September 1, 2009 Feature

The Biological Mechanisms of Hyperacusis

Animal Models Help Uncover Brain Basis for Disorder

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Hyperacusis, or recruitment, is characterized by an abnormally strong reaction or reduced tolerance to ordinary environmental sound. Hyperacusis can reduce the quality of life. Patients with severe hyperacusis avoid going to parties, restaurants, and even meetings, since the environment is just "too loud" for them. Some people with this condition will leave their homes only if wearing ear plugs.

The prevalence of hyperacusis in the general population is about 9%–15% (Herraiz et al., 2006). Hyperacusis can occur along with a variety of disorders including acoustic trauma, stapedectomy, Williams syndrome in children, migraine attacks, facial paralysis, and tinnitus. The mechanism underlying hyperacusis is unclear and as yet there is no treatment.

Physiological Mechanisms

It has been hypothesized that hyperacusis is induced by hyperactivity of the auditory nerve, which will increase the sensitivity to a loud sound (Moore, 1995). Supporting this hypothesis is the fact that noise exposure, a common cause of hyperacusis, can broaden the tuning curve of the auditory nerve, i.e., the auditory nerve acquires poor frequency selectivity. This poor frequency selectivity was assumed to cause the faster recruitment of activated auditory fibers with increasing sound intensity. However, recent animal studies contradict this assumption because excitation of auditory nerve fibers decreases following acoustic trauma, suggesting that hyperacusis may not be induced by hyperactivity of the auditory nerve (Heinz et al., 2004).

A growing body of evidence from animal studies shows that cochlear damage can induce an abnormally rapid growth in the amplitude of sound-evoked potentials as well as other neuronal response properties within the central auditory system (Salvi et al., 2000; Syka et al., 2000). Exposure to noise or ototoxic drugs can enhance the response in the central auditory system despite a reduced output from the cochlea. For example, when rats received a high dose of sodium salicylate (the major component of aspirin), known to temporarily induce high-frequency hearing loss and tinnitus, the amplitude of the compound action potential was reduced (Sun et al., 2009; see Figure 1A [PDF, 2.67 MB]). Paradoxically, the sodium salicylate dose significantly enhanced the sound-evoked auditory cortical response (Figure 1B [PDF, 2.67 MB]). Because the enhanced cortical response was not caused by a reduction in peripheral input, salicylate may increase the cortical response by adjusting the "volume" of neural input.

Most activities in the brain are strongly regulated by inhibitory neurons, known as GABAergic neurons. A reduction of inhibitory influences in the brain may cause an increased state of excitation in the brain. Recent studies detected salicylate's ability to reduce inhibitory neuronal activity in the auditory cortex, which presumably would result in an overall enhancement of the cortical response to sound (Wang et al., 2008). Because the auditory cortex is essential for sound perception, the enhanced cortical response to acoustic stimuli is to increase the perception of loudness and may underlie hyperacusis.

Animal Model for Hyperacusis

Because hyperacusis involves the perception of sound, a behavioral test is critical in an animal model of hyperacusis to corroborate the relationship of hyperacusis perception to changes in neurological activity. Several laboratories recently reported using the acoustic startle reflex, a contraction of the skeletal and facial muscles to sudden, intense sounds, to measure the behavioral response to loud sounds (Ison et al., 2007; Sun et al., 2009; Turner et al., 2008). As shown in Figure 2A [PDF], the startle reflex can be quantified by measuring the power of the animal's response using the voltage output of a piezoelectric transducer mounted under the animal's testing chamber. In normal animals, the acoustic reflex is proportional to the sound intensity. Interestingly, when animals develop aging-related high-frequency hearing loss, they show an exaggerated startle response to low-frequency sound stimuli. This exaggerated response suggests that the animal developed an increased sensitivity to low-frequency stimuli as it developed a high-frequency hearing loss. This observation is consistent with the frequent co-occurrence of hyperacusis with presbycusis in humans.

We found that salicylate can induce an enhanced acoustic startle reflex response as well as mild hearing loss, as shown in Figure 2B [PDF]. The increased startle reflex is consistent with the salicylate-induced enhancement of the sound-evoked auditory cortex response described above and implies that hyperacusis may be related to the enhanced response in the central auditory system, such as in the auditory cortex. These results also suggest that the response in the central auditory system can be altered by ototoxic drugs or by another mechanism regardless of the level of peripheral input.

The incidence of hyperacusis is very high among people who have tinnitus; 40%–86% of those who have tinnitus also have hyperacusis (Moller, 2007). Determining the biological mechanism of hyperacusis and whether there is a relationship between hyperacusis and tinnitus may provide insight for clinical treatment of both of these disorders.

Wei Sun, PhD, CCC-A, assistant professor in the Department of Communicative Disorders and Sciences at State University of New York at Buffalo, researches the physiological mechanisms of the central auditory system reorganization related to tinnitus and hyperacusis in animal models. His research is funded by The Royal National Institute for Deaf People and the American Federation for Aging Research. Contact him at weisun@buffalo.edu.

cite as: Sun, W. (2009, September 01). The Biological Mechanisms of Hyperacusis : Animal Models Help Uncover Brain Basis for Disorder. The ASHA Leader.

References

Heinz, M.G., & Young, E.D. (2004). Response growth with sound level in auditory-nerve fibers after noise-induced hearing loss. Journal of Neurophysiology, 91, 784–95.

Herraiz, C., Plaza, G., & Aparicio, J.M. (2006). Mechanisms and management of hyperacusis (decreased sound tolerance). Acta Otorrinolaringol Espanola, 57, 373–7.

Ison, J.R., Allen, P.D., & 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. Journal of the Association for Research in Otolaryngology, 8, 539–50.

Moller, A.R. (2007). Tinnitus: presence and future. Progress in Brain Research, 166, 3–16.

Moore, B.C. (1995). Perceptual Consequences of Cochlear Damage. New York: Oxford University Press.

Salvi, R.J., Wang, J., & Ding, D. (2000). Auditory plasticity and hyperactivity following cochlear damage. Journal of Hearing Research, 147, 261–74.

Sun, W., Lu, J., Stolzberg, D., Gray, L., Deng, A., Lobarinas, E., & Salvi, R.J. (2009). Salicylate increases the gain of the central auditory system. Neuroscience, 159, 325–334.

Syka, J., & Rybalko, N. (2000). Threshold shifts and enhancement of cortical evoked responses after noise exposure in rats. Journal of Hearing Research, 139, 59–68.

Turner, J.G., & Parrish, J. (2008). Gap detection methods for assessing salicylate-induced tinnitus and hyperacusis in rats. Am J Audiol 17, S185–92.

Wang, H.T., Luo, B., Huang, Y.N., Zhou, K.Q., & Chen, L. (2008). Sodium salicylate suppresses serotonin-induced enhancement of GABAergic spontaneous inhibitory postsynaptic currents in rat inferior colliculus in vitro. Journal of Hearing Research, 236, 42–51.



  

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