The Role of the Efferent System in Auditory Performance in Background Noise

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The Role of the Efferent System in Auditory Performance in Background Noise Utah Speech-Language Hearing Association, 2015 Skyler G. Jennings Ph.D., Au.D. CCC-A

Outline Hearing in a noisy background Normal vs. hearing impaired listeners The medial olivocochlear (MOC) system Effects on basilar membrane responses Time course of the MOC reflex The effects of the MOC reflex on perception Improved signal-to-noise ratio Improved peak-valley contrast Perceptual evidence for the role of the MOC reflex Auditory masking Auditory intensity discrimination Speech-in-noise performance Clinical applications Conclusions

Learning objectives Understand the anatomy and physiology of the auditory efferent system Understand the role of the medial olivocochlear reflex in regulating outer hair cell amplification Understand recent research on how the auditory efferent system may be dysfunctional in listeners with cochlear hearing loss, leading to altered auditory perception.

Hearing in a noisy background Normal vs. hearing impaired listeners

Listening in background noise is difficult for hearing-impaired individuals

Normal-hearing listeners do quite well understanding speech in a noisy background

Many factors may contribute to effectively understanding speech in a noisy background Peripheral factors Audibility Clear signal (healthy OHCs/IHCs) Redundancy among neural pathways Efferent function

Many factors may contribute to effectively understanding speech in a noisy background Central factors Auditory stream segregation Pitch Common fate Location Decoding the speech message from an impoverished signal Brain noise may increase with age and HI

Medial olivocochlear anatomy / physiology A brief review

Medial olivocochlear neurons innervate the outer hair cells from Maison and Liberman (2000) 10

Innervation of OHCs is primarily efferent OHC

Medial olivocochlear reflex pathway

Detour: review of cochlear mechanics

The basilar membrane exhibits tonotopic traveling motion Traveling wave demo from Rick Rabbitt in bioengineering

The response of the cochlea depends on the state of the outer hair cells When OHCs are impaired, the cochlear response is: Insensitive (high thresholds) Broadly tuned Linear When OHCs are healthy, the cochlear response is: Sensitive Sharply tuned Compressive *Outer hair cells amplify BM motion and sharpen the peak of the traveling wave.

Active and passive cochlear processes Cochlear motion is the sum of passive and active processes- Passive process: motion due to the physical properties of the basilar membrane (e.g., stiffness and mass) Active process: amplification introduced by the OHCs to motion of the basilar membrane. *The active process is decreased with sensorineural hearing loss and absent after death.

The interaction of passive and active processes results in cochlear compression. Signal coming out of cochlea This graph of the basilar membrane output as a function of stimulus level is called a cochlear input/output function. Signal going in to the cochlea 17

Compression facilitates a large perceptual dynamic range (but ) Modified from Ruggero et al (1997) Compressed Output Large Range of Input Levels

Byproducts of compression: reduced SNR Speech Noise Poorer post-cochlear SNR N S *Cochlear compression may limit speech understanding in background noise. Speech Noise Favorable input SNR

The speech envelope is important for understanding speech Speech envelope: has gross fluctuations characterized by peaks and valleys *Early cochlear implant studies showed that the speech envelope must be faithfully coded for speech understanding (e.g., Shannon, 1995).

Byproducts of compression: reduced peak-valley contrast Peak Valley Poorer post-cochlear peak-valley contrast *Cochlear compression may limit the contrast between speech peaks and valleys of the speech envelope. This may negatively influence speech understanding. Peak Valley V P Favorable input peak-valley contrast

Summary of cochlear mechanics Cochlear motion is determined by active and passive processes The interaction of active and passive processes results in cochlear compression Compression may lead to a reduced post-cochlear SNR Compression may lead to a reduced post-cochlear peak-valley contrast

Back to MOC efferents Nature s solution to avoiding the byproducts of cochlear compression

Efferent (MOC) Effects on Basilar Membrane Responses (Cooper and Guinan, 2006) Brainstem slice where MOC neurons originate MOC neurons stimulated by electric shock MOC neurons connect to OHCs Basilar membrane motion measured

Efferent (MOC) Effects on Basilar Membrane Responses (Cooper and Guinan, 2006) (no shocks) (shocks) The influence of stimulating the MOC bundle is to reduce the amplification provided by OHCs. *MOC stimulation results in decreased basilar membrane displacement, especially at low sound levels

