In 1977, Konkle, Beasley, and Bess pub- lished a ... A Tribute to Fred H. Bess: 40 Years of Influence in ..... imize audibility differences between young and.
The Complexity of Auditory Aging Brad A. Stach, Ph.D.,1 Benjamin W. Y. Hornsby, Ph.D.,2 Mia Alexandra Lee Rosenfeld, Ph.D.,2 and Albert R. DeChicchis, Ph.D.3
ABSTRACT
Age-related decline in hearing is the result of complex changes in audibility, suprathreshold processing, and cognition. Changes in cochlear structures, whether from biological aging of the structures themselves or secondary to intrinsic and extrinsic influences that occur with the passage of time, result in hearing sensitivity loss. The outward expression of the underlying disorder is fairly consistent. That is, loss of function of cochlear hair cells and other structures consistently manifest hearing sensitivity loss and the consequent deficits in audibility. Agerelated changes in auditory nervous system structures may also play a role in overall hearing capability, although the outward expression of the disorder is likely to be subtler than cochlear loss in a given individual and considerably more variable among individuals. Regardless, the complex hearing disorder associated with the aging process can have a significant impact on overall wellness. This review article provides an overview of aging and age-related decline in audition, with an emphasis on speech perceptual deficits with aging. KEYWORDS: Presbyacusis, audibility, auditory processing disorder, aging, hearing loss
Learning Objectives: As a result of this activity, the participant will be able to describe the factors that contribute to the decline in speech perception with age.
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n 1977, Konkle, Beasley, and Bess published a landmark study on speech perception decline in aging.1 The authors compared results among older subjects on measures of word recognition of stimuli that had been time compressed to various degrees. The subjects were
divided into four age groups, 54 to 60 years, 61 to 67 years, 68 to 74 years, and 75 years and older. All subjects had excellent absolute word recognition scores presented in quiet. In contrast, with time compression of 20%, 40%, and 60% of normal duration, word recognition
1 Henry Ford Hospital, Detroit, Michigan; 2Department of Hearing and Speech Sciences, Vanderbilt University School of Medicine, Nashville, Tennessee; 3Communication Sciences and Disorders, University of Georgia, Athens, Georgia. Address for correspondence and reprint requests: Brad A. Stach, Ph.D., Henry Ford Hospital, 2799 West Grand Boulevard K8, Detroit, MI 48202 (e-mail: bradstach
@mac.com). A Tribute to Fred H. Bess: 40 Years of Influence in Audiology; Guest Editor, Anne Marie Tharpe, Ph.D. Semin Hear 2009;30:94–111. Copyright # 2009 by Thieme Medical Publishers, Inc., 333 Seventh Avenue, New York, NY 10001, USA. Tel: +1(212) 584-4662. DOI 10.1055/s-0029-1215438. ISSN 0734-0451.
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scores declined systematically to a much greater extent than expected based on results from younger listeners. In addition, results showed that scores decreased as independent functions of increasing time compression and of age. These results showed not only that older listeners had marked difficulty processing timecompressed speech, but also that the decline in performance increased as a function of advancing age. Among other conclusions, the authors noted that the results emphasized ‘‘the subsequent perceptual difficulties which occur with loss of the temporal resolving power of the central nervous system as a result of the aging process.’’ This study helped usher in 3 decades of research aimed at understanding the complex way in which hearing changes as people get older. The results suggested that as individuals age, their ability to process in the time domain diminishes, and this decline in auditory processing appears to be attributable not only to peripheral sensitivity loss but also to changes in central auditory nervous system function. Viewed historically, Konkle et al1 were probably right, or at least partially so. Emerging since then has been an increasing understanding of the independent roles of hearing sensitivity loss, auditory processing disorder, and cognitive age-related decline in speech perception and, to a lesser extent, how these roles interact to affect communication function. This review article provides an overview of aging and age-related decline in audition, with an emphasis on the contributions of hearing sensitivity loss and more central factors on speech perceptual deficits with aging.
