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Identifying the Role of the Spiral Ganglion in Speech Discrimination

Nyatepe-Coo, Efoe F.; Parker, Mark A. PhD

doi: 10.1097/01.HJ.0000466874.97809.89
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Mr. Nyatepe-Coo, left, is a final-year audiology student at Northwestern University and an audiology fellow at Steward St. Elizabeth's Medical Center in Boston. Dr. Parker, right, is director of audiology at Steward St. Elizabeth's Medical Center and assistant professor of otolaryngology at Tufts University School of Medicine in Boston.



Pure-tone audiometry (PTA) is the standard behavioral assessment of hearing, enabling the determination of the degree, type, and configuration of a hearing loss. However, this technique is unable to identify intracochlear etiology or the sight of lesion of a sensorineural hearing loss, which is essential to understanding the otopathology causing the condition.



The incompleteness of standard audiometry's auditory system assessment is demonstrated in the clinic when we see patients who produce similar audiograms but exhibit different levels of hearing impairment.



One of the most common complaints expressed by hearing aid patients is their difficulty discriminating speech in the presence of background noise. A more complete understanding of the functional roles of inner hair cells, outer hair cells, and spiral ganglion neurons, which connect hair cells to the brainstem, would lead to better assessment and treatments for sensorineural hearing loss.

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It seems we have come full circle regarding our understanding of the cellular basis of audition in the cochlea. As early as the 1950s, the spiral ganglion was proposed to play the primary role in the ability to understand speech, leading to the development of the cochlear implant, which is arguably the most clinically successful biotechnological implant available in any field.

However, the discovery of otoacoustic emissions in the 1970s and outer hair cells’ motile abilities in the 1980s led to a paradigm shift that attributed to outer hair cells a primary role in the fine-tuning of the speech signal essential for understanding spoken language. More recently, several strong lines of evidence in animal models have suggested a significant part for the spiral ganglion to play in speech understanding, particularly in the presence of background noise.

Moderate noise exposure that causes a loss of up to 50 percent of spiral ganglion cells results in no permanent changes in distortion product otoacoustic emission (DPOAE) or auditory brainstem response (ABR) threshold, animal studies show ( J Neurosci 2009;29[45]:14077-14085; J Assoc Res Otolaryngol 2011;12[5]:605-616; J Neurophysiol 2013;110[3]:577-586 This research highlights the evidence that damage to the peripheral auditory system is not apparent in threshold-based assessments.

In contrast to threshold-based assessments, the amplitude of wave I of the ABR is correlated with the number of surviving spiral ganglion neurons, with smaller amplitudes indicating greater neuronal loss, animal studies show. The reduction in wave I amplitude is observed even in the absence of any permanent shift in DPOAE or ABR threshold ( J Neurosci 2009;29[45]:14077-14085; J Assoc Res Otolaryngol 2011;12[5]:605-616

These studies suggest the importance of the spiral ganglion's role in speech discrimination in noise. Unfortunately, speech discrimination is very difficult to measure in animal studies, so confirmation of this hypothesis has been elusive.

Speech Perception Ability in Noise Is Correlated with Auditory Brainstem Response Wave I Amplitude

Bramhall N, Ong B, Ko J, Parker M

J Am Acad Audiol

Accepted Jan. 2015

In a paper that was recently accepted for publication in the Journal of the American Academy of Audiology, our group sought to determine whether the spiral ganglion plays a role in speech discrimination in humans.

We estimated spiral ganglion density using the wave I amplitude of the auditory brainstem response and compared these responses with variables such as age, audiometric thresholds, and speech discrimination in quiet and in competing background noise. Linear mixed models were used to analyze whether wave I amplitude had significant effects on these variables.

We found that reduced ABR wave I amplitudes (0.267 µV or less) are related to increased age, which is consistent with the results of animal and human temporal bone studies showing an inverse relationship between the number of spiral ganglion neurons and age ( J Neurophysiol 1996;76[4]:2799-2803; J Assoc Res Otolaryngol 2011;12[6]:711-717

However, aging did not significantly affect speech discrimination in quiet or in noise, suggesting that factors such as age-related cognitive decline or memory loss did not have a significant influence on speech discrimination in noise in the participants tested.

Importantly, we also found that lower wave I amplitudes are correlated with decreased speech-in-noise performance, with the greatest effects seen in people with worse hearing (PTA 25 dB HL or greater).

No correlation was seen between wave I amplitudes and speech discrimination in quiet, suggesting that the spiral ganglion plays a role in speech discrimination in the presence of background noise.

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Literature from animal studies supports the functional role of a healthy spiral ganglion in speech discrimination in the presence of complex auditory stimuli. Spiral ganglion fibers are functionally classified as low-spontaneous-rate (SR) fibers, associated with high absolute thresholds, or high SR fibers, associated with low absolute thresholds ( J Acoust Soc Am 1978;63[2]:442-455

Previous animal studies also suggest that low SR fibers are more vulnerable to noise damage and aging than high SR fibers ( J Neurophysiol 1996;76[4]:2799-2803; J Neurophysiol 2013;110[3]:577-586 The absence of any permanent threshold shift and the lack of a significant relationship between ABR wave I amplitude and speech discrimination in quiet can be attributed to the presence of the more robust high SR fibers, which encode low absolute thresholds and speech in quiet.

However, in the presence of noise, the responses of the high SR fibers become saturated ( J Assoc Res Otolaryngol 2011;12[1]:71-88, leaving the low SR fibers to encode the information required to discriminate speech in background noise. In our study, the decline in speech discrimination in noise performance as ABR wave I amplitude decreased may be attributed to loss of these low SR fibers.

Our findings strongly suggest that people with elevated pure-tone thresholds and lower wave I amplitudes are more likely to experience difficulty with speech understanding in noise due to loss of spiral ganglion neurons. In the clinic, these patients should be counseled on communication strategies to minimize the effect of background noise and provided with hearing aids that have aggressive noise-reduction features.

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