Abstract
Temporary hearing threshold shift (TTS) resulting from a “benign” noise exposure can cause irreversible auditory nerve afferent terminal damage and retraction. While hearing thresholds and acute tissue injury recover within 1–2 weeks after a noise overexposure, it is not clear if multiple TTS noise exposures would result in cumulative damage even though sufficient TTS recovery time is provided. Here, we tested whether repeated TTS noise exposures affected permanent hearing thresholds and examined how that related to inner ear histopathology. Despite a peak 35–40 dB TTS 24 hours after each noise exposure, a double dose (2 weeks apart) of 100 dB noise (8–16 kHz) exposures to young (4-week-old) CBA mice resulted in no permanent threshold shifts (PTS) and abnormal distortion product otoacoustic emissions (DPOAE). However, although auditory brainstem response (ABR) thresholds recovered fully in once- and twice-exposed animals, the growth function of ABR wave 1 p-p amplitude (synchronized spiral ganglion cell activity) was significantly reduced to a similar extent, suggesting that damage resulting from a second dose of the exposure was not proportional to that observed after the initial exposure. Estimate of surviving inner hair cell afferent terminals using immunostaining of presynaptic ribbons revealed ribbon loss of ∼40 % at the ∼23 kHz region after the first round of noise exposure, but no additional loss of ribbons after the second exposure. In contrast, a third dose of the same noise exposure resulted in not only TTS, but also PTS even in regions where DPOAEs were not affected. The pattern of PTS seen was not entirely tonotopically related to the noise band used. Instead, it resembled more to that of age-related hearing loss, i.e., high frequency hearing impairment towards the base of the cochlea. Interestingly, after a 3rd dose of the noise exposure, additional loss of ribbons (another ∼25 %) was observed, suggesting a cumulative detrimental effect from individual “benign” noise exposures, which should result in a significant deficit in central temporal processing.
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References
Adams JC (2009) Immunocytochemical traits of type IV fibrocytes and their possible relations to cochlear function and pathology. J Assoc Res Otolaryngol 10:369–382
Canlon B, Fransson A (1998) Reducing noise damage by using a mid-frequency sound conditioning stimulus. Neuroreport 9:269–274
Darrow KN, Simons EJ, Dodds L, Liberman MC (2006) Dopaminergic innervation of the mouse inner ear: evidence for a separate cytochemical group of cochlear efferent fibers. J Comp Neurol 498:403–414
Darrow KN, Maison SF, Liberman MC (2007) Selective removal of lateral olivocochlear efferents increases vulnerability to acute acoustic injury. J Neurophysiol 97:1775–1785
Hequembourg S, Liberman MC (2001) Spiral ligament pathology: a major aspect of age-related cochlear degeneration in C57BL/6 mice. J Assoc Res Otolaryngol 2:118–129
Hirose K, Liberman MC (2003) Lateral wall histopathology and endocochlear potential in the noise-damaged mouse cochlea. J Assoc Res Otolaryngol 4:339–352
Khimich D, Nouvian R, Pujol R, Dieck ST, Egner A, Gundelfinger ED, Moser T (2005) Hair cell synaptic ribbons are essential for synchronous auditory signalling. Nature 434:889–894
Kujawa SG, Liberman MC (2006) Acceleration of age-related hearing loss by early noise exposure: evidence of a misspent youth. J Neurosci 26:2115–2123
Kujawa SG, Liberman MC (2009) Adding insult to injury: cochlear nerve degeneration after "temporary" noise-induced hearing loss. J Neurosci 29:14077–14085
Lang H, Jyothi V, Smythe NM, Dubno JR, Schulte BA, Schmiedt RA (2010) Chronic reduction of endocochlear potential reduces auditory nerve activity: further confirmation of an animal model of metabolic presbyacusis. J Assoc Res Otolaryngol 11:419–434