THE NATURE OF AUDITORY AGING The increasing number and proportion of elders is among the great demographic imperative facing health care today. Recent U.S. Census information2 highlights population trends relevant to aging. In 1900, the average life expectancy in the U.S. was 47 years, but by the year 2000 it had risen to 77 years. From 2000 to 2030, the number of elders is expected to double, from 35 million to 72 million. The fastest growing segment of the population includes those 85 years and older. Factors ac-
countable for these dramatic changes include those associated with reductions in mortality, such as advances in health care and improved hygiene, and the aging of the large baby-boom cohort, the first of whom will turn 65 in 2011. Physical aging is a biological process but one that occurs within psychosocial and behavioral contexts that greatly influence the course of an individual’s experience of aging. Biological aging is associated with greater vulnerability to disease and disability and, indeed, 80% of individuals > 65 years of age live with at least one chronic health condition. However, it also should be noted that rates of disability and functional limitations in elders declined between the 1990 and 2000 censuses. Several explanations exist, including increasing levels of education in successive cohorts of elders, improved health care, and lifestyle modifications such as diet and exercise. Based on studies of ‘‘successful aging,’’3 genetics are thought to account for about a third of the way we age, with the balance strongly influenced by factors that are extrinsic. Hence, although age-related trends can be observed in many health conditions, individual variability is high, and overgeneralization is to be avoided. Heterogeneity is a hallmark in studies of aging, and we cannot assume that successive generations of elders will age along the same trajectory as past or current cohorts. Age is the greatest risk factor for sensorineural hearing loss.4 Both prevalence and severity of hearing loss increase with age, as demonstrated by large-scale epidemiological studies.4,5 It is frequently noted that approximately a third of those > 65 years of age have significant hearing loss;6,7 however, the relationship between aging and hearing loss becomes even clearer when viewed within finer stratifications. In the Beaver Dam epidemiology of hearing loss study,4 almost 90% of those > 80 years of age demonstrated significant hearing impairment. Other more recent analyses8,9 indicate a 75% prevalence of high-frequency hearing loss among elders. The hearing loss associated with aging is typically sensorineural, of greater degree in the high frequencies and gradually progressive. The term presbyacusis (Greek ‘‘elder: þ ‘‘hear‘‘hearing’’) refers to age-associated hearing loss,
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and it can reflect both peripheral and central auditory system dysfunction.10 Deficits in speech understanding, particularly in the presence of background noise or in other less than optimal listening conditions, are well documented (see Willott10 for a comprehensive review). Structural and physiological changes occur throughout the auditory system with age. The outer and middle ears undergo noticeable or measurable age-related changes, but most of these are relatively inconsequential for hearing. Alterations in skin composition of the pinna and ear canal may lead to atrophy, loss of elasticity, or enlargement. Cerumen glands in older persons are fewer and less active, leading to a drier consistency of earwax and the greater likelihood of cerumen impaction.11 The possibility of arthritic and degenerative changes in the bones, joints, and ligaments of the middle ear also can occur.10,12 Any such changes do not appear to appreciably affect sound transmission through the middle ear system. Likewise, stiffening of the tympanic membrane can occur but usually without functional significance. Older persons may display pathologies of the middle ear system, such as otitis media, cholesteatoma, or otosclerosis, but these are not associated with an age-related increase in prevalence. The inner ear appears to be a site of particular vulnerability to deleterious aging changes.13 Inner ear and central auditory cells are generally considered to be of the ‘‘nonmitotic’’ variety, and thus they do not replicate. Specifically, degeneration and loss of hair cells occur, with outer hair cells from basal regions of the cochlea the most severely affected. Loss or degeneration of outer hair cells in basal regions of the cochlea is associated with the mild to moderate high-frequency hearing loss characteristic of presbyacusis. Most older people demonstrate some loss of outer hair cells. As more apical regions and/or inner hair cells become involved, more severe losses covering a broader frequency range ensue. Because both types of hair cells play crucial roles in hearing, auditory sensitivity is impaired when critical numbers are lost. Spiral ganglion cell loss is also common and may occur as either a primary process or secondary to the loss of their afferent
connections, the inner hair cells. This loss is also most severe in the basal or high-frequency regions. Atrophy of the stria vascularis is also common in aging and may be more pronounced in the apical regions. Strial changes may affect hearing by altering the chemical balance needed for cochlear function. Changes in cochlear support structures and blood supply also have been reported. Vascular insufficiency might compromise vital nutrition to inner ear structures. Ischemia or anoxia within the cochlea has been implicated in an excess release of glutamate, the presumed afferent neurotransmitter, which could in turn damage inner hair cells.14 Some evidence indicates that efferent cochlear and neural mechanisms might be less influenced by aging changes than the afferent structures, enhancing inhibition and thereby reducing information delivered to the central auditory system.10 Schuknecht and Gacek developed a metric for categorizing presbyacusis based on common types of physiological damage seen during temporal bone analysis of cochlear structures. This metric has been modified over time. The most recent version divides presbycusic hearing loss into five categories: sensory loss, strial (or metabolic) loss, cochlear conductive (or mechanical) loss, mixed loss, and indeterminate losses.15 Each type is named for the primary site of lesion identified via histopathological analysis of tissue from postmortem temporal bones. Although this categorization scheme provides an important metric for studying underlying pathology associated with aging, its clinical utility is somewhat limited, in part because it is likely that elderly ears suffer from multiple types of histologic damage. In addition, although these types of damage are often associated with specific audiometric patterns and speech-understanding abilities, substantial overlap has been observed.16 The central auditory system ages as well, although the impact is likely to be subtler and more variable in its expression than effects on the peripheral auditory system. What is known about the aging central auditory system is congruous with that of the aging brain in general. Neuronal loss or degeneration occurs within central auditory structures in a manner that can vary from site to site. In addition, large
