Age-Related Electrophysiological Changes in the Auditory Brain

C H A P T E R

9 Age-Related Electrophysiological Changes in the Auditory Brain Much of what is known about the effect of age on auditory processing in humans has been based on understanding speech-in-noise and gap detection (Chapters 3 and 5). Age-related declines in neural synchrony in the human auditory system have been inferred from recordings of brainstem and cortical auditory evoked potentials. Although the presence of a cortical auditory evoked potential may indicate that a stimulus was physiologically represented, however, this does not fully specify the encoding of this stimulus. In addition, cortical auditory evoked potentials (CAEPs) cannot discriminate between the effects of subcortical age-related changes and pure cortical changes. Subcortical electrophysiological responses may elucidate that distinction. Importantly, it is relevant to investigate whether there is a one-to-one relationship between perceptual and electrophysiological signs of agerelated hearing impairment.

9.1 BRAINSTEM AND MIDBRAIN RESPONSES IN NORMAL-HEARING ELDERLY We start with an overview of some early studies on the effects of aging on the auditory brainstem response (adding to those already covered in Chapter 2), but now in particular referring to auditory brainstem response (ABR) interpeak latencies as they may reflect central abnormalities. Otto and McCandless (1982) studied the combined effects of adult age and hearing loss on the ABR. They evaluated elderly (n 5 30; mean age 5 68.7 years), and young adults with similar sensorineural hearing

The Auditory Brain and Age-Related Hearing Impairment DOI: https://doi.org/10.1016/B978-0-12-815304-8.00009-8

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losses (n 5 30; mean age 5 30.6 years), as well as normal-hearing young adults (n 5 30; mean age 5 25.4 years). They found that hearing loss and aging resulted in greater deterioration of the click-ABR waveforms than hearing loss alone. Comparison of ABR interpeak latencies between these three groups revealed no consistent pattern of changes due to aging. Rosenhall et al. (1986) reported similar results in 209 elderly participants (mean age 5 69.8 years) with a hearing loss, and compared to young or middle-aged adults (n 5 164; mean age 5 38 years) also with a cochlear hearing loss. They found that the older individuals had generally longer ABR wave latencies than the young and middle-aged participants. The I V interpeak latency was significantly prolonged in the older age groups compared with the group of younger individuals, except for subjects with pronounced hearing loss. This suggested to Rosenhall et al. (1986) that an age-related dysfunction in the auditory brainstem might be present in presbycusis. Martini et al. (1991) reported contrasting results in the ABRs in 18 healthy males and 18 healthy females with a mean age of 67.2 years. They found a latency increase of all principal waves of ABR, reflecting the hearing loss, but without a significant change in the I V delay. Ottaviani et al. (1991) compared ABRs in 74 older adults aged 60 80 years with presbycusis (PTA0.5 4 kHz . 39 dB HL) with those from normal-hearing older (PTA0.5 4 kHz ,30 dB HL) and young adults with a sloping hearing loss (PTA0.5 4 kHz 5 31 39 dB HL). They found that the latency increase of ABR waves observed in the presbycusis group was mainly correlated with the audiometric shape of the hearing loss and not with age on its own. There were no significant differences between presbycusic and young cochlear hearing-loss adults concerning I III and I V interpeak latencies. It is fair to conclude from these early cross-sectional studies that click ABRs in general do not show indications of abnormalities in brainstem conduction time in the elderly. More recently, Clinard et al. (2010) examined the effect of age on behavioral and electrophysiological measures of frequency representation. Thirty-two adults (ages 22 77), with hearing thresholds ,25 dB HL at octave frequencies 0.25 8.0 kHz were studied. They found significant declines in frequency-discrimination differences at 500 and 1000 Hz with increasing age. Frequency-following responses were elicited by tone bursts with frequencies 463 500 Hz and 925 1000 Hz, and frequency following response (FFR) phase coherence and amplitude at those frequencies decreased significantly as age increased. Clinard et al. (2010) suggested that behavioral pitch discrimination, as reflected in frequency-discrimination differences, and neural representation strength of frequency, as reflected by FFR, declined as age increased. However, although perception and neural representation of frequency