Liberman LD, Wang H, Liberman MC (2011) Opposing gradients of ribbon size and AMPA receptor expression underlie sensitivity differences among cochlear-nerve/hair-cell synapses. J Neurosci 31(3):801–808. doi:10.1523/JNEUROSCI.3389-10.2011
Liberman MC (1982) Single-neuron labeling in the cat auditory nerve. Science 216:1239–1241
Liberman MC, Dodds LW (1984a) Single-neuron labeling and chronic cochlear pathology. II. Stereocilia damage and alterations of spontaneous discharge rates. Hear Res 16:43–53
Liberman MC, Dodds LW (1984b) Single-neuron labeling and chronic cochlear pathology. III. Stereocilia damage and alterations of threshold tuning curves. Hear Res 16:55–74
Limb CJ, Ryugo DK (2000) Development of primary axosomatic endings in the anteroventral cochlear nucleus of mice. J Assoc Res Otolaryngol 1:103–119
Lin HW, Furman AG, Kujawa SG, Liberman MC (2011) Primary neural degeneration in the Guinea pig cochlea after reversible noise-induced threshold shift. J Assoc Res Otolaryngol 12(5):605–616. doi:10.1007/s10162-011-0277-0
Meyer AC, Frank T, Khimich D, Hoch G, Riedel D, Chapochnikov NM, Yarin YM, Harke B, Hell SW, Egner A, Moser T (2009) Tuning of synapse number, structure and function in the cochlea. Nat Neurosci 12:444–453
Muller M, Hunerbein K, Hoidis S, Smolders JW (2005) A physiological place-frequency map of the cochlea in the CBA/J mouse. Hear Res 202:63–73
Nordmann AS, Bohne BA, Harding GW (2000) Histopathological differences between temporary and permanent threshold shift. Hear Res 139:13–30
Prijs VF (1986) Single-unit response at the round window of the guinea pig. Hear Res 21:127–133
Puel JL, Ruel J, D'Aldin CG, Pujol R (1998) Excitotoxicity and repair of cochlear synapses after noise-trauma induced hearing loss. Neuroreport 9:2109–2114
Robertson D (1982) Effects of acoustic trauma on stereocilia structure and spiral ganglion cell tuning properties in the guinea pig cochlea. Hear Res 7:55–74
Seal RP, Akil O, Yi E, Weber CM, Grant L, Yoo J, Clause A, Kandler K, Noebels JL, Glowatzki E, Lustig LR, Edwards RH (2008) Sensorineural deafness and seizures in mice lacking vesicular glutamate transporter 3. Neuron 57:263–275
Song L, McGee J, Walsh EJ (2008) Development of cochlear amplification, frequency tuning, and two-tone suppression in the mouse. J Neurophysiol 99:344–355
Stamataki S, Francis HW, Lehar M, May BJ, Ryugo DK (2006) Synaptic alterations at inner hair cells precede spiral ganglion cell loss in aging C57BL/6J mice. Hear Res 221:104–118
Taberner AM, Liberman MC (2005) Response properties of single auditory nerve fibers in the mouse. J Neurophysiol 93:557–569
Tsuji J, Liberman MC (1997) Intracellular labeling of auditory nerve fibers in guinea pig: central and peripheral projections. J Comp Neurol 381:188–202
Wang Y, Hirose K, Liberman MC (2002) Dynamics of noise-induced cellular injury and repair in the mouse cochlea. J Assoc Res Otolaryngol 3:248–268
Wang Y, Liberman MC (2002) Restraint stress and protection from acoustic injury in mice. Hear Res 165:96–102
Willott JF, Erway LC (1998) Genetics of age-related hearing loss in mice. IV. Cochlear pathology and hearing loss in 25 BXD recombinant inbred mouse strains. Hear Res 119:27–36
Yoshida N, Kristiansen A, Liberman MC (1999) Heat stress and protection from permanent acoustic injury in mice. J Neurosci 19:10116–10124
Yoshida N, Liberman MC (2000) Sound conditioning reduces noise-induced permanent threshold shift in mice. Hear Res 148:213–219
Acknowledgments
We thank Dr. A. Park and M. Pasker for comments and proofreading the manuscript. Dr. MC Liberman provided the original schematic drawing used in Fig. 5A. Supported by NIDCD R03DC008190
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Wang, Y., Ren, C. Effects of Repeated “Benign” Noise Exposures in Young CBA Mice: Shedding Light on Age-related Hearing Loss. JARO 13, 505–515 (2012). https://doi.org/10.1007/s10162-012-0329-0
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DOI: https://doi.org/10.1007/s10162-012-0329-0