The Auditory Brain and Age-Related Hearing Impairment

By Jos J. Eggermont

The Auditory Brain and Age-Related Hearing Impairment provides an overview of the interaction between age-related hearing impairments and cognitive brain function. This monograph elucidates the techniques used in the connectome and other brain-network studies based on electrophysiological methods. Discussions of the manifestations of age-related hearing impairment, the causes of degradation of sound processing, compensatory changes in the human brain, and rehabilitation and intervention are included. There is currently a surge in content on aging and hearing loss, the benefits of hearing aids and implants, and the correlation between hearing loss, cognitive decline and early onset of dementia.

Given the changing demographics, treatment of age-related hearing impairment need not just be bottom-up (i.e., by amplification and/or cochlear implantation), but also top-down by addressing the impact of the changing brain on communication. The role of age-related capacity for audio-visual integration and its role in assisting treatment have only recently been investigated, thus this area needs more attention.

• Relates the techniques used in the connectome and other brain-network studies to the human auditory-cortex and age-related hearing loss research findings
• Examines the side effects of age-related hearing impairment and their impact on the quality of life for the elderly
• Evaluates the importance of multi-modal means in the rehabilitation of the elderly with hearing aids and cochlear implants
• Discusses the role of neurostimulation and various training procedures to halt, or potentially reverse, cognitive decline in the elderly

• Language: English
• Publisher: Academic Press
• Release date: Jan 3, 2019
• ISBN: 9780128155455

Jos J. Eggermont

Dr. Jos J. Eggermont is an Emeritus Professor in the Departments of Physiology and Pharmacology, and Psychology at the University of Calgary in Alberta, Canada. Dr. Eggermont is one of the most renowned scientists in the field of the auditory system and his work has contributed substantially to the current knowledge about hearing loss. His research comprises most aspects of audition with an emphasis on the electrophysiology of the auditory system in experimental animals. He has published over 225 scientific articles, authored/edited 10 books, and contributed to over 100 book chapters all focusing on the auditory system.

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hearing

Section I

Manifestations of Age-Related Hearing Impairment

Outline

Chapter 1 Hearing and the Auditory Brain in the Elderly

Chapter 2 Age-Related Changes in Auditory Sensation

Chapter 3 Age-Related Changes in Auditory Perception

Chapter 4 Aging, Cognition, and Dementia

Chapter 1

Hearing and the Auditory Brain in the Elderly

Abstract

Beyond auditory processing, cognitive processing is crucial to the basic functions of listening, comprehending, and communicating. Thus, the age-related hearing impairment–associated changes occur in at least three levels, including the peripheral auditory system, central auditory system, and cognitive functions. An important aspect is that auditory stimuli, especially to voice, activate neurons in the prefrontal and other nonauditory areas. These areas are often implicated as covariants with declining speech discrimination. It is thus clear that the auditory brain extends well beyond the classical auditory areas in the temporal lobe. In hearing-impaired geriatric patients, the age-related declines of peripheral and central auditory processing interact with the diminished cognitive functions and support, leading to reduced auditory perception of speech.

Keywords

Hearing loss; speech understanding; auditory evoked potentials; lifespan; tinnitus; brain atrophy; attention

1.1 Introduction

Age-related hearing impairment (ARHI), an invisible handicap, combines hearing loss (in the ear) and hearing problems, for example, in speech understanding (in the brain). ARHI is a condition with three underlying characteristics: (1) Reduced auditory sensation as a result of hearing loss, resulting in reduced input to the central auditory nervous system. (2) Degradation of auditory perception, resulting from frequency-dependent gain changes in the central auditory system synapses as well as a dysfunction in auditory temporal processing. This manifests itself in decreased speech understanding, especially in background noise. (3) Changes in nonauditory brain structures involved in attention, working memory, and executive functions. These cognitive changes affect auditory perception, especially in more demanding conditions, such as noisy or babble environments. Consequently, hearing impairment tends to isolate people from friends and family because of a decreased ability to communicate; as such, untreated ARHI may have considerable negative social, psychological, cognitive, and health effects (Li et al., 2014). We will discuss these three defining characteristics in detail in Chapters 2–4.