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individual differences in structural changes in the brain are common in aging in general. Changes in structure and function occur throughout the peripheral and central auditory nervous systems as a result of the aging process.17 Evidence of neural degeneration has been found in the auditory nerve, brainstem, and cortex.18 Age-related changes in the central structures of the brainstem and cortex are relatively more subtle than peripheral changes, but they include the reduction in size and volume of nerve cells and alterations of neuronal connections and neurotransmitters.19 Willott10,18 categorized the influence of these changes as emanating from at least two processes. One is the central effect of peripheral pathology, or those that are secondary to the deprivation effects of cochlear hearing loss. Reducing auditory input from sensory structures has long been known to result in degenerative changes in neuronal structures normally receiving such input. In addition, change in the nature of the input may result in synaptic and pathway reorganization, whose consequence may or may not be detrimental to hearing. The other process is the central effect of biological aging of the nervous system structures. These central effects of biological aging include a loss of neuronal tissue; loss of dendritic branches, reducing the number of synaptic contacts; changes in excitatory and inhibitory neurotransmitter systems; and other degenerative changes. These changes vary considerably among individuals due, presumably, to genetic factors. In addition to these two factors, of course, are various pathologies of the central auditory nervous system that can accompany aging, such as anoxia and arteriosclerosis, whose effects may or may not impact the auditory portion of the nervous system. Not all auditory disorders occurring in old age are necessarily ‘‘caused’’ by aging. The delineation of hearing loss ‘‘caused by’’ versus ‘‘associated with’’ aging is often simply not possible. Diabetes,20 cardiovascular disease,21 genetic factors, and changes in bone composition10 are among the many age-linked factors correlated with hearing loss, either epidemiologically or theoretically. Most of these are audiometrically indistinguishable from presbyacusis, and all might be linked to
some more generalized process of aging, for example, oxidative damage caused by free radical production. Currently, hearing loss is considered a universal, although variable, aspect of normal aging, for which no medical interventions are possible. Using a single term presbyacusis to capture auditory system alterations associated with aging belies the fact that there are indeed numerous processes responsible for observed changes. Somewhat different patterns emerge for men and women, with men tending to show greater levels of hearing loss at younger ages. In general, women demonstrate less high-frequency hearing loss but tend toward greater low-frequency hearing loss.22 Greater occupational noise exposure among men is one obvious explanation for these findings, but the gender differences remain even when controlling for occupation, history of noise exposure, and education.4 The classic studies of the Mabaan tribe of Sudan23 suggest that the severity of age-associated hearing loss seen in industrialized societies may not be inevitable and in part be attributed to maladies such as hypertension and stress. However, it seems likely that at least some high-frequency hearing loss is normative in aging, and that presbyacusis represents underlying intrinsic biological processes that affect the structure and function of the auditory system over time. Although it can be debated whether presbyacusis should be considered a disease or a normal part of aging, what cannot be understated is the fact that hearing loss is a highly prevalent condition among elders, and it is one with significant ramifications for individual well-being, as well as relationships. Hearing impairment in old age is neither trivial nor benign. Impaired audition potentially compromises all of an individual’s interactions with his or her environment, from basic awareness of warning sounds to the complex and subtle nuances of conversation. Auditory/ verbal communication is integral to relationships, whether between spouses, with children, with medical professionals, or across any of the range of social networks vital to the well-being of elders. Numerous correlation analyses have
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linked hearing impairment with far-reaching negative consequences in the lives of those afflicted, including reduced psychosocial wellbeing,24,25 lower quality of life,26 poorer functional health,27 cognitive decline,28,29 greater likelihood of skilled nursing home placement,30 and higher rates of mortality.31 Because hearing is vital to social function, interpersonal relationships may be disrupted when one party is hearing impaired.32–34 Qualitative inquiry has highlighted personal meanings and struggles associated with integrating acquired hearing loss into self-concept.35 Even beyond the expected psychosocial realm, hearing loss among elders has been linked to physical health or the broader concept of functional health. Bess and colleagues27 were among the first to explore the association between hearing loss in elders and quality of life using a generic health-related quality-oflife instrument, the Sickness Impact Profile.36 Although it is clear that hearing loss adversely affects communication, the use of a generic instrument allowed for an analysis of the relationship between hearing loss and other broad domains of functional health, and it enabled comparison of scores of elders with hearing loss with those with other health problems. Hearing impairment was shown to contribute independently to reduced quality of life in both physical and psychosocial domains, with greater levels of hearing loss demonstrating a continuous relationship with increased functional disability. Somewhat surprisingly, hearing loss was more strongly associated with physical than psychosocial health. The authors speculated that this relationship implied that ‘‘auditory cues are more important than previously recognized for successful physical interactions with the environment.’’ In addition, this work highlighted the relevance of hearing loss in the context of other serious disorders and diseases. The original findings of Bess et al27 have been borne out in other investigations. For example, Dalton and colleagues37 reported an association between hearing impairment and activities of daily living and instrumental activities of daily living, as well as with decreased function in both the Mental Component Summary score and the Physical Component
Summary score of another generic functional health survey, the SF-36.38 Many elders can and do benefit from amplification, in the form of hearing aids or other assistive devices. By alleviating the audibility and communication deficits associated with hearing impairment, broader gains in terms of quality of life can be achieved. Nevertheless, the use prevalence of hearing aids among American hearing-impaired elders is quite low, remaining 20%.39 This figure has been stable in spite of the increasing technological sophistication of available devices, and in spite of evidence of hearing aid benefit, short and long-term, in quiet and in noise.40,41 Hearing loss, then, is a common condition of growing older. Age-related changes in cochlear structures, whether from biological aging of the structures themselves or secondary to intrinsic and extrinsic influences that occur with the passage of time, result in hearing sensitivity loss. The outward expression of the underlying disorder is fairly consistent. That is, loss of function of cochlear hair cells and other structures consistently manifest hearing sensitivity loss and the consequences of that loss. Age-related changes in auditory nervous system structures also may play a role in overall hearing capability, although the outward expression of the disorder is likely to be subtler than cochlear loss in a given individual and considerably more variable among individuals. Regardless, the complex hearing disorder associated with the aging process can have a significant impact on overall wellness.
REDUCED SUPRATHRESHOLD HEARING As Konkle et al1 showed, in addition to agerelated changes in hearing sensitivity, the ability to hear at suprathreshold levels also is impacted by the aging process. That is, they found that older subjects demonstrated a decline in speech perception that was greater than observed in younger listeners and seemed out of proportion with the degree of hearing sensitivity loss attributable to cochlear hearing loss in their older subjects. One of the more intriguing questions addressed over the ensuing years is whether this decline in suprathreshold hearing,
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usually quantified by scores on speech-recognition measures, is merely a reflection of peripheral hearing sensitivity loss, a reflection of auditory processing disorder relating to a degraded central auditory nervous system, or a reflection of the influence of generalized cognitive decline on interpretation of these suprathreshold measures.
