Hyperacusis, an abnormally low tolerance to moderately loud sounds, can be severely debilitating. Developing effective treatments remains challenging since the neurological mechanisms responsible for loudness intolerance are not yet fully understood. However, one mechanism likely involved with generating hyperacusis is auditory gain. This mechanism essentially attempts to auto-correct neural activity levels in the central auditory pathway for diminished activity levels at the auditory nerve. For instance, in the case of sensorineural hearing loss, sound-evoked auditory nerve activity is reduced, but activities in the auditory midbrain and cortex are actually enhanced (i.e., auditory gain). This seemingly positive attribute of auditory gain—making muffled sound audible again—may actually be responsible for generating hyperacusis percepts if it becomes excessively upregulated or activated alongside normal thresholds. In cases of hyperacusis, excessive gain causes moderately intense sounds to be perceived as louder than normal.
DEVELOPMENT OF HYPERACUSIS
Loudness is encoded in auditory neurons by spike discharge rates, whereby louder sounds result in higher spike discharge rates. Since people with hyperacusis perceive sounds louder than normal, it's presumed that their auditory neurons have higher-than-normal discharge rates when sound reaches moderately loud levels. Increased sound-evoked neural discharge rates are one of the defining characteristics of enhanced auditory gain, making this mechanism a likely cause of loudness intolerance. Furthermore, agents known to induce hyperacusis such as traumatic noise exposure and ototoxic drugs also give rise to enhanced auditory gain.1,2 Hyperacusis can also occur in the absence of a clinically defined hearing loss; even in these instances, undetected cochlear pathology can lead to positive auditory gain and possibly hyperacusis.3
The above-mentioned studies suggest that excessive auditory gain in the central auditory pathways plays an important role in the development of hyperacusis. If excessive central gain is the primary neural mechanism responsible for hyperacusis, it seems plausible that reducing auditory neural activity would alleviate symptoms of hyperacusis.
LOW-LEVEL NOISE-INDUCED GAIN CHANGES
Some studies have aimed at reducing neural activity within the central auditory pathway. One method is administering neural inhibiting pharmaceuticals, but these only had limited success. Alternatively, auditory gain can be reduced using low-level noise to promote auditory plasticity. A series of studies have examined the effects of low-level noise on neural plasticity and sound-evoked activity along the ascending auditory pathway.4 Some have found that sound-evoked neural activity in the auditory cortex of cats is reduced after prolonged exposure to low-level (∼78 dB SPL) tone pip ensembles in the absence of measureable hearing loss evaluated with auditory brainstem responses.5 However, in rats, a prolonged (24 h/day) exposure to low-level (65-75 dB SPL) broadband noise (10-20 kHz) resulted in reduced auditory nerve activity at the periphery, but enhanced neural activity in the inferior colliculus in the auditory brainstem.6,7 Surprisingly, when the low-level noise was presented intermittently for 12 hours a day, sound-evoked activity in the inferior colliculus was dramatically reduced in the frequency region associated with the noise exposure band.8
The results of continuous versus intermittent low-level sound exposure may have important implications for future clinical trials. These results suggest that a critical factor involved in reducing central gain, at least in the auditory midbrain, appears to be the overall duty cycle of low-level noise exposure. They also suggest that prolonged, continuous exposure to low-level noise could lead to very mild auditory threshold shifts that provoke enhanced auditory gain (positive gain), potentially worsening symptoms of hyperacusis. In contrast, prolonged but intermittent exposure to low-level noise appears to suppress neural gain in the auditory brain, i.e., it leads to negative gain. Furthermore, the tonotopic region, which shows the greatest negative gain, corresponds to the frequency band of the prolonged but intermittent noise. If hyperacusis is in fact alleviated by reduced neural activity, it seems that in addition to noise intensity, temporal and spectral features of the long-term noise should also be considered.
Surprisingly, only a few studies have investigated the effectiveness of low-level auditory desensitization protocols. These studies suggest that continuous or intermittent prolonged exposure to low-intensity noise or pure tones increase a patient's tolerance to loud sounds.9-11 The most common clinical approach to hyperacusis management is desensitization with noise generators or hearing aid amplification. The most typical perceptual method used to evaluate sound intolerance and hyperacusis is determining the intensity level at which sounds become uncomfortably loud. Loudness discomfort levels are subjective and do not directly link changes in loudness tolerance to excessive auditory neural gain. Furthermore, loudness discomfort levels are subject to other cognitive and emotional factors that are commonly present alongside hyperacusis. For instance, many patients with hyperacusis often develop misophonia, a dislike of certain types of sounds (e.g., chewing), or phonophobia, a fear of sounds, which could cause inaccurate measurement of loudness discomfort levels. Future studies should begin to discriminate between these disorders and provide more specific and objective treatment options.
1. Auerbach, B.D., Rodrigues, P.V., Salvi, R.J. 2014. Central gain control in tinnitus and hyperacusis. Frontiers in neurology
2. Sheppard, A., Hayes, S.H., Chen, G.D., Ralli, M., Salvi, R. 2014. Review of salicylate-induced hearing loss, neurotoxicity, tinnitus and neuropathophysiology. Acta otorhinolaryngologica Italica : organo ufficiale della Societa italiana di otorinolaringologia e chirurgia cervico-facciale 34, 79-93.
3. Salvi, R., Sun, W., Ding, D., Chen, G.D., Lobarinas, E., Wang, J., Radziwon, K., Auerbach, B.D. 2016. Inner Hair Cell Loss Disrupts Hearing and Cochlear Function Leading to Sensory Deprivation and Enhanced Central Auditory Gain. Frontiers in neuroscience
4. Pienkowski, M. 2018. Rationale and Efficacy of Sound Therapies for Tinnitus and Hyperacusis. Neuroscience.
5. Pienkowski, M., 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. Hearing research
6. Sheppard, A., Liu, X., Ding, D., Salvi, R. 2018a. Auditory central gain compensates for changes in cochlear output after prolonged low-level noise exposure. Neuroscience letters
7. Sheppard, A.M., Chen, G.D., Manohar, S., Ding, D., Hu, B.H., Sun, W., Zhao, J., Salvi, R. 2017. Prolonged low-level noise-induced plasticity in the peripheral and central auditory system of rats. Neuroscience
8. Sheppard, A., Liu, X., Alkharabsheh, A., Chen, G.D., Salvi, R. 2018b. Intermittent Low-level Noise Causes Negative Neural Gain in the Inferior Colliculus. Neuroscience.
9. Formby, C., Sherlock, L.P., Gold, S.L. 2003. Adaptive plasticity of loudness induced by chronic attenuation and enhancement of the acoustic background. The Journal of the Acoustical Society of America
10. Jastreboff, P.J., Jastreboff, M.M. 2015. Decreased sound tolerance: hyperacusis, misophonia, diplacousis, and polyacousis. Handb Clin Neurol
11. Norena, A.J., Chery-Croze, S. 2007. Enriched acoustic environment rescales auditory sensitivity. Neuroreport