High-frequency hearing loss is one of the hallmarks of sensory aging. Zwaardemaker (1891), a physiology professor in Utrecht, the Netherlands, was the first to describe and measure this, using Galton whistles tuned to various high frequencies. The Galton whistle, invented by Sir Frances Galton (1822–1911), was one of the earliest devices used in testing hearing. The Galton whistle can be adjusted to produce very high-frequency sounds between 5 and 42 kHz, and was used by its inventor to test the limits of hearing in the dogs he met on his walks in London’s Hyde Park. Later, Zwaardemaker (1897) coined the term presbycusis. Bunch (1929) was the first to use an audiometer to measure hearing loss associated with aging, thereby replacing the Galton whistle and other instruments such as the often-used monochord, a single-string tunable instrument (Mollison, 1917).

One of the earlier studies (Otto and McCandless, 1982) into the potential loci of ARHI used a battery of auditory tests, including impedance measures, speech discrimination tests, synthetic sentence identification, compressed speech, two measures of tone decay, the short increment sensitivity index, a digit span test, and auditory brainstem response (ABR) audiometry (see Appendix). Decrease in synthetic sentence identification was the most consistent aging effect among the outcomes of central auditory function tests. The ABR revealed some prolonged interpeak latencies, potentially suggesting mild brainstem abnormalities. Otto and McCandless (1982) concluded that peripheral as well as central auditory disorders frequently accompany senescence. Using a comparable test battery, Arlinger (1991) also found that, in contrast to young adults with normal hearing and those with cochlear hearing loss, the elderly showed a mixture of characteristics typical of cochlear, retrocochlear, and central lesions. Later we will see that in more recent studies of healthy aging one rarely finds retrocochlear lesions and often only modest cochlear lesions, whereas the central lesions are typical of the cognitive variety, which do not show up in the ABR. The ABR is however useful in detecting temporal processing disorders (Chapter 5).

In this chapter I will introduce the general effects of auditory aging by describing lifespan changes in hearing loss, changes in the perception of speech, and structural and functional changes in auditory cortex. I then introduce nonclassical auditory-responsive cortical areas, which will be relevant because of their changes in aging, and involvement in cognitive processes. Finally, I will address the diverging paths of hearing loss and tinnitus prevalent across the lifespan.

1.2 Tracking Age-Related Hearing Impairment

1.2.1 Increasing Hearing Loss

Let us start with a definition of presbycusis as used in the late 1960s (Spoor, 1967): Presbycusis is the phenomenon that the threshold of hearing of people with otologically normal ears increases with age. It has to be realized, that this is not a pure physiological phenomenon, but that this is influenced to a certain degree by the [noisy] nature of Western civilization. To quantify this progression of hearing loss across the lifespan, my colleague Spoor (1967) compiled information from eight large published studies. Epidemiological information on these studies is presented in Table 1.1. In Fig. 1.1 the relative changes for 4 kHz with age are shown for males with reference to their hearing at age 20–25 years.

Table 1.1

Figure 1.1 Data points (median values) derived from eight large studies showing hearing level in dB at 4000 Hz as a function of age with respect to the hearing level in the 20–25 year-old age group in the same investigations. For the characteristics of the populations used and indicated by name, see Table 1.1. Source: From Spoor, A., 1967. Presbycusis values in relation to noise induced hearing loss. Audiology 6, 48–57, reprinted by permission of the publisher (Taylor & Francis Ltd, http://www.tandfonline.com).

Interestingly, the data indicated by the ×–× symbols in Fig. 1.1 represent median values for men from a large industrial noise-exposed group (Glorig and Nixon, 1962), whereas the +–+ data symbols represent median values from a large group of, likely less-exposed, professionals attending the 1954 Wisconsin State Fair (Glorig, 1957). These two particular studies illustrate an overall effect of occupational noise, on the amount of hearing loss, but they also showed the absence of an effect on the rate of hearing loss change with age. The other studies included in Fig. 1.1 likely are from populations with varying degrees of occupational hearing loss as they fall mostly in between the two extremes just presented.

