Pump Up the Volume: Could Excessive Neural Gain Explain Tinnitus and Hyperacusis?

Abstract

Naturally occurring stimuli can vary over several orders of magnitude and may exceed the dynamic range of sensory neurons. As a result, sensory systems adapt their sensitivity by changing their responsiveness or ‘gain'. While many peripheral adaptation processes are rapid, slow adaptation processes have been observed in response to sensory deprivation or elevated stimulation. This adaptation process alters neural gain in order to adjust the basic operating point of sensory processing. In the auditory system, abnormally high neural gain may result in higher spontaneous and/or stimulus-evoked neural firing rates, and this may have the unintended consequence of presenting as tinnitus and/or sound intolerance, respectively. Therefore, a better understanding of neural gain, in health and disease, may lead to more effective treatments for these aberrant auditory perceptions. This review provides a concise summary of (i) evidence for changes in neural gain in the auditory system of animals, (ii) physiological and perceptual changes in adult human listeners following an acute period of enhanced acoustic stimulation and/or deprivation, (iii) physiological evidence of excessive neural gain in tinnitus and hyperacusis patients, and (iv) the relevance of neural gain in the clinical treatment of tinnitus and hyperacusis.

Inner Hair Cell Loss Disrupts Hearing and Cochlear Function Leading to Sensory Deprivation and Enhanced Central Auditory Gain

“…These findings are consistent with recent reports showing central gain enhancement with various forms of cochlear pathology; however, an unusual feature of carboplatin is that hearing thresholds are largely unaffected by the cochlea pathology (Salvi et al, 1990, 2000b; Sun et al, 2009; Stolzberg et al, 2011; Yuan et al, 2014; Brotherton et al, 2015; Chen et al, 2016). Interestingly, similar perceptual and electrophysiological changes were observed in a recent study examining ouabain treatment in mice, which selectively destroys type-1 SGN (Chambers et al, 2016).…”

Speech Comprehension Difficulties in Chronic Tinnitus and Its Relation to Hyperacusis

“…Answers to the two screening questions for hyperacusis (Schecklmann et al, 2015) were significantly related to speech comprehension in the cocktail party situation, but not to speech comprehension in general. As hyperacusis is presumably due to increased central gain as a consequence of deficient central inhibitory mechanisms (Brotherton et al, 2015), our findings suggest that this inhibitory dysfunction of the auditory pathway has a specific impact on speech comprehension difficulties in the cocktail party situation.…”

Tinnitus with a normal audiogram: Relation to noise exposure but no evidence for cochlear synaptopathy

“…Optimum sensitivity was achieved with high modulation frequencies (∼1 kHz), which limited the influence of more central nuclei. In contrast, the present study used a much lower modulation frequency and likely elicited the responses of higher centers, where the effects of deafferentation might be mitigated by enhanced central gain (Brotherton et al., 2015, Chambers et al., 2016). Hence the present EFR amplitude data must be interpreted with caution.…”