The Influence of Audibility As noted, age-related structural changes to the peripheral auditory mechanism are well documented. Although age-related changes occur to the outer and middle ear structures, in most cases these changes do not appear to affect speech perception significantly in the elderly.42 This is not surprising given that these structures contribute primarily to passive amplification of sound that is relatively unaltered by the aging process. This is not the case for inner ear structures. Primary changes within the inner ear include damage to the stria vascularis, atrophy and reduction of inner and outer hair cells and surrounding support cells within the organ of Corti, and a reduction in the number of spiral ganglion cells and auditory neurons that synapse with hair cells.15,43 The physiological consequences of age-related changes in cochlear structures are varied, but a common finding includes a reduction or loss of the active compressive nonlinearities seen in a healthy ear. The most prominent consequence of this is a reduction in basilar membrane sensitivity to low-level sounds, particularly in regions of the cochlea response to high-frequency sounds, and a loss of sharp tuning on the basilar membrane (i.e., reduced frequency selectivity) in the damaged areas. One result of this is the high-frequency hearing loss commonly observed among elderly individuals. An additional consequence, if the damage results in moderate or greater hearing loss, is decreased perceptual processing and reduced discrimination of sounds due to reduced frequency and temporal processing abilities.44 It is important to note here that these consequences are a result of the underlying cochlear damage, not to age per se. That is, although the underlying structural damage may vary, similar consequences are observed in younger individuals
with cochlear hearing loss due to factors other than age (e.g., noise exposure). Functionally, the loss of sensitivity to soft sounds frequently results in reduced audibility of speech and thus can have predictable consequences on speech perception in elderly individuals. Given that the underlying cochlear damage and high-frequency hearing loss commonly increase with age, the reduced audibility associated with these changes also increases. The effects of reduced audibility on speech understanding are well known. Audibility metrics, such as the Articulation Index45 (AI) or the more recent Speech Intelligibility Index46 (SII), are effective in predicting average speech recognition in young adults with normal hearing in a wide range of conditions. In its simplest form, the AI is a mathematical derivation, based on frequency-specific speech, noise, and threshold levels, of the proportion of audible speech information. The index ranges between 0 (no audible information) and 1 (all speech is audible) and is highly correlated with speech understanding. An empirically derived transfer function is used to predict performance on a given speech-recognition task based on the calculated AI/SII. Decades of work in this area have shown that these procedures do quite well predicting average performance of persons with normal hearing in a wide range of audibility conditions (e.g., various filter conditions or signal-to-noise ratios [SNRs]).47–49 Researchers have expanded the use of AI metrics to predict understanding in other groups, such as hearing-impaired or elderly individuals, in an attempt to examine effects of other factors such as hearing loss or age on speech recognition.50–54 A general finding of these types of studies is that the AI/SII does a better job predicting performance of young adults and individuals with milder hearing loss than the elderly or those with more severe hearing loss. To improve predictive accuracy of the AI/SII for specific groups (e.g., hearing impaired and/or elderly), correction factors have had to be used to adjust the AI/SII based on a given variable. For example, Sherbecoe and Studebaker53 examined the predictive accuracy of the AI for adults with hearing loss. They reported that predictive accuracy was best, although still poorer than for persons
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without hearing loss, when separate correction factors based on speech presentation level, degree of hearing loss, and age were included. However, the increased accuracy in predictions with the inclusion of a correction factor for age was small and beneficial only for individuals 70 years of age. Several researchers have attempted to minimize audibility differences between young and elderly listeners by introducing a masking noise so that the noise, rather than threshold, limits audibility.55–58 Humes and Roberts57 compared speech understanding in three groups, young normal-hearing, elderly hearing-impaired, and young normal-hearing individuals listening in a masking noise to elevate thresholds to that of the elderly hearing-impaired group. Participants listened to speech materials through earphones both monaurally and binaurally. Materials were recorded through a Knowles Electronics Mannequin for Acoustic Research in quiet and noise in both an anechoic and reverberant environment. A general finding was that the young normal-hearing group performed better than the elderly hearing-impaired group in all conditions. However, there was no difference between the elderly hearing-impaired and the noise-masked normal-hearing groups, suggesting that differences in audibility were the primary factor responsible for the poorer performance by the elderly group. Souza and Turner58 reported similar findings in both steady-state and modulated noises when comparing monosyllable recognition in younger (22 to 35 years of age) and older (64 to 77 years of age) hearing-impaired individuals with similar amounts of hearing losses. Another method of accounting for audibility differences as a function of age is to screen multiple people of varying ages and identify groups with similar amounts of hearing loss. As part of a longitudinal study of agerelated hearing loss,59 Dubno et al assessed auditory function in a large group of individuals. A subgroup of 129 individuals (250 ears) ranging in age from 55 to 84 years with similar degrees of hearing loss was identified. Participants were divided into three groups based on age (55 to 64, 65 to 74, and 75 to 84 years). Average hearing thresholds were within 5 dB across a wide frequency range (250 to 8000 Hz)