To introduce the differences in age-related hearing loss between males and females, we present data from a recent epidemiological study covering 15,606 participants up to 85 years of age, based on the Korea National Health and Nutrition Examination Survey 2010–12 (Park et al., 2016). Hearing thresholds of 3, 4, and 6 kHz showed a statistically significant difference between both genders for people older than 30 years of age, with the 4 kHz frequency showing the largest difference. The hearing thresholds for all the tested frequencies became worse with increasing age (Fig. 1.2), in close agreement with the Spoor’s (1967) data compilation.

Figure 1.2 Gender difference of the mean hearing threshold in proportion to age at 0.5 kHz (A), 1 kHz (B), 2 kHz (C), 3 kHz (D), 4 kHz (E), and 6 kHz (F) frequencies (highly screened population, n = 33,011,778 ears). At 0.5, 1, and 2 kHz, no difference in the mean threshold level was found between males and females. However, at 3, 4, and 6 kHz, the mean threshold levels for males are worse than the levels for females. Among the three frequencies, the most significant difference of the mean threshold level between males and females with the same age occurs at 4 kHz. Source: From Park, Y.H., Shin, S.-H., Byun, S.W., Kim, J.Y., 2016. Age- and gender-related mean hearing threshold in a highly-screened population: The Korean National Health and Nutrition Examination Survey 2010–2012. PLoS ONE 11 (3), e0150783. doi:10.1371/journal.pone.0150783.

The data illustrate the very similar changes in hearing for men and women for the lower frequencies (Fig. 1.2A–C), but also the potential effect of more noise exposure in men compared to women for higher frequencies starting at 3 kHz, but especially pronounced at 4 kHz (Fig. 1.2D–F). Hoffman et al. (2012) had found that median thresholds for men across all frequencies except at 1 kHz are lower (better) in the 1999–2006 National Health and Nutrition Examination Survey compared with 1959–62. Results for women were similar. The prevalence of hearing impairment in older adults, age 70 years (65–74 years), was lower in 1999–2006 compared with 1959–62, consistent with earlier findings for younger adults. This potentially resulted from increased awareness of the effects of occupational noise with time.

The above-cited studies did not cover people older than 85 years of age. What happens with the middle and inner ear beyond that age? Mao et al. (2013) measured middle-ear impedance, pure-tone behavioral thresholds, and distortion-product otoacoustic emissions (DPOAEs) from 74 centenarians living in the city of Shaoxing, China. DPOAEs originate from the active transduction process of cochlear outer hair cells (OHCs; Chapter 2). Their data showed that most >100-year-old participants had a reduced static compliance of the tympanic membrane, suggesting some conductive hearing loss. Pure-tone audiometry showed that more than 90% suffered from moderate to severe (41–80 dB) hearing loss below 2000 Hz, and profound (≥81 dB) hearing loss at 4000 and 8000 Hz. This indicates a disproportional large threshold increase at frequencies below 2 kHz compared to the values for 85-year-olds in Fig. 1.2. DPOAEs were undetectable in the majority of centenarians, suggesting severe OHC loss. Liu et al. (2015) confirmed these findings in a study of 54 centenarians from North China, and noted that only a few centenarians had normal levels of speech detection scores.