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differences concurrently declined with age, they were not significantly correlated. Presacco et al. (2015) recorded the envelope-following response (EFR) to the speech syllables /da/ and /a/ from 15 younger (mean age 5 24.4 years) and 15 older (mean age 5 63.7 years) adults with normal hearing, normal IQ, and no history of neurological disorders. They found that the EFRs of older adults were significantly delayed with respect to younger adults for the transition and onset regions of the /da/ syllable (Fig. 9.1A) and for the onset of the /a/ vowel (Fig. 9.1B). However, in contrast with the younger adults, who had shorter latencies for /da/ than for /a/ (as was expected given the high-frequency energy in the /da/ stop consonant burst), latencies in older adults were not significantly different between the responses to /da/ and /a/. Unexpected were the amplitude and phase dissimilarities between the two groups in the later part of the steady-state region, rather than in the transition region (Fig. 9.1B). Looking at Fig. 9.1B, one notices that the peak amplitude to the vowel in /a/ decreases with time much more pronounced and rather abrupt compared to the response to /da/ in Fig. 9.1A, which is surprising to say the least. Group data (their Figure 5), however, also showed this particular difference. According to Presacco et al. (2015) this may potentially be due to reduced audibility. Since no stimulus levels were reported, other than that this was a replication of the Anderson et al. (2012) study which used a level of 80 dB sound pressure level (SPL) for the /da/ (see Chapter 5), and assuming the steady-state levels for the /da/ and /a/ were the same, this reduced audibility argument specifically for the /a/ is not valid. Alternatively, this amplitude reduction for the /a/ may indicate prolonged neural recovery or response decay associated with a loss of auditory nerve fibers. Even that is debatable since the number of periods in the /da/ was the same as for the /a/. Mamo et al. (2016) also used the envelope following response (EFR) to investigate age-related differences in periodicity encoding of the temporal envelope and fine structure components of the response to a /da/ speech token (cf. Fig. 9.1A) in 22 younger (mean age 5 23.2 years) and 22 older (mean age 5 70.5 years) adults. They found reduced amplitude of the fundamental frequency and harmonic components in the spectral domain of the recorded response of the older listeners (cf. Fig. 5.5). They then employed temporally jittered stimuli and found that the young adults showed a systematic reduction in the response amplitude of the most robust response components as the degree of applied jitter increased. In contrast, the older adults did not demonstrate significant response reduction when tested under jitter conditions. The overall pattern suggested to Mamo et al. (2016) that older adults face reduced neural synchrony for encoding periodic, complex signals at the level of the brainstem, and that

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FIGURE 9.1 (A) Stimulus waveform (top) and average brainstem responses to /da/ in the younger (red) and older (black) adults (bottom). The prestimulus and response regions are labeled with respect to the onset, formant transition, and steady-state vowel of the stimulus. (B) Stimulus waveform (top) and average brainstem responses to /a/ in the younger (red) and older (black) adults (bottom). The steady-state region in the /a/ response starts at B20 ms, but for comparison purposes with /da/, the transition region, in addition to the prestimulus, onset, steady-state, and offset regions, is also marked. Source: From Presacco, A., Jenkins, K., Lieberman, R., Anderson, S., 2015. Effects of aging on the encoding of dynamic and static components of speech. Ear Hear. 36, e352 e363. With permission from Wolters Kluwer Health.

this reduced synchrony can be modeled in young adults by simulating neural jitter via disruption of the temporal waveform of the stimulus. See also Pichora-Fuller et al. (2007) and the description of their behavioral results in Chapter 5.

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9.2 OBLIGATORY CORTICAL RESPONSES IN NORMAL-HEARING ELDERLY A primer on the various cortical auditory evoked responses is presented in the Appendix.

