposed subjects receiving 5 Hz acoustic stimulation, overlaid on an anatomical image. The primary structures in the central auditory system are active, including the contralateral (left) superior olivary complex (SOC), lateral lemniscus (LL), inferior colliculus (IC), medial geniculate body (MGB), and auditory cortex (AC). The ipsilateral (right) cochlear nucleus (CN), SOC, and AC are also active. The highest t-values are observed in the LL
Discussion
Functional magnetic resonance imaging (fMRI) with pulsed acoustic stimulation was performed on adult rats which were passively exposed for two months to broadband noise at 65 dB total sound pressure level (SPL). Higher fMRI signal amplitudes were recorded during 10 Hz compared to 5 Hz pulsed acoustic stimulation. During 10 Hz (but not 5 Hz) stimulation, the contralateral medial geniculate body (MGB) and auditory cortex (AC) of exposed subjects showed significantly lower signal amplitudes compared to
Conclusion
Functional magnetic resonance imaging (fMRI) was performed on rats after long-term, passive acoustic exposure at moderate sound pressure levels. Higher fMRI signal amplitudes were recorded from subjects receiving high pulse rate acoustic stimulation than from subjects receiving low pulse rate stimulation. During high pulse rate stimulation, the contralateral medial geniculate body (MGB) and auditory cortex of exposed subjects had significantly lower signal amplitudes than those of controls. The
Acknowledgments
This research was supported by the Hong Kong General Research Fund (#661313), the Hong Kong Health and Medical Research Fund (#11122581), and start-up funding from the City University of Hong Kong and the Hong Kong University of Science and Technology.
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