Effects of age and age-related hearing loss on the neural representation of speech cues
Introduction
Older adults, with and without normal-hearing sensitivity, often have difficulty understanding speech (Marshall, 1981, Jerger et al., 1989, Jerger et al., 1990, Humes, 1996). They frequently complain, “I can hear you, but I can't understand you.” Because speech is a complex signal, composed of multiple time-varying acoustic cues, it is frequently hypothesized that aging adversely affects the ability to process temporal cues (Dubno et al., 1984, Trainor and Trehub, 1989, Abel et al., 1990, Moore et al., 1992, Fitzgibbons and Gordon-Salant, 1994, Schneider et al., 1994, Snell, 1997). More specifically, it is speculated that: (1) temporal processing is dependent on the neural detection of time-varying acoustic cues and (2) impaired perception results from age-related factors affecting neural synchrony (Frisina and Frisina, 1997, Schneider and Pichora-Fuller, 2001).
Recent findings by Strouse et al., 1998, Tremblay et al., 2002 support the notion that older adults have more difficulty processing time-varying cues, and perceptual difficulties might be related to factors affecting neural synchrony. For example, in the English language, the voiced stop consonant /b/ is distinguished from its voiceless counterpart /p/ based on a temporal cue called voice-onset-time (VOT). VOT is defined as the time interval between the release from the consonant stop closure and the onset of voicing (Lisker and Abramson, 1970). Both Strouse et al., 1998, Tremblay et al., 2002 found that older adults, compared with younger adults, had difficulty discriminating short VOTs along a /ba/–/pa/ continuum. In addition, these same /ba/–/pa/ speech-sounds-evoked abnormal neural response patterns in older adults (Tremblay et al., 2002). That is, synchronous responses to the onset of the vowel were delayed in older adults.
Tremblay and colleagues used the N1–P2 complex to examine the neural representation of the VOT in younger and older adults. The N1 component of the N1–P2 complex is an onset response reflecting synchronous neural activation of structures in the thalamic-cortical segment of the central nervous system in response to acoustic change (Wolpaw and Penry, 1975, Naatanen and Picton, 1987, Woods, 1995). Moreover, N1 latency has been shown to reflect the onset of voicing along a VOT continuum (Kurtzberg, 1989, Steinschneider et al., 1999, Sharma et al., 2000, Tremblay et al., 2002). Because speech-evoked N1–P2 responses reflect spectral and temporal acoustic changes contained within the speech signal (Kaukoranta et al., 1987, Ostroff et al., 1998, Martin and Boothroyd, 1999), there has been a surge of interest in using speech-evoked N1 and P2 responses to assess the neural representation of time-varying speech cues in various populations with communication disorders. For instance, abnormal speech-evoked N1–P2 responses have been reported in people with impaired speech perception (e.g. simulated hearing loss, Martin et al., 1997, Whiting et al., 1998, Martin and Boothroyd, 1999; auditory neuropathy, Kraus et al., 2000, Rance et al., 2002 and children with auditory based learning problems, Cunningham et al., 2001, Purdy et al., 2002, Wible et al., 2002). In addition, the N1–P2 complex reflects central auditory plasticity associated with various types of auditory rehabilitation including cochlear implantation (Ponton et al., 2000, Purdy et al., 2001) and auditory training (Tremblay et al., 2001, Tremblay and Kraus, 2002, King et al., 2002).
When Tremblay et al. (2002) recorded N1–P2 responses in younger and older adults, N1 and P2 latencies were prolonged for older adults. Specifically, N1 latencies were prolonged for older listeners in response to stimuli with increased VOT durations. P2 latencies were delayed for all stimuli. Because participants in the Tremblay et al., 2002, Strouse et al., 1998 studies had hearing thresholds that fell within normal limits, age-related differences were unrelated to audibility differences between the two groups. However, most aging adults experience age-related sensorineural hearing loss. The combination of aging and hearing loss likely exacerbates communication problems in at least two ways. First, peripheral hearing loss reduces the audibility of certain acoustic cues and the perceptual consequence is decreased speech intelligibility (Boothroyd, 1984). Second, animal research has shown that peripheral hearing loss alters spatial and temporal response properties throughout the central auditory system (Kitzes, 1984, Willott, 1986, Robertson and Irvine, 1989, Harrison et al., 1993, Rajan and Irvine, 1998, Irvine et al., 2001).