across all groups. Speech recognition was assessed using six different test materials, including words and sentence materials, in quiet and in noise. Results showed no difference in speech understanding between the age groups for any of the materials or conditions tested. These findings suggest that, when audibility is equivalent, increases in age, per se, do not lead to decreases in speech understanding at least for the age ranges of 55 to 85 years. Using a similar approach,54 Studebaker et al identified 140 individuals between 20 and 90 years of age (20 participants per decade group) with auditory thresholds of 25 dB HL or better for frequencies between 250 and 2000 Hz. Thresholds > 2000 Hz were poorer than 25 dB HL for some groups and varied with age. To limit the effects of differences in audibility between groups at frequencies > 2000 Hz, the speech materials (NU-6 monosyllables) were band-pass filtered (220 to 2300 Hz) and presented in a steady-state noise at an SNR of þ2.5 dB. This SNR was chosen, based on AI predictions, to result in average performance near 50% correct. Participants were recruited at two sites (70 per site). Average performance, across sites, was similar for individuals between 20 and 69 years at 55%. For older individuals, a small but significant decline in performance was noted. Scores for individuals in their 70s and 80s were poorer at 50% and 47%, respectively. It is interesting to note that this age effect varied across test sites. Thus, consistent with Dubno et al,59 these findings suggest minimal age effects, when audibility is equated across age groups, for individuals between 20 and 80 years of age. Poorer performance, despite equated audibility, was observed for some individuals between 81 and 90 years of age (at one site only). Finding individuals with similar hearing loss across a wide age range is difficult and time consuming. Likewise, using a masking noise to equate audibility across age groups is problematic in that it is achievable only if the hearing loss is mild to moderate. Masking noise cannot be used to simulate more severe losses due to the excessive loudness of the noise for the unimpaired group. To overcome these difficulties, several investigators have used statistical methods, such as factor analysis and multiple
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regression, to investigate the contribution of age, in addition to other factors such as reduced audibility, to speech-recognition difficulties in the elderly population.60–63 Using this approach, both age and degree of hearing loss (and thus audibility) are treated as continuous variables, and statistical methods are used to examine the relationship between these, and other, predictor variables to speech perception in the elderly. Representative of this approach, Humes61 examined the relationship between a set of 33 predictor variables and both unaided and aided speech recognition in 171 elderly individuals between 60 and 89 years of age. Variables included, in part, age, behavioral and physiological measures of auditory function (e.g., thresholds, otoacoustic emissions [OAEs], auditory brainstem response [ABR]), auditory processing abilities (e.g., temporal and frequency resolution), and cognitive abilities (i.e., IQ measures). Eight different measures of speech recognition, including nonsense syllables and contextually rich sentence materials, presented both in quiet and noise, were used. In an attempt to generalize the results across the wide range of speech materials, principal components analysis was used to collapse the multiple speech scores into a single speechrecognition factor. Results showed that this factor accounted for 61% of the variance between the different measures of speech understanding assessed in the study. A similar analysis was completed on the 33 predictor variables, resulting in a reduced set of seven orthogonal factors. These factors were related to verbal IQ, hearing loss, nonverbal IQ and age, distortion product OAEs, ABR, and a ‘‘miscellaneous’’ factor. It is important to note that, because all speech materials were presented at fixed levels and SNRs, variations in hearing loss resulted in variations in audibility across listeners. In other words, the hearing loss factor also represented an audibility factor. A multiple linear regression approach was then used to examine the relationship between the seven predictor variables and general speech-recognition ability. Consistent with previous studies that focused on unaided speech perception,60,62,63 differences in speech recognition across these elderly
participants was due primarily to differences in audibility. The hearing loss/audibility factor accounted for the largest amount of variance (53% of total variance/80% of the systematic variance) in speech recognition among the elderly participants. Specifically, those older adults with more hearing loss/less audibility had poorer speech recognition than those with less hearing loss/more audibility. Other factors, apart from degree of hearing loss/audibility, also played a significant but much smaller role in explaining variations in speech perception in the elderly. A factor loading on nonverbal IQ and age accounted for an additional 7% of total variance in speech recognition in the elderly. Further analysis attempting to disentangle the relative contributions of nonverbal IQ and age suggested that variations in age, per se, played a smaller role compared with variations in nonverbal IQ. In summary, results across multiple studies using a variety of methodologies provide converging lines of evidence to suggest that the deficits in speech recognition experienced by elderly individuals, at least for those < 70 to 80 years of age with mild to moderate hearing loss, are due primarily to the loss of audibility and/or reduced perceptual processing resulting from peripheral cochlear damage.