The MOC reflex is elicited by sound and its response grows with sound level

The MOC timecourse includes onset, delay, build-up, offset delay, and decay stages Onset delay: ~25 ms Build-up: ~200 ms Offset delay: ~25 ms Decay: ~100-200 ms *This suggests that there is a slight lag between when the stimulus is turned on and off and when the MOC system effects Based on Backus and Guinan (2006)

MOC stimulation decompresses the cochlear response and may improve SNR Signal coming out of the cochlea Without the MOC (MOC-): Post-cochlear SNR is small Post-cochlear contrast is poor With the MOC (MOC+): Post-cochlear SNR is improved Post-cochlear contrast is greater Signal going in to the cochlea

Potential roles of the MOC reflex in perception Reduction in masking by improving SNR (Guinan, 2006) Facilitate selective attention (Scharf et al, 1997) Protection against noise-induced hearing loss (Maison and Liberman, 2000) Protection against loss of spiral ganglion neurons (Liberman and Maison, 2014)

Listeners with sensorineural hearing loss may have reduced MOC function Damage to cochlear structures disrupts the MOC pathway This may reduce the ability of the MOC reflex to regulate OHC amplification This suggests that the hearing-impaired system may have difficulty adapting to a noisy background.

Interim conclusions Sensorineural hearing loss results in difficulty listening in background noise Hearing aids currently do not address this issue The MOC efferent system regulates the amplification of the outer hair cells Regulation of OHC amplification can improve SNR and peak-valley contrast Listeners with sensorineural hearing loss may lose partial function of the MOC reflex, resulting in the inability to adapt to a noisy background

MOC effects in human perception

Perceptual studies on the MOC reflex Simple stimuli Masking Intensity increment/decrement detection Complex stimuli Speech in noise

Framework for masking experiments Assumption #1: The probe is detected through an auditory filter centered on the cochlear location that responds best to the probe Assumption #2: The probe energy through the auditory filter must be greater than the masker energy through the same filter by some criterion amount (criterion postcochlear SNR). Auditory Filterbank criterion post-cochlear SNR probe masker 34

onset A perceptual task that takes advantage of the sluggish start of the MOC reflex: Masking Masking Stimulus Basilar Membrane Response onset Temporal center temporal center MOC Time course

Probe Level (db SPL) Detection threshold improves by up to 20 db when the probe is moved from the onset to the temporal center 80 70 Improvement called overshoot 60 onset 50 40 Temporal center 30 20 10 Normal Hearing Listeners 0 Onset 60 db SPL Masker Temporal Center

Probe Level (db SPL) Hearing impaired listeners show little or no improvement in threshold when the probe is moved (i.e, small overshoot) 80 70 Small overshoot 60 onset 50 40 Temporal center 30 20 10 Hearing-Impaired Listeners 0 Onset 60 db SPL Masker Temporal Center

Overshoot in NH listeners who ingest aspirin show very little improvement in threshold Before aspirin Days during aspirin regimen Weeks after aspirin High aspirin ingestion produces a temporary hearing loss by temporarily impairing the OHCs Overshoot decreases during an aspirin regimen, while temporary hearing loss increases McFadden and Champlin (1990)

Overshoot can be explained with an auditory model that includes MOC effects OHC component of the model was used to manually regulated OHC amplification Jennings et al (2011)

Model predicts reduced overshoot in HI listeners Normal hearing simulations Hearing impaired simulations Jennings et al (2011)

MOC reflex magnitude and growth rate may be reduced in HI listeners Remember MOC strength depends on sound level OHC amplification is reduced at a rate of -1 db/db with increasing masker level in YNH and ONH subjects. OHC amplification is reduced changes at a slower rate in OHI subjects (-0.56 db/db). On average the largest reduction in OHC amplification was roughly -45 db in normal-hearing listeners and about -25 db in hearing-impaired listeners. Jennings et al (in preparation)

Framework for decrement detection experiments Assumption #1: The decrement is detected through an auditory filter centered on the cochlear location that responds best to the pedestal Assumption #2: The peakvalley contrast through the auditory filter must reach some criterion amount (criterion PV contrast). Auditory Filterbank criterion peak-valley ratio decrement 42

A perceptual task that takes advantage of the sluggish start of the MOC reflex: Decrement Detection onset Decrement Stimulus Basilar Membrane Response Temporal center MOC Time course

Decrement detection improves as the decrement is move to the temporal center of the pedestal Lower numbers = better performance Chen and Jennings, ARO 2015

Summary of simple perceptual experiments Detection thresholds improve as a tone is moved to a center of a noise This improvement only occurs in NH listeners This improvement can be explained by an increase in SNR during the course of the masker Decrement detection threshold improve as the decrement is moved to the center of the pedestal This improvement can be explained by a relatively better peak-valley contrast.

