The effects of age on temporal coding in the auditory system

Lead Research Organisation: Lancaster University
Department Name: Psychology

Abstract

Hearing ability deteriorates with age, leading to communication difficulties and a reduced quality of life. Some of these changes are apparent in the audiogram, the standard clinical measure of hearing sensitivity, which describes the sensitivity of the ear to pure tones at different frequencies. However, in addition to the changes that can be detected using standard clinical techniques, it is becoming increasing clear from animal and human studies that a deterioration in auditory function may occur before, or independently from, a significant decline in sensitivity to low-level sounds as measured by the audiogram.

Listeners with clinically normal hearing may experience an age-related decline in their ability to understand speech in noisy environments, an ability that is vital for real-world communication. It has been suggested that this may be due, in part, to a deficit in the ability of nerve fibres to represent the rapid fluctuations in sounds in terms of their synchronised patterns of activation. An age-related deficit in this "temporal coding" has been demonstrated recently in humans using techniques that record the electrical activity of nerve fibres in the auditory brain by attaching electrodes to the scalp. Temporal coding may be important for speech identification per se, but it is thought to be particularly important for segregating speech from interfering sounds. In particular, we rely on fine-grained timing information to separate sounds on the basis of their spatial locations (for example, several people talking at a noisy party).

The neural bases for the age-related decline in temporal coding are unclear, but there are two potential candidates. First, animal studies and post-mortem examinations of human ears suggest that there is a progressive loss in auditory nerve fibres with age, particularly those fibres that represent information at medium-to-high levels. Hence, this loss can occur without a reduced sensitivity to quiet sounds. Second, it is possible that the deficit in temporal coding may be due to a loss of synchrony between nerve fibres. This may occur because age is associated with a patchy degeneration of the fatty sheaths that surround nerve fibres and increase the speed of transmission of nerve impulses.

The proposed research will use a combination of state-of-the-art electrophysiological and listening-test techniques to provide a comprehensive understanding of the neural bases and perceptual consequences of the age-related decline in temporal coding in humans. Our focus will be on listeners with clinically normal hearing, so that we can study these effects in isolation from the effects of dysfunction of the hair cells and other structures in the inner ear that are associated with clinical loss. By testing a large cohort of volunteers across the age range with measures of nerve-fibre function and listening ability with laboratory and "real world" sounds, we will be able to make connections and inferences that are not possible with less ambitious studies. In particular, we will determine whether the age-related temporal coding deficits are due to a loss in nerve fibres, a reduction in nerve fibre transmission speed, or both. We will also be able to determine how the deficit in temporal coding is related to real-world hearing ability on tasks such as speech detection in noise, and musical pitch perception.

The results will provide the basis for a diagnostic test that can identify the neural dysfunction. Early diagnosis of damage, before any deficit is apparent in the audiogram, will allow clinicians to provide personalised healthcare advice, for example, to avoid any situations that will compound the problems, such as exposure to recreational noise. The research will also pave the way for future interventions that may correct for the deficits, for example hearing aids with directional microphones to facilitate speech reception, and drug and stem cell therapies to restore neural function.

Technical Summary

Hearing ability deteriorates with age, leading to communication difficulties, social withdrawal, and a reduced quality of life. Although some of these changes can be measured using the pure tone audiogram, a deterioration in auditory function may occur before, or independently from, a significant increase in audiometric threshold. In particular, there is evidence that the ability of neurons to synchronise their firing to features in the temporal fine structure and temporal envelope of sounds declines with age. A deficit in phase locking may arise from two types of neural dysfunction. First, animal models suggest that the number of synapses between inner hair cells and auditory nerve fibres declines with age. Second, there is evidence for myelin degeneration with age, both in the auditory nerve and the central nervous system. This will reduce axonal conduction speed, potentially leading to a loss in synchrony across fibres.