The Influence of Auditory Processing Ability As noted earlier, age-related changes occur throughout the auditory system, including the peripheral and central auditory nervous system. These detrimental effects of aging on the auditory nervous system can have significant consequences on suprathreshold perception in elderly individuals over and above that which can be explained on the basis of any underlying cochlear damage and consequent loss of audibility associated with increasing age.64 The deficits most commonly attributed to these nervous system changes are reductions in speech perception in competition, speech perception at high intensities, temporal processing, and binaural hearing, particularly in terms of dichotic listening and spatial hearing. These types of deficits have long been known clinically to be associated with neurological
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involvement of the auditory system and are generally referred to collectively as auditory processing disorders.65–67 To understand the conceptual framework around which the clinical testing of auditory processing is based, it is important to understand the influence of the neurological disease process on auditory function. It is well known that the influence of an auditory nervous system disorder is considerably more subtle than the influence of cochlear hearing loss.68 Indeed, unless the disorder impacts the auditory nerve directly and prominently, it is unlikely to affect outcomes of pure-tone and simple speech audiometric measures. That is, absolute word recognition scores, whether determined in quiet or in the presence of some form of steady-state noise, are seldom influenced by auditory nervous system disorder. Therefore, in a patient with a neurological disorder and concomitant cochlear hearing loss, the rules of audibility most often apply. For the influence of the nervous system disorder to be revealed, the speech audiometric measures must be sensitized in some way to challenge the auditory system. It is not surprising, then, that subtle or diffuse changes in the auditory nervous system that occur with aging are not revealed by such simple measures as word recognition scores. As already discussed, the early suggestion of a disproportionate decline in word recognition with age beyond that which might be predicted from degree of cochlear hearing loss, known as phonemic regression, has been largely refuted over the years as explainable by the cochlear hearing loss and its impact on audibility. This was demonstrated by Gates et al,69 who studied word recognition and audibility in a population-based cohort of older individuals. Only 5.6% of older listeners in the cohort showed word recognition scores that were poorer than those predicted by the AI. The notion that some of the difficulties experienced by older patients resulted from changes in the central auditory nervous system came from early studies such as those by Jerger68 and by Konkle et al1 in which test outcomes known to be associated with auditory nervous system disorder were observed in older patients. With a series of case studies, Jerger and Hayes70 showed that patterns of speech
audiometric outcomes measured in some older patients were similar to those of patients with nervous system tumors and other lesions and that this central aging effect became more prominent as patients aged. The inference here and from many other studies was that speech perception outcomes in older patients that resemble those from younger patients with neurological disorders implicate the auditory nervous system as the primary contributing factor, given that hearing sensitivity loss can be accounted for in test interpretation. Findings in older patients of central or retrocochlear signs on suprathreshold measures of speech perception thus became associated with changes in auditory nervous system function rather than cochlear function. One of the most important consequences of auditory aging is an inability to extract signals of interest from a background of competition.70–74 Although measurable with several different speech audiometric techniques, in general, the more meaningful or speech-like the competition, the more it will interfere with the perception of speech.75–77 Prominent among the work in this area over the years was that by Jerger and his colleagues.70,78 Among other measures, they used the synthetic sentence identification test, a procedure in which nonsense sentences are presented in the presence of background competition. The competition in this case is a single talker presented at a 0 dB SNR. The task is a fairly simple one perceptually for anyone with an intact auditory system even in the presence of considerable hearing sensitivity loss and audibility reduction. Because of the silent periods between words in the single-talker competition, the sentences are readily identifiable. Many older patients and patients with auditory nervous system disorder, however, do not seem to avail themselves of these dips in masker amplitude and perform more poorly than expected. The outcomes in older individuals are relatively independent of hearing loss and cognitive decline.78,79 Another speech perception outcome that is much more commonly found in cases of auditory nervous system disorder than cochlear disorder is decreased performance at high intensity levels when speech is presented in quiet.80,81 In cases of normal auditory processing ability,
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regardless of any hearing sensitivity loss, speech-recognition performance in quiet increases systematically as speech intensity is increased to an asymptotic level, representing the best speech understanding that can be achieved in that ear. In some cases of auditory processing disorder, however, the paradoxical rollover effect exists, in which performance declines substantially as speech intensity increases beyond the level producing the maximal performance score. In other words, as speech intensity increases, performance rises to a maximum level and then declines or ‘‘rolls over’’ sharply as intensity continues to increase. This rollover effect is commonly observed when the site of the hearing loss is retrocochlear, in the auditory nerve or the auditory pathways in the brainstem, and it is a common finding in aging patients.70 Interestingly, the underlying nature of this effect may well be related to temporal synchrony issues at high-intensity levels.82 Other impairments in processing in the time domain have been associated with central auditory disorders.83,84 Temporal processing as a specific deficit in aging has been reported on measures of speech perception, such as time-compressed speech.1,85–88 Although interpretation of such measures is influenced by hearing sensitivity loss, age is an independent factor in performance reduction.89 In addition to reduced performance on speech audiometric measures, temporal processing deficits90,91 have been described on measures of precedence,92,93 duration difference limens,90 duration discrimination,94 and gap detection and discrimination.95–97 The ability to localize acoustic stimuli spatially generally requires auditory system integration of sound from both ears. Some patients with auditory processing disorders have difficulty locating the directional source of a sound. Disorders of the central auditory nervous system are associated with deficits in the ability to localize the source of a sound in a sound field or to lateralize the perception of a sound within the head. Spatial and binaural hearing also may be reduced as people age.60,98 For example, using a technique referred to as cued discourse, Jerger and Jordan99 showed a substantial leftside deficit in perception in older individuals who had symmetrical hearing sensitivity. In this
procedure, identical ongoing speech signals are presented from speakers opposite the right and left ear. The speech signal is a single talker reading a story written in the first person. The same story is presented from both speakers with a delay of 1 minute in one of the speakers. The patient’s task is to count the number of times that the personal pronoun ‘‘I’’ is perceived from the speaker that is being cued. The number of errors is counted, and the opposite speaker is cued. Following completion, multi-talker babble is introduced from an overhead speaker, and the process is repeated over a range of SNRs. Results of the cued discourse measure have shown significant asymmetries in patients with central auditory processing disorders100 and in the aging population.99 Disorders of the central auditory nervous system, particularly those caused by impairment of the corpus callosum and auditory cortex, often result in dichotic deficits characterized by substantial reduction in left ear performance. Tests of dichotic performance also are adversely affected by aging.101–104 Furthermore, these deficits seem to resemble in nature those found in patients with corpus callosum deficits.102 Another kind of deficit in binaural processing is referred to as binaural interference. Under normal circumstances, binaural hearing provides an advantage over monaural hearing. This binaural advantage has been noted in loudness judgments, speech recognition, and evoked potential amplitudes. In contrast, in cases of binaural interference, binaural performance is actually poorer than the best monaural performance. It appears that the poorer ear actually reduces binaural performance below the better monaural performance. Binaural interference has been reported in patients with multiple sclerosis105 and in elderly individuals.106 In addition to these results from behavioral speech-perception measures, there is growing physiological evidence of age-related changes in auditory nervous system function. Electrophysiological data point to a change in synchrony of neural activity,107 the possible disinhibition of function,108–110 and changes in hemispheric symmetry in aging patients.106,111
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In summary, results across multiple studies using a variety of methodologies provide converging lines of evidence to suggest that the deficits in suprathreshold hearing experienced by many older individuals are due not only to the loss of audibility from peripheral cochlear damage, but to temporal processing deficits imposed by changes to the auditory nervous system. Regardless of whether a disorder is identified as a problem in temporal processing, dichotic listening, or localization, the functional consequence to the patient tends to be difficulty with spatial hearing in adverse listening environments. In older patients, this behavioral consequence may occur in disproportion to the degree of hearing sensitivity loss.