While much is known about the perceptual consequences of age-related hearing loss, less is known about the physiological effects of age and age-related hearing loss in the human central auditory system. From a neuroscientific perspective, this information is important because it helps define neural processes associated with aging and age-related hearing loss. From a clinical perspective, this information may identify a source of performance variability among people who wear hearing aids. Only 40–60% of hearing aid users report significant benefit from using their hearing aids (Humes, 2001). Because aging auditory systems have more difficulty processing temporal cues, making sounds louder through the use of a hearing aid might have a better outcome for younger than older users. Thus, information from the proposed experiment might help explain some of the performance variability experienced by hearing aid users, and could change the way we approach rehabilitating older hearing-impaired adults.
For these reasons, we use the N1–P2 complex to examine the effects of age and age-related hearing loss on the perception and neural detection of VOT. Three groups are examined: (1) young normal-hearing listeners, (2) older normal-hearing listeners and (3) older listeners with high-frequency sensorineural hearing loss. Because Tremblay et al. (2002) reported prolonged N1 and P2 latencies in older normal-hearing listeners, perhaps reflecting age-related changes in neural synchrony, we expect that older adults with hearing loss will show similar latency delays. Prolonged latencies and decreased amplitudes have also been reported in young adults with simulated (Martin et al., 1997, Whiting et al., 1998, Martin and Boothroyd, 1999) and organic hearing loss (Polen, 1984, Oates et al., 2002); therefore, we hypothesize that the presence of age-related hearing loss will add to the age-effects previously reported. That is, older adults with hearing loss will have more difficulty than younger and older normal-hearing groups perceiving VOT contrasts. Also, compared with both younger and older normal-hearing groups, the presence of age-related hearing loss will result in additional N1 and P2 latency delays as well as amplitude reductions.
Section snippets
Participants
Participants were 10 young normal-hearing (mean=26.3 years; range=19–32 years), 10 older normal-hearing (mean=68.3 years; range=61–79 years) and 10 older adults with age-related high-frequency hearing loss (mean=71.2; range=60–81 years). Audiometric thresholds for the right ear are shown in Fig. 1. To rule out any major age-related cognitive impairment, participants older than 65 years obtained a passing score of 24 or better on the mini mental status examination (Folstein et al., 1975).
Behavioral results
Older listeners, compared with younger listeners, had more difficulty discriminating 10 ms VOT contrasts (young normal-hearing group: mean d′=2.0, standard error=0.20; older normal-hearing: mean d′=1.4, standard error=0.14; older hearing-impaired: mean d′=0.94, standard error=0.15). A one-way repeated measures analysis of variance (ANOVA) revealed a significant age effect (F=10.57, df=2, P<0.001). Post hoc tests indicate that younger adults performed significantly better than older adults with (
Main findings
The present findings reinforce Strouse et al. (1998) and others (Moore et al., 1992, Fitzgibbons and Gordon-Salant, 1994, Schneider et al., 1994, Snell, 1997, Schneider and Pichora-Fuller, 2001) who report that older adults have more difficulty than younger adults perceiving temporal cues. In this experiment, older listeners (with or without hearing loss) had more difficulty than younger listeners discriminating 10 ms VOT contrasts. The presence of age-related hearing loss appears to compound
Conclusion
In conclusion, aging affects the ability to discriminate time-varying acoustic speech cues. Furthermore, aging affects temporal properties of auditory cortical responses resulting in delayed synchronous firing to the onset of voicing. Together, these brain and behavior measures suggest that some of the speech understanding difficulties expressed by elderly adults may be related to impaired temporal precision in the aging central auditory system. The problem appears to be compounded by the
Acknowledgements
This work was supported by an NIH grant, R03 AG18552-01, awarded to K.T. The authors wish to acknowledge the helpful comments of Jos Eggermont. We also thank C. Kejriwal, J. VeraSforzza, M. McFarland and C. Billings for their assistance with subject recruitment and data collection. Portions of this paper were presented at the Association for Research in Otolaryngology and American Auditory Society Meetings in 2002.
References (98)
- et al.
Temporal resolution in young and elderly subjects as measured by mismatch negativity and a psychoacoustic gap detection task
Clin Neurophysiol
(2002) - et al.
Auditory evoked potentials in aged gerbils: responses elicited by noises separated by a silent gap
Hear Res
(1996) - et al.
Neurobiologic responses to speech in noise in children with learning problems: deficits and strategies for improvement
Clin Neurophysiol
(2001) Between sound and perception: reviewing the search for a neural code
Hear Res
(2001)- et al.