MOC effects in speech perception Contralateral suppression of OAEs is a technique for assessing MOC strength Kumar and Vanaja (2004) found a significant correlation between speech identification and contralateral suppression of OAEs. They speculated that the relatively better speech identification in individuals with stronger OAE inhibition was due to the MOC reflex regulating OHC amplification

MOC effects in speech perception (cont ) ABR latency shift in the presence of noise can predict the degree of masking Longer latencies more masking ABR latency shift and consonant discrimination was measured in the same listeners Consonant were discriminated on a continuum from ba to ga The consonant discrimination thresholds is the distance along the continuum before ba is clearly distinguished from ga Lower scores are better. Consonant discrimination is correlated with ABR latency shift This latency shift was also correlated with contralateral suppression of OAEs The authors concluded that the unmasking effect may be due to the MOC regulation of OHC amplification de Boer et al. (2012)

Potential applications and conclusions

Potential applications: MOC inspired noise reduction Speech in noise with linear compression Speech in noise with MOC-inspired adjustment in OHC amplification Speech in noise sound clip from: http://www.ece.rochester.edu/~zduan/is2012/examples.html

Conclusions Robust speech perception in noise may be facilitated by the MOC reflex in NH listeners The MOC reflex improves speech understanding in noise by improving the SNR and increasing peak-valley contrast HI listener may suffer from a partially dysfunctional MOC reflex Behavioral studies in masking, decrement detection, and consonant identification support the potential role of the MOC reflex in speech perception An MOC inspired processing algorithm may improve the benefit derived from hearing aids and cochlear implants when listening to speech in a noisy background

references Backus, B. C., & Guinan, J. J., Jr. (2006). Time-course of the human medial olivocochlear reflex. J Acoust Soc Am, 119(5 Pt 1), 2889-2904. Bacon, S. P. (1990). Effect of masker level on overshoot. J Acoust Soc Am, 88(2), 698-702. Cooper, N. P., & Guinan, J. J., Jr. (2006). Efferent-mediated control of basilar membrane motion. J Physiol, 576(Pt 1), 49-54. Guinan, J. J., Jr. (2006). Olivocochlear efferents: anatomy, physiology, function, and the measurement of efferent effects in humans. Ear Hear, 27(6), 589-607. Jennings, S. G., Heinz, M. G., & Strickland, E. A. (2011). Evaluating adaptation and olivocochlear efferent feedback as potential explanations of psychophysical overshoot. J Assoc Res Otolaryngol, 12(3), 345-360. doi: 10.1007/s10162-011-0256-5 Killion, M. C., & Niquette, P. A. (2000). What can the pure-tone audiogram tell us about a patient's SNR loss?. The Hearing Journal, 53(3), 46-48. Neely, S. T., & Kim, D. O. (1983). An active cochlear model showing sharp tuning and high sensitivity. Hearing Research, 9(2), 123-130. Maison, S., Micheyl, C., Andeol, G., Gallego, S., & Collet, L. (2000). Activation of medial olivocochlear efferent system in humans: influence of stimulus bandwidth. Hear Res, 140(1-2), 111-125. Maison, S. F., Usubuchi, H., & Liberman, M. C. (2013). Efferent feedback minimizes cochlear neuropathy from moderate noise exposure. J Neurosci, 33(13), 5542-5552. doi: 10.1523/JNEUROSCI.5027-12.2013 McFadden, D., & Champlin, C. A. (1990). Reductions in overshoot during aspirin use. J Acoust Soc Am, 87(6), 2634-2642. Ruggero, M. A., Rich, N. C., Recio, A., Narayan, S. S., & Robles, L. (1997). Basilar-membrane responses to tones at the base of the chinchilla cochlea. J Acoust Soc Am, 101(4), 2151-2163. Scharf, B., Magnan, J., & Chays, A. (1997). On the role of the olivocochlear bundle in hearing: 16 case studies. Hear Res, 103(1-2), 101-122. Shannon, R. V., Zeng, F. G., Kamath, V., Wygonski, J., & Ekelid, M. (1995). Speech recognition with primarily temporal cues. Science, 270(5234), 303-304. Spoendlin, H. (1985). Anatomy of cochlear innervation. American journal of otolaryngology, 6(6), 453-467. Warr, W. B. (1992). Organization of olivocochlear efferent systems in mammals. In The mammalian auditory pathway: Neuroanatomy (pp. 410-448). Springer New York.