The Influence of Cognitive Decline Changes in speech-recognition ability with aging can be attributed to audibility issues caused by hearing sensitivity loss and auditory processing disorder caused by nervous system dysfunction. This decline in ability, or at very least its measurement, also may be influenced significantly by a reduced capacity brought on by senescent changes in cognition. It appears that for most of the perceptual tasks in routine audiometry and in measures of auditory processing ability, task-related demands are low enough not to be influenced by generalized reductions in memory or cognition. For example, Jerger and colleagues112 showed that results on suprathreshold speech audiometric measures were independent of cognitive disability. Audiological data were analyzed from 23 patients with a neuropsychological diagnosis of dementia. Among the cognitive deficits found in these patients were those of memory, tolerance of distraction, mental tracking and sequencing, and cognitive flexibility. Despite such deficits, 12 of the 23 subjects (52%) yielded speech audiometric results consistent with normal auditory processing ability. That is, patients with dementia performed well on behavioral speech audiometric tests, arguing against any simple explanation that auditory processing disorders can be explained as easily by subtle cognitive decline as by an auditory deficit. In another study, Jerger
and colleagues113 measured both auditory and cognitive status in 130 aged subjects. They found that auditory processing ability and cognitive function were congruent in only 64% of subjects, indicating that the two measures were relatively independent. That is, auditory processing disorders occurred in those individuals with normal cognitive status, and cognitive decline occurred in those with normal auditory processing ability. Although, in general, speech audiometric measures are independent of significant cognitive decline, the story is not quite that simple. In other studies of the aging process involving dichotic measures, some performance deficits were found to be task related.104,114,115 These findings suggest that dichotic results could be overinterpreted as deficits if care was not taken to limit these nonauditory influences. In one study,104 patients were asked to perform a dichotic measure in two ways. One was a free-recall mode, in which the patient’s task was to identify both sentences in either order. The other was a focused-recall task, in which the patient was asked to identify only those sentences perceived in the right ear. The task was then repeated for the left ear. Several elderly patients had difficulty on the freerecall task, but they improved when the task was simplified. It appears that short-term memory problems were influencing the results on this dichotic measure. When the task was simplified, some patients still showed deficits, but they appeared to be truly auditory in nature. The processes involved in auditory processing and other, more supramodal cognitive functions overlap to an extent that they cannot always be measured independently. As an example, one study116 suggests the intriguing notion that auditory processing disorder precedes the onset of Alzheimer’s disease. Although the influence of cognitive ability may be negligible or controllable on simple clinical measures of speech perception, the question remains whether cognitive decline with aging adds to the auditory system decline to reduce communication function. Evidence suggests an important interaction between the complexity of speech and its speed of presentation and the ability of aging
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individuals to perceive accurately, implicating memory, attention, and other cognitive factors in reduced functioning.117,118 Several theories might explain the potential influences of cognitive decline on communication ability.119 One, the resource theory, suggests that older individuals have limited resources for completing complex cognitive tasks in comparison with younger adults. These diminished cognitive capabilities include processing speed, working memory, attention, and inhibition. The ability to process speech accurately requires fast execution of cognitive operations. If cognitive processing occurs too slowly, some of the message might be lost because the time window is insufficient to analyze the entire signal. Alternatively, portions of the message might become embedded in the successive speech signal, thereby reducing the amount of time for the processing of later speech components.120 In fact, elderly listeners have been shown to perform more poorly on time-compressed speech measures when linguistic cues are limited as compared with their performance on time-compressed meaningful sentences121 or when speech consonants were targeted specifically for time compression.122 As noted earlier, several other investigations have shown that speech recognition decreases when the rate of speech is increased by time compression, and this finding is consistent even when hearing loss is taken into account.123–125 Speech perception also has been examined using time-expanded speech.126 When sentences were presented at an expanded speech rate, both young and old listeners showed excellent performance; in contrast, performance was significantly poorer for timecompressed speech. Elderly listeners and listeners with hearing loss, however, showed improvement in speech understanding for selected forms of time expansion, with best achievements occurring when consonants were time expanded. In addition to the decline in processing speed, the aging individual also may have a general decline in cognitive performance that affects working memory.120,127 Working memory is the limited capacity storage system that can perform active computations on data stored in short-term memory for brief time periods.128
Declines in selective attention abilities have been found to have negative effects on working memory. The clinical implications relating to these changes in cognitive function are important. For elderly individuals, listening effort is increased when working memory is functionally reduced.129 Moreover, when the speech signal is degraded due to temporal alterations, complexity of the speech signal, or other external factors, a greater taxation on working memory occurs. Attention also may play a role in reducing communication function. Several models have been postulated to explain the relationship between attention and cognition. The resource model130 suggests that individuals have a limited capacity for attention-related tasks. The context model suggests that this decline in attention is related to a decreased ability to use context.131 The neural noise model and others129,132 suggest that attention follows one of three types: (1) vigilance search attention processing, meaning that listeners have to expend considerable effort to hear; (2) selective attention, similar to a filtering concept; or (3) divided attention, which is similar to resource allocation. Selective attention differs from divided attention in that the former relates to the ability to focus on relevant information and ignore irrelevant information, and the latter relates to the ability to divide attention and complete multiple tasks.133 Regardless of the manner in which attention affects speech understanding, whenever attention is divided, a heavier burden is placed on executive function and, subsequently, working memory.134 Cognition, then, plays an important role relative to memory, attention, and speech perception. Although it has been shown that complex changes in hearing account for much of the inability to hear and understand speech, when hearing ability has been restored, many older individuals still find speech comprehension and ease of listening to be very challenging.
