Can long-term exposure to non-damaging noise lead to hyperacusis or tinnitus?
Hearing loss triggers changes in the central auditory system, some maladaptive. A region of primary auditory cortex (A1) deprived of input responds more strongly to cochlear lesion-edge frequencies, and its spontaneous firing rate (SFR) increases. This spontaneous and sound-evoked hyperactivity has been associated with tinnitus and hyperacusis, respectively. Regional increases in A1 spontaneous and sound-evoked activity are also observed after long-term exposure to non-damaging levels of noise. Adult cats exposed to such noise bands had suppressed SFR and evoked activity in the A1 region mapped to the noise band, but had increased SFR and evoked activity in A1 regions above and below the band. We hypothesized that, post-exposure, frequencies within the noise band should for some time be perceived as softer than before (hypoacusis), whereas frequencies outside of the noise band might be perceived as louder than before (hyperacusis), and might even be internalized as tinnitus. To investigate this possibility, adult CBA/Ca mice were exposed for >2 months to 8–16 kHz bandpass noise at 70 dB SPL, and tested for hypo/hyperacusis and tinnitus using prepulse inhibition (PPI) of the acoustic startle reflex (ASR), and gap-PPI of the ASR (GPIAS), respectively. ABRs and DPOAEs showed that the 70 dB SPL exposure was indeed non-damaging, whereas the same noise band at 75 dB SPL appeared to cause cochlear synaptopathy. Contrary to hypothesis, long-term exposure to non-damaging noise had no significant effect on PPI ASR and GPIAS testing. These negative findings nevertheless have important implications for PPI and GPIAS testing, and for the mechanisms of tinnitus and hyperacusis.
Bowen, G.P., Lin, D., Taylor, M.K., et al. (2003). ”Auditory cortex lesions in the rat impair both temporal acuity and noise increment thresholds, revealing a common neural substrate,” Cereb. Cortex., 13, 815-822.
Carlson, S., and Willott, J.F. (1996). “he behavioral salience of tones as indicated by prepulse inhibition of the startle response: relationship to hearing loss and central neural plasticity in C57BL/6J mice,” Hear. Res., 99, 168-175.
Chen, G., Lee, C., Sandridge, S.A., et al. (2013). ”Behavioral evidence for possible simultaneous induction of hyperacusis and tinnitus following intense sound exposure,” J. Assoc. Res. Otolaryngol., 14, 413-424.
Coomber, B., Berger, J.I., Kowalkowski, V.L., et al. (2014). “Neural changes accompanying tinnitus following unilateral acoustic trauma in the guinea pig,” Eur. J. Neurosci., 40, 2427-2441.
Davis, M., and Gendelman, P.M. (1977). “Plasticity of the acoustic startle response in the acutely decerebrate rat,” J. Comp. Physiol. Psychol., 91, 549-563.
Dobie, R.A., and Humes, L.E. (2017). “Commentary on the regulatory implications of noise-induced cochlear neuropathy,” Int. J. Audiol., 56, 74-78.
Eggermont, J.J., and Kenmochi, M. (1998). “Salicylate and quinine selectively increase spontaneous firing rates in secondary auditory cortex,” Hear. Res., 117, 149-160.
Eggermont, J.J. (2012). The Neuroscience of Tinnitus. Oxford University Press.
Eggermont, J.J. (2017). “Acquired hearing loss and brain plasticity,” Hear. Res., 343, 176-190.
Elgoyhen, A.B., Langguth, B., De Ridder, D., et al. (2015). “Tinnitus: perspectives from human neuroimaging,” Nat. Rev. Neurosci., 16, 632-642.
Engineer, N.D., Riley, J.R., Seale, J.D., et al. (2011). ”Reversing pathological neural activity using targeted plasticity,” Nature, 470, 101-104.
Fernandez, K.A., Jeffers, P.W., Lall, K., et al. (2015). ”Aging after noise exposure: Acce-leration of cochlear synaptopathy in “recovered” ears,” J. Neurosci., 35, 7509-7520.
Fox, J.E. (1979). “Habituation and prestimulus inhibition of the auditory startle reflex in decerebrate rats,” Physiol. Behav., 23, 291-297.
Galazyuk, A., and Hébert, S. (2015). “Gap-prepulse inhibition of the acoustic startle reflex (GPIAS) for tinnitus assessment: Current status and future directions,” Front. Neurol., 6, 88.