9.2.1 Effects of Attention The effect of selective attention on the middle latency responses (MLRs) and CAEPs deserves some introduction. The earliest attention effect that has been consistently observed in the auditory CAEP is a negative deflection, sometimes called the “negative difference wave” or “Nd” (Hansen and Hillyard, 1980). Generally, this effect can be described as a greater negativity in the CAEPs elicited by attended stimuli relative to the CAEPs elicited by ignored stimuli. The enhanced negativity may be observed as early as 50 ms poststimulus, and typically increasing the amplitude of the evoked N1 component at 80 120 ms (Woldorff and Hillyard, 1991). Furthermore, Woldorff et al. (1993) demonstrated using magnetoencephalography (MEG) and functional magnetic resonance imaging (fMRI) that tones in the attended ear evoked larger magnetic responses than did unattended tones already in the latency ranges of 20 50 ms (but only clearly visible in the M50) poststimulus onset. Source location techniques in conjunction with fMRI placed the neural generators of these early attention-sensitive brain responses, that is, the M50, in auditory cortex on the supratemporal plane. Schroeder et al. (1995) recorded CAEPs from normal elderly and young adult subjects during simple reaction time (RT) and discrimination conditions. In both response conditions, the stimuli were randomly presented, as in an auditory “oddball” paradigm. They found that an early latency attention-dependent negative component (Nd) was significantly delayed in the elderly. Although the latency of N1 was not significantly different between the groups, the latencies of N2 and P3 were significantly longer for the aged subjects. The amplitudes of N1, Nd, and N2 showed no group differences. These findings suggest that the age-related slowing of later CAEP components and behavior may be partially accounted for by delays in early attention-dependent perceptual processes, as represented by Nd.

9.2.2 Early Studies in Putatively Normal-Hearing Elderly Pfefferbaum et al. (1979) were among the first to demonstrate neurophysiological changes in the central nervous system with age, by

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recording CAEPs in healthy, aged women (n 5 8; mean age 5 78.9 years) and in young women (n 5 9; mean age 5 22.7 years). All women had relatively intact auditory acuity with auditory thresholds less than 30 dB SPL at 500 Hz, albeit that no audiograms were obtained. The CAEPs were evoked by 500 Hz tones of 60 90 dB SPL. Compared to the young, the elderly women showed decreased amplitude of the late sustained potential (SP, latency B200 ms; Appendix), and increased P2 latency. The fact that the N1 amplitude was unaltered in the aged group, while the P1 was enhanced, the SP was diminished, and the P2 showed changes in the amplitude-intensity function, suggested to Pfefferbaum et al. (1979) that these changes were not merely the result of nonspecific degradation of physiological processes. Spink et al. (1979) studied CAEPs in young (n 5 5; mean age 5 22 years) and older (n 5 5; mean age 5 63 years) adults. They found that the P2-latencies of the older subjects were significantly shorter for 60, 75, and 90 dB HL than those of the younger group, contrasting with the findings of Pfefferbaum et al. (1979). No significant difference between the two groups could be found for the N1 P2 amplitudes or the P1 and N1 latencies. Smith et al. (1980) studied CAEPs in 10 young (mean age 5 21.3 years) and 10 elderly (mean age 5 71.1 years) females using an oddball paradigm. The amplitudes of the P1, N1, and P2 components were not affected by an infrequent change in pitch of the tones or instructing subjects to count or ignore them. Compared to the young, the elderly had a larger P1 and smaller P2 amplitude and a difference in the scalp distribution of P2. Clearly, these early studies showed no concensus.

9.2.3 Recent Studies Gmehlin et al. (2011), using a passive double-click paradigm [interstimulus interval (ISI) 5 500 ms], recorded MLRs (P30 P50) and CAEPs (N1 and P2) in healthy young (n 5 20; mean age 5 26 years.) and healthy elderly subjects (n 5 23; mean age 5 72 years). No audiograms were obtained. Aging did not affect the suppression of the response amplitude to the second click relative to that for the first click. Both age groups showed clear suppression of the P50 and N1 components, whereas P30 was not attenuated (Fig. 9.2). Irrespective of age, the magnitude of suppression was most pronounced for N1. P2 amplitude was not affected. Since the P2 reflects the activity of the auditory brainstem via the reticular activating system (Ponton et al., 2000), whereas the N1 represents thalamocortical processing, this is not surprising. Gmehlin et al. (2011) concluded that inhibition of redundant information seems to be preserved with aging.