1.2.2 Decreasing Speech Understanding

In the 1960s, it was not well known how background speech disrupted perception of the target speech in people with hearing impairment. Carhart and Tillman (1970) were pioneers in measuring the discrimination for monosyllables in a background of competing sentences in the same ear. There were two groups (n = 6 each) with normal hearing and conductive hearing loss, respectively, and two groups (n = 6 each) with similar sensorineural hearing loss but differing in speech discrimination in quiet (89.7% and 66.3%). They found that persons with conductive loss functioned as well as the normal-hearing subjects in the speech test. However, the people with sensorineural loss, regardless of their speech discrimination in quiet, found the competing-speech sentences disturbing. The disruption of their speech understanding was equivalent to having the masking efficiency of the competing sentences enhanced from 12 to 15 dB compared to that in the other two groups. Thus an additional handicap may be imposed by sensorineural pathology. Namely, such a pathology not only changes hearing thresholds and often impairs intelligibility in quiet but can also disturb the ability to overcome masking when in complex environments containing other sounds, particularly speech. This was further analyzed in depth by Plomp (1978) and will be presented in some detail in Chapter 3.

Investigating speech discrimination in terms of the 50% discrimination score, also called the speech reception threshold (SRT), Mazelová et al. (2003) compared 30 elderly (mean age = 75.7 years) and 30 young (mean age = 23.1 years) people. They found that the SRT changed abruptly in the elderly when the pure-tone average (PTA) for 0.5–2 kHz increased above 10 dB and then increased linearly with hearing loss (cf. Fig. 5.3). Although in this study there were only a few young participants with PTA0.5–2 kHz > 10 dB hearing level (HL), the data suggested that hearing loss in the young had less of an effect on the SRT. They also found an average shift in the SRT of 24.6 dB between the young and the elderly that translated to 0.47 dB/year, and was significantly larger than the mean 17 dB drop in PTA (0.32 dB/year). Mazelová et al. (2003) suggested that presbycusis represents a combination of deteriorated function in both the auditory periphery and the central auditory system, reflecting closely the suggestions of Carhart and Tillman (1970).

Gates et al. (2008) compared the age-dependent rates of change in measures of peripheral and central aspects of the auditory system of 241 participants aged 71–96 years. As a measure of cochlear function they used DPOAEs to assess OHC function, and PTAs both at 1, 2, and 3 kHz. As measures of central function they recorded ABRs, middle latency responses (MLRs), and cortical auditory evoked potentials (CAEPs), and a competing-speech test. The Appendix describes details about these electrophysiological responses, and Chapter 9 presents more extensive age-related electrophysiological findings. Gates et al. (2008) found that DPOAE thresholds increased by 0.34 dB/year, whereas the PTAs increased by 0.5 dB/year, which is quite a bit larger than in the Mazelová et al. (2003) study. This likely reflects differences in the particular cohorts studied, which is a general confound in cross-sectional studies. The latency of the ABR wave V, and the amplitudes of the MLR (the Pa component) and CAEP (P2 component) did not vary with age. The mean synthetic sentence identification test scores with competing speech in the same ear dropped 1.7% per year. After adjustment for the decrease in hearing threshold level with age, the decline in synthetic sentence identification test was still significant. Gates et al. (2008) concluded that changes in central auditory functions are a prominent component of presbycusis.

A more recent study parceled out effects of hearing loss from effects of aging on speech discrimination in noise (Billings et al., 2015). The effects of hearing impairment on SNR50 (i.e., the SRT in noise) were estimated to be about 12 dB; that is, the 50% speech understanding point on the psychometric function for the old hearing-impaired group is 12 dB to the right of the 50% point on the old normal-hearing psychometric function (Fig. 1.3). Pure age effects obtained by comparing SNR50 in the old normal-hearing group with the young normal-hearing one were only ~2 dB. Note that this minor shift of the SRT curve induced by pure aging still represents ~15% less speech understanding at this signal-to-noise ratio (SNR) compared to the young normal-hearing controls. Thus, the magnitude of hearing impairment effects at the 50% point of the psychometric functions (older normal hearing vs older hearing impaired) was about five to six times greater than the magnitude of age effects in young vs older normal-hearing participants. In addition, the older hearing impaired never reached more than 80% discrimination at favorable SNRs, whereas the older normal hearing performed not significantly less at high SNRs. We are still missing here a comparison between young normal hearing and young people with hearing loss for a pure hearing impairment effect not confounded with aging, as it is likely that these effects do not add