Grimsley, C.A., Longenecker, R.J., Rosen, et al. (2015). ”An improved approach to separating startle data from noise,” J. Neurosci. Meth., 253, 206-217.
Gu, J.W., Halpin, C.F., Nam, E.C., et al. (2010). “Tinnitus, diminished sound-level tolerance, and eleva-ted auditory activity in humans with normal hearing sensitivity,” J. Neurophysiol., 104, 3361-3370.
Gu, J.W., Herrmann, B.S., Levine, R.A., et al. (2012). “Brainstem auditory evoked potentials suggest a role for the ventral cochlear nucleus in tinnitus,” J. Assoc. Res. Otolaryngol., 13, 819-833.
Guest, H., Munro, K.J., Prendergast, G., et al. (2017). “Tinnitus with a normal audiogram: Relation to noise exposure but no evidence for cochlear synaptopathy,” Hear. Res., 344, 265-274.
Hesse, L.L., Bakay, W., Ong, H.C., et al. (2016). “Non-monotonic relation between noise expo-sure severity and neuronal hyperactivity in the auditory midbrain,” Front. Neurol., 7, 133.
Hickox, A.E., and Liberman, M.C. (2014). “Is noise-induced cochlear neuropathy key to the generation of hyperacusis or tinnitus?” J. Neurophysiol., 111, 552-564.
Ison, J.R., O’Connor K., Bowen, G.P., et al. (1991). ”Temporal resolution of gaps in noise by the rat is lost with functional decortication,” Behav. Neurosci., 105, 33-40.
Ison, J.R., Allen, P.D., and O'Neill, W.E. (2007). “Age-related hearing loss in C57BL/6J mice has both frequency-specific and non-frequency-specific components that produce a hyperacusis-like exaggeration of the acoustic startle reflex,” J. Assoc. Res. Otolaryngol., 8, 539-550.
Kaltenbach, J.A., Zacharek, M.A., Zhang, J., et al. (2004). ”Activity in the dorsal cochlear nucleus of ham-sters previously tested for tinnitus following intense tone exposure,” Neurosci. Lett., 355, 121-125.
Koch, M. (1999). “The neurobiology of startle,” Prog. Neurobiol., 59, 107-128.
Kujawa, S.G., and Liberman, M.C. (2015). “Synaptopathy in the noise-exposed and aging cochlea: Primary neural degeneration in acquired sensorineural hearing loss,” Hear. Res., 330, 191-199.
Lau, C., Zhang, J.W., McPherson, B., et al. (2015). ”Functional magnetic resonance imaging of the adult rat central auditory system following long-term, passive exposure to non-traumatic acoustic noise,” Neuroimage, 107, 1-9.
Li, L., and Frost, B.J. (2000). “Azimuthal directional sensitivity of prepulse inhibition of the pinna startle reflex in decerebrate rats,” Brain Res. Bull., 51, 95-100.
Li, S., Choi, V., and Tzounopoulos, T. (2013). “Pathogenic plasticity of Kv7.2/3 channel acti-vity is essential for the induction of tinnitus,” Proc. Natl. Acad. Sci. USA., 110, 9980-9985.
Longenecker, R.J., and Galazyuk, A.V. (2016). “Variable effects of acoustic trauma on behavioral and neural correlates of tinnitus in individual animals,” Front. Behav. Neurosci., 10, 207.
Maison, S.F., Usubuchi, H., and Liberman, M.C. (2013). “Efferent feedback minimizes cochlear neuropathy from moderate noise exposure,” J. Neurosci., 27, 5542-5552.
Munguia, R., Pienkowski, M., and Eggermont, J.J. (2013). “Spontaneous firing rate changes in cat primary auditory cortex following long-term exposure to non-traumatic noise: Tinnitus without hearing loss?” Neurosci. Lett., 546, 46-50.
NIOSH (1998). “Criteria for a recommended standard: Occupational noise exposure,” National Institute for Occupational Safety and Health Publication No: 98-126.
Noreña, A.J., Gourévitch, B., Aizawa, N., et al. (2006). “Spectrally enhanced acoustic environ-ment disrupts frequency representation in cat auditory cortex,” Nat. Neurosci., 9, 932-939.
OSHA (2002). Hearing Conservation. Occupational Safety and Health Administration, U.S. Department of Labor, Publication No: OSHA 3074.