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FIGURE 9.2 Grand averages for auditory double clicks in young subjects and elderly subjects. Shown are the responses to the first (full line) and the second click (dashed line) separated by 500 ms. The grand averages were additionally band-pass filtered (1 12 Hz, 12 dB/oct) and corrected according to the 100-ms preclick baseline. Source: Reprinted from Gmehlin, D., Kreisel, S.H., Bachmann, S., Weisbrod, M., Thomas, C., 2011. Age effects on preattentive and early attentive auditory processing of redundant stimuli: is sensory gating affected by physiological aging? J. Gerontol. A Biol. Sci. Med. Sci. 66A (10), 1043 1053. By permission of Oxford University Press.

Kim et al. (2012) presented brief 100-ms duration tones (1 kHz, 60 100 dB SPL) in quiet and in the presence of continuous broadband noise (70 dB SPL) and recorded the N1 P2 responses. They found that in normal-hearing (#25 dB HL from 250 8000 Hz) older adults (n 5 8;

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FIGURE 9.3 Grand average ERPs to the frequent and infrequent stimuli recorded at Fz, Cz, and Pz for the old and young subjects. Peaks are labeled for the target responses at Fz. Source: Reprinted from Pfefferbaum, A., Ford, J.M., Roth, W.T., Kopell, B.S., 1980b. Age-related changes in auditory event-related potentials. Electroencephal. Clin. Neurophysiol. 49, 266 276. With permission from Elsevier.

mean age 5 65.8 years) the N1 latencies to tones in quiet were delayed at 60 and 70 dB SPL compared with those for younger adults (n 5 8; mean age 5 26.5 years). No significant age effects were observed for the P2 latencies and N1 P2 amplitudes in quiet between the two groups. Rufener et al. (2014) investigated electrophysiological correlates of auditory related selective attention in young (n 5 21, mean age 5 22.7 years) and older (n 5 20; mean age 5 68.1 years) healthy adults (Fig. 9.3). No audiograms were obtained. During the electroencephalography (EEG), participants were instructed to listen carefully to all of the presented stimuli. Participants were also required to respond via button press at random time intervals indicated by a question mark on the screen. Rufener et al. (2014) found that: “whereas behavioral data showed no difference in task accuracy between the two age samples irrespective of the modulation of attention, the N1 and the P2 component evoked by speech and non-speech stimuli are specifically modulated in older adults and young adults depending on the subjects’ focus of attention.” Rufener et al. (2014) noted that according to the topographical maps, N1 and P2 seem to originate from distinct neural generators and processing steps, and thus assumed that the occurrence of both the N1

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and P2 components is not an essential requirement for accomplishing the task. According to Rufener et al. (2014), the lack of an additional P2 taskrelated modulation in older adults is likely a consequence of an unspecific age-related neural degeneration process. However, as the P2 is a component that matures as early as the ABR (Ponton et al., 2000), it is understandable that only the late maturing N1 is the relevant one for cortical processing. Rufener et al. (2014) concluded that: “The most important finding, however, of this study pertains to an inconsistency between behavioral and neurophysiological data. In particular, while we observed age-related differences in the neurophysiological pattern we did not find corresponding effects in the behavioral task accuracy (i.e., discrimination between words and pseudo words, or between short and long white noise stimuli, respectively).” Harris et al. (2012) examined age-related and individual differences in CAEP amplitudes and latencies, processing speed, and gap detection from 25 younger (mean age 5 24.2 years) and 25 older adults (mean age 5 69.8 years) with normal hearing. They found that “the most obvious difference in CAEP waveforms of younger and older adults was the absence of the N2 response in many older subjects.” This corroborates earlier findings (Bertoli and Probst, 2005; Ceponiene et al., 2008) that the N2 peak most often shows a marked decrease in amplitude with age. Harris et al. (2012) noted that the N2 is likely generated in frontal attention-related brain regions such as the medial frontal areas, including anterior cingulate cortex, and the right ventral and dorsolateral prefrontal cortex. Harris et al. (2012) concluded: “The large age-related differences in N2 amplitude or absence of the N2 in older adults, and the increased variability in attention modulation of N2 amplitudes in older adults, may represent an age-related change in the structure and function of frontal attention networks.” Details on the temporal processing aspects of this study are presented in Chapter 5.