The proposed research aims to determine the neural bases and perceptual consequences of the decline in auditory temporal coding with age. A single cohort of participants aged 18-70 will take part in a test battery comprising electrophysiological measures of neural function (the auditory brainstem response and the frequency-following response), psychophysical measures of temporal coding, and performance measures related to "real-world" tasks such as detecting speech in noise, and musical pitch perception. By combining information from the different measures we will be able to test hypotheses regarding the underlying neural basis of the temporal coding deficits, and regarding the impact of these deficits on real-world hearing ability. We will also determine the contribution of noise exposure to the age-related decline.

Planned Impact

Beneficiaries of the research include:

1. Individuals experiencing an age-related decline in hearing ability.

An understanding the neural basis of the temporal coding decline will allow earlier and more sensitive diagnosis of hearing loss, and personalised healthcare advice, to help prevent further loss (~5-10 yr impact).

An understanding the neural basis of the temporal coding decline will also pave the way for potential treatments such as noise reduction / directional hearing aids (~5-10 year impact) and pharmaceutical and stem cell therapies (~15-30 year impact).

2. Healthcare providers / clinicians

Benefit through improved diagnosis of hearing disorders, and ability to offer appropriate advice and counselling to those that report difficulties hearing in noisy situations but are currently told that they have "normal" hearing (~5-10 yr impact).

3. Hearing-aid manufacturers

Potentially benefit through an expansion of the market to individuals with sub-clinical loss, via devices such as directional hearing aids and FM systems (~5-10 year impact).

4. Pharmaceutical companies

Potentially benefit through development of drug therapies to prevent and treat age-related neural degeneration (~15-30 year impact).

5. UK economy

Management of hearing disorders will improve individual productivity, and reduce unemployment due to hearing disability (~10-15 year impact).
 
Description The overall aim of the project was to understand the age-related changes in the neural representation of the waveform of sounds over time ("temporal coding"), changes that occur before substantial changes in standard clinical hearing tests (e.g. the audiogram) are apparent. As originally planned, we tested 100 listeners over a wide age range (18-74), using a number of electrophysiological measures of nerve function, listening tests, and tests of cognitive function. The study involved over 1400 hours of data collection, and had high levels of experimental control.

Listed below are our four main research questions from the original grant application, together with a description of our findings (although analysis is ongoing).

1. Are temporal coding deficits with ageing a consequence of a loss of nerve fibres and/or a change in neural transmission speed?

We found some evidence for an age-related loss of auditory nerve fibres at high frequencies, but there was little evidence for a loss at lower frequencies. We did find good electrophysiological and listening-test evidence for a decline in neural coding in the central auditory system, consistent with neural loss. There was also evidence for an increase in neural transmission speed.

2. At what age do these deficits become apparent?

Several of our measures of temporal coding showed age-related declines across the age range we studied; these deficits were apparent even after accounting for audiometric hearing threshold and age-related declines in cognitive function. The losses seem to be progressive with age, with no evidence for a more rapid deterioration for older listeners.

3. What are the impacts of temporal coding deficits on performance on real-world tasks?

There were no relations between electrophysiological measures and speech-in-noise ability. However, some of the listening tests measuring temporal coding were associated with speech perception ability.

4. To what extent are the temporal coding deficits related to noise exposure over the lifetime?

Lifetime noise exposure was unrelated to temporal coding deficits, after taking into account the effects on audiometric threshold. Age is a much stronger predictor of these deficits. This is an important finding of our research - the effect of age on temporal coding is much more than just the accumulation of noise damage over the lifespan.

Overall, our research has shown that ageing is associated with progressive declines in auditory temporal coding that cannot be explained by clinical hearing measures, by age-related declines in cognitive function, or by lifetime noise exposure. However, the impact on real-world hearing is unclear from our results.
Exploitation Route The research highlights the importance of considering auditory function "beyond the clinical audiogram" when assessing age-related hearing deficits. Several of our tests show promise as clinical measures of temporal coding, that could be used to better understand the hearing difficulties experienced by an individual. This will facilitate future interventions that may correct for the deficits, for example hearing aids with directional microphones to aid speech reception, and drug and stem cell therapies to restore neural function.
Sectors Electronics,Healthcare,Manufacturing, including Industrial Biotechology,Pharmaceuticals and Medical Biotechnology

 
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