Paul, B.T., Bruce, I.C., and Roberts, L.E. (2017). “Evidence that hidden hearing loss underlies amplitude modulation encoding deficits in individuals with and without tinnitus,” Hear. Res., 344, 170-182.
Pienkowski, M., and Eggermont, J.J. (2009). “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., 257, 24-40.
Pienkowski, M., and Eggermont, J.J. (2010a). “Intermittent exposure with moderate-level sound impairs central auditory function of mature animals without concomitant hearing loss,” Hear. Res., 261, 30-35.
Pienkowski, M., and Eggermont, J.J. (2010b). “Passive exposure of adult cats to moderate-level tone pip ensembles differentially decreases AI and AII responsiveness in the exposure frequency range,” Hear. Res., 268, 151-162.
Pienkowski, M., and Eggermont, J.J. (2011). “Cortical tonotopic map plasticity and behaviour,” Neurosci. Biobehav. Rev., 35, 2117-2128.
Pienkowski, M., Munguia, R., and Eggermont, J.J. (2011). “Passive exposure of adult cats to bandlimited tone ensembles or noise leads to long-term response suppression in auditory cortex,” Hear. Res., 277, 117-126.
Pienkowski, M., and Eggermont, J.J. (2012). “Reversible long-term changes in auditory processing in mature auditory cortex in the absence of hearing loss induced by passive, moderate-level sound exposure,” Ear. Hearing, 33, 305-314.
Pienkowski, M., Munguia, R., and Eggermont, J.J. (2013). “Effects of passive, moderate-level sound exposure on the mature auditory cortex: Spectral edges, spectrotemporal density, and real-world noise,” Hear. Res., 296, 121-130.
Pienkowski, M., Tyler, R.S., Roncancio, E.R., et al. (2014). ”A review of hyperacusis and future directions: Part II. Measurement, mechanisms, and treatment,” Am. J. Audiol., 23, 420-436.
Ropp, T.J., Tiedemann, K.L., Young, E.D., et al. (2014). ”Effects of unilateral acoustic trauma on tinnitus-related spontaneous activity in the inferior colliculus,” J. Assoc. Res. Otolaryngol., 15, 1007-1022.
Rubak, T., Kock, S., Koefoed-Nielsen, B., et al. (2008). “The risk of tinnitus following occupational noise exposure in workers with hearing loss or normal hearing,” Int. J. Audiol., 47, 109-114.
Schaette, R., and McAlpine, D. (2011). “Tinnitus with a normal audiogram: physiological evi-dence for hidden hearing loss and computational model,” J. Neurosci., 31, 13452-13457.
Sturm, J.J., Zhang-Hooks, Y.X., Roos, H., et al. (2017). “Noise trauma induced behavioral gap detection deficits correlate with reorganization of excitatory and inhibitory local circuits in the inferior colliculus and are prevented by acoustic enrichment,” J. Neurosci., 37, 6314-6330.
Sun, W., Lu, J., Stolzberg, D., et al. (2009). “Salicylate increases the gain of the central auditory system,” Neuroscience, 159, 325-334.
Sun, W., Deng, A., Jayaram, A., et al. (2012). “Noise exposure enhances auditory cortex responses related to hyperacusis behaviour,” Brain Res., 1485, 108-116.
Turner, J.G., and Parish, J. (2008). “Gap detection methods for assessing salicylate-induced tinnitus and hyperacusis in rats,” Am. J. Audiol., 17, S185-S192.
Tyler, R.S., Pienkowski, M., Roncancio, E.R., et al. (2014). ”A review of hyperacusis and future directions. Part I. Definitions and manifestations,” Am. J. Audiol., 23, 402-419.
Weible, A.P., Moore, A.K., Liu, C., et al. (2014). “Perceptual gap detection is mediated by gap termination responses in auditory cortex,” Curr. Biol., 24, 1447-1455.
Weisz, N., Hartmann, T., Dohrmann, K., et al. (2006). “High-frequency tinnitus without hearing loss does not mean absence of deafferentation,” Hear. Res., 222, 108-114.
Wu, C., Martel, D.T., and Shore, S.E. (2016). “Increased synchrony and bursting of dorsal cochlear nucleus fusiform cells correlate with tinnitus,” J. Neurosci., 36, 2068-2073.
Xiong, B., Alkharabsheh, A., Manohar, S., et al. (2017). “Hyperexcitability of inferior colli-culus and acoustic startle reflex with age-related hearing loss,” Hear. Res., 350, 32-42.
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