9.2.4 Effects of Presbycusis Bertoli et al. (2011) reported larger P2 amplitudes for adults with mild moderate hearing loss, who were long-term hearing aid users, and attributed the larger auditory cortical responses in adults with hearing loss to an increase in “effortful listening.” Larger P2 amplitudes have also been reported after auditory training (Shahin et al., 2003; Ross and Tremblay, 2009; Tong et al., 2009). Aging is also a factor in increased P2 amplitude and latency, possibly due to decreased central inhibition (Ross et al., 2007). Given that P2 amplitude has been associated with re-allocation of cognitive resources (Tremblay et al., 2003), it would appear that the degree of cortical reorganization increases with the severity of the hearing loss.

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9.3 PREATTENTIVE AND TASK-DEPENDENT CORTICAL RESPONSES The mismatch negativity (MNN) and the P3, among others, are modulated by cognitive processes in the brain and are collectively called event-related potentials (ERPs) (Chapter 5).

9.3.1 The P3 The P3 can be separated into two components, the P3a and P3b, indicating a preattentive and task-related component, respectively. P3a often accompanies the MMN. Typically, studies using the label P3 imply P3b. Let’s start with a note of caution pertaining to isolating the effects of hearing loss and cognition on the P3. 9.3.1.1 A Note of Caution Pollock and Schneider (1992) evoked the P3 event-related potential by auditory stimuli under two conditions: (1) 250 Hz standard, 500 Hz target and (2) 1000 Hz standard, 2000 Hz target. A group with normal hearing (n 5 10, mean age 5 52.7 years), defined as less than a 16-dB loss at each tone frequency, was compared to a group with hearing impairment (n 5 8, mean age 5 69.9 years), defined as a loss of 16 dB or more at each tone frequency. At 500 Hz, the mean loss in this group was 26 dB, and 44.4 dB at 2000 Hz. The hearing-impaired group showed significant P3 latency prolongations compared to those with normal hearing for the 2000 Hz, but not the 500 Hz target, even though subject age was used as a covariate. Under both conditions, hearing-impaired subjects showed reduced P3 amplitudes compared to those with normal hearing. This raises the possibility that some of the latency prolongations ascribed to age or cognitive processing deficits might instead be attributed to hearing impairment. This was recently amplified by Porto et al. (2016), who investigated whether differences in visual acuity influence one of the most commonly observed findings in the event-related potentials literature on cognitive aging, namely a reduction in posterior P3b amplitude and increased latency, which is typically used as an index of cognitive decision-making/updating (cf. Fig. 1.9). Neuropsychological well-matched young (n 5 26; age 18 32 years) and old adults (n 5 29; age 65 79 years) participated in a visual oddball task. Porto et al. (2016) demonstrated that the robust age-related decline in P3b amplitude to visual targets disappeared after controlling for visual acuity.