DISCUSSION The Konkle et al1 findings serve as a valuable reminder of the challenges in studying suprathreshold changes in aging. One of the important lessons from this study is the importance of
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controlling for audibility and, therefore, degree of hearing sensitivity loss. Clearly, age-related change in cochlear function, resulting in peripheral hearing loss, is a primary factor responsible for at least some of the speech perception difficulties in elderly individuals. However, given the same access to audibility information, it appears that a young and an old ear are able to recognize simple speech targets equally. Similarly, it should be no real surprise that one ear deprived of information because of a hearing sensitivity loss might not recognize speech as proficiently as an ear with better access to that information. From all that we know and understand about the nature of cochlear sensitivity loss and speech audiometry, the old and young ear should act the same given equal audibility, and, for the most part, they do. Another important lesson, though, is the importance of defining the problem itself in terms of what is actually being measured. From what is known clinically about auditory nervous system changes in cases of neuropathologic disease, it is not expected that word recognition scores, or even word recognition in steady-state noise, would be affected by most disorders beyond that expected from any hearing sensitivity loss. That is, structural changes to the neurological system, such as those that occur as the result of tumors, multiple sclerosis, or embolism, are likely to have a subtle effect on audition, unless they severely affect function of the eighth nerve. It is unlikely that such disorders will result in reduced scores on conventional measures of word recognition. To hypothesize that more diffuse changes from aging would somehow impact these measures is to miss the point entirely. It seems apparent, from the previous discussion, that simple word recognition ability depends primarily on what is audible to the patient and, on average, is highly correlated with the audiogram. Konkle et al showed exactly that in their data at 0% time compression. Such measures are simply not sensitive to changes in nervous system function except in extreme cases. By challenging the auditory system, however, differences might emerge in the performance of older individuals in comparison with younger individuals with similar hearing loss. Measures of speech in complex competition and at high
levels and measures of binaural ability that have been validated as sensitive to changes in auditory nervous system disease and trauma are sensitive to the more subtle effects of nervous system aging in some individuals. Another important lesson relates to sample selection. Most laboratory studies draw subjects from the population in general, resulting in a sample of vibrant, ambulatory, active volunteers from the community who may not be experiencing much hearing loss. Most clinical studies draw subjects from the population of patients with hearing disorders. If, in fact, there is any reason to believe the aging population is homogeneous, then, at best, subjects are being drawn from different ends of the distribution. The case in point can be made by several studies of prevalence of suprathreshold disorders in the elderly population. In clinical studies of patients who seek assistance for hearing problems, the likelihood of observing deficits is fairly high in older patients and increases with age.135 In contrast, population-based studies show considerably less evidence for such complex auditory deficits.136 On one hand, careful control over the virility of the aging sample may all but eliminate the effect; on the other, the complexity of the aging effect might be significantly exaggerated by the nature of the sample. One final lesson learned is in treatment of the data. Many studies treat auditory aging as a homogeneous problem, collapsing data across the group as if the group is representative of the individual. Clinical studies by their nature usually treat data more individually, focusing on those with apparent disorder rather than losing those data to the mean. A 2006 study by Roup and colleagues137 on dichotic performance serves to make this point. Although the group data showed an expected right ear advantage that was greater in the elderly groups than in the younger group, examination of the individual data showed a small subgroup with substantial deficits that provided new insight into the challenges that some older patients face. The expression of neurological disorders, whether from space-occupying lesions or from diffuse changes, is variable, not consistent. Treatment of the data as if the underlying cause will result in a consistent expression of the disorder is unlikely to reveal the true nature of the issue.
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It seems fair, knowing what we do now, to suggest that in the Konkle et al1 study, a considerable amount of the deficit they reported in their elderly groups on the measure of time-compressed speech was attributable to reduced audibility of cochlear origin in the older groups, which had progressively more hearing sensitivity loss with age. It is also fair to suggest that some individuals in the older groups were experiencing more temporal auditory deficits relating to subtle aging changes of their central auditory nervous systems. Finally, it is fair to presume that the progression of cognitive decline with age interacted, to at least some extent, both with hearing sensitivity loss and suprathreshold decline to further reduce performance in subjects as they aged.
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