Mini-mental state: a practical method for grading the cognitive state of patients for the clinician
J Psychiatr Res
(1975) - et al.
Speech recognition in noise and presbycusis: relations to possible neural mechanisms
Hear Res
(1997) - et al.
Age-related variations in evoked potentials to auditory stimuli in normal human subjects
Electroenceph clin Neurophysiol
(1978) - et al.
Deficits in auditory brainstem pathway encoding of speech sounds in children with learning problems
Neurosci Lett
(2002) Some physiological consequences of neonatal cochlear destruction in the inferior colliculus of the gerbil, Meriones unguiculatus
Brain Res
(1984)- et al.
The effects of frontal and temporal–parietal lesions on the auditory evoked potential in man
Electroenceph clin Neurophysiol
(1980)
Effect of age on auditory evoked responses (AER) and augmenting-reducing
Neurophysiol Clin
GABAA receptor binding in the aging rat inferior colliculus
Neuroscience
Age-related differences in recovery cycle of auditory evoked potentials
Neurobiol Aging
Event-related potential changes in healthy aged females
Electroenceph clin Neurophysiol
Age-related changes in auditory event-related potentials
Electroenceph clin Neurophysiol
Human auditory sustained potentials. II. Stimulus relationships
Electroenceph clin Neurophysiol
EEG and ERP assessment of normal aging
Electroenceph clin Neurophysiol
Auditory brainstem responses in younger and older adults for broadband noises separated by a silent gap
Hear Res
Parameters of temporal recovery of the human auditory evoked potential
Electroenceph clin Neurophysiol
Speech-evoked activity in primary auditory cortex: effects of voice onset time
Electroenceph clin Neurophysiol
The sources of auditory evoked responses recorded from the human scalp
Electroenceph clin Neurophysiol
Auditory brainstem response forward-masking recovery functions in older humans with normal hearing
Hear Res
Abnormal neural encoding of repeated speech stimuli in noise in children with learning problems
Clin Neurophysiol
Comparison of the auditory sensitivity of neurons in the cochlear nucleus and inferior colliculus of young and aging C57BL/6J and CBA/J mice
Hear Res
A temporal component of the auditory evoked response
Electroenceph clin Neurophysiol
Age-related changes in human middle latency auditory evoked potentials
Electroenceph clin Neurophysiol
Auditory detection, discrimination and speech processing in aging, noise sensitive and hearing-impaired listeners
Scand Audiol
Aging affects hemispheric asymmetry in the neural representation of speech sounds
J Neurosci
Auditory perception of speech contrasts by subjects with sensorineural hearing loss
J Speech Lang Hear Res
Effects of age and mild hearing loss on speech recognition in noise
J Acoust Soc Am
Representation of a voice onset time continuum in primary auditory cortex of the cat
J Acoust Soc Am
Neural correlates of gap detection in three auditory cortical fields in the cat
J Neurophysiol
Neural responses in primary auditory cortex mimic psychophysical, across-frequency-channel, gap-detection thresholds
J Neurophysiol
Age effects on measures of auditory duration discrimination
J Speech Lang Hear Res
Pathological studies in presbycusis
Arch Otolaryngol
Auditory evoked potentials in cats with neonatal high frequency hearing loss
Acta Otolaryngol
Speech understanding in the elderly
J Am Acad Audiol
Issues in evaluating the effectiveness of hearing aids in the elderly: what to measure and when
Semin Hear
Injury-and-use related plasticity in adult auditory cortex
Audiol Neurootol
The ten-twenty system of the international federation
Electroenceph clin Neurophysiol
Speech understanding in the elderly
Ear Hear
Impact of central auditory processing disorder and cognitive deficit on the self-assessment of hearing handicap in the elderly
J Am Acad Audiol
Effect of age on interaural asymmetry of event-related potentials in a dichotic listening task
J Am Acad Audiol
Responses of the human auditory cortex to vowel onset after fricative consonants
Exp Brain Res
Binaural interaction measured behaviorally and electrophysiologically in young and old adults
Audiology
Software for cascade/parallel formant synthesizer
J Acoust Soc Am
Auditory pathway encoding and neural plasticity in children with learning problems
Audiol Neurootol
Consequences of neural asynchrony: a case of auditory neuropathy
J Assoc Res Otolaryngol
Speech perception in the chinchilla: identification functions for synthetic VOT stimuli
J Acoust Soc Am
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