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9.3.1.2 Early P3 Studies We proceed with three early aging studies, all from the same research group, focusing on the task-related P3 component. Ford et al. (1979) used N1 and P3 components to test participants’ abilities to decrease attention to irrelevant stimuli in order to better detect target stimuli. Twelve healthy old (mean age 5 80.3 years) and 12 healthy young adults (mean age 5 22.0 years) listened to 1500-Hz tones in one ear and 800-Hz tones in the other ear. Note that audiometry was performed but only to exclude subjects with threshold levels greater than 30 dB SPL at 500 Hz (cf. Fig. 2.1 for average audiograms per age group). Infrequently, the frequency of either tone was raised to function as the target. During one run, infrequent tones in the right ear were targets, and in the other run those in the left ear were targets. The participants were asked to count the targets. For both groups, the early N1 component was larger to tones in the attended ear than in the unattended ear, and the P3 component was largest to the targets. This suggests that both age groups can attenuate irrelevant stimuli and can use stimulus probability information in this task. P3 latency was longer for old subjects (cf. Fig. 1.9) and this indicated to Ford et al. (1979) that these took longer to decide stimulus relevance. However, in the light of our caution in the previous section, they may have had a greater hearing loss in the test frequencies compared to the controls (cf. Fig. 2.1). This caution applies to nearly all of the following studies. Pfefferbaum et al. (1980a) obtained single-trial P3 responses in healthy young (n 5 12; mean age 5 23 years) and elderly (n 5 8; mean age 5 83 years) women during a memory retrieval task of digits. No audiograms were obtained. They reported that P3 amplitude was smaller, P3 latency and RT were longer for older subjects, and the relationship between P3 latency and RT was considerably altered in the elderly. The old subjects had lower single-trial P3 RT correlations and longer P3 peak latency than did the young subjects. Pfefferbaum et al. (1980b) then tested elderly (n 5 12; mean age 5 78.6 years) and young (n 5 12; mean age 5 22.5 years) women in a reaction-time task designed to elicit middle and late event-related potentials. Auditory thresholds were obtained only at 1000 Hz. Tones of 1000 Hz (72% of the time), 500 Hz (14%), and 2000 Hz (14%) were presented randomly. The subject was instructed to press a button when one of the two types of infrequent tones occurred. The aged subjects differed from the young with respect to the later-occurring ERP components: P2 was larger and had a longer latency; P3 had a longer latency and had a different scalp distribution, and the slow (or sustained) wave (SW) was smaller. In contrast, no agerelated differences were found for N1 amplitude or latency (Fig. 9.3). Pfefferbaum et al. (1980b) found it surprising that the old subjects

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responded as quickly and as accurately as the young. Furthermore, the single-trial variability of RT and of P3 latency was no different between the old subjects than the young. There were no P3 RT correlation differences between old and young. They attributed this to the simplicity of the task. 9.3.1.3 Reaction Time, Neuropsychological Tests, and P3 Do ERPs, in particular the P3, relate to behavioral responses? Ford et al. (1982) collected P3 responses in 10 young (mean age 5 22 years) and 10 elderly (mean age 5 77 years) women for random sequences of 1000- and 1500-Hz tone pips in a two-alternative, forced choice, RT task. Audiometry was performed in the elderly participants to exclude people with thresholds .30 dB SPL at 500 Hz. Trials were sorted and averaged according to the sequence of the preceding four tones [1000 (A) or 1500 (B) Hz]: continuations of repetitions (AAAAA) and discontinuations of repetitions (BBBBA). For both groups the P3 component of the event-related brain potentials was larger and later to discontinuations than continuations. Mean RT did not differ between the two groups, although P3 latencies were significantly longer for the elderly group. Picton et al. (1984) recorded event-related brain potentials from 72 normal subjects aged 20 79 years. All subjects were screened for normal hearing at 20 dB above normal threshold for 1000- and 2000-Hz tones. The ERP to a detected improbable signal (2000 Hz, probability 5 10%) in a series of 1000-Hz tones (90%) contained a P3. The latency of the P3 wave in the response to the auditory signal increased regularly with increasing age at a rate of 1.36 ms per year, and its amplitude decreased at a rate of 0.18 µV per year. The change in the latency of the P3 wave occurred independently of any change in the reaction time, which showed no significant age-related change. Pratt et al. (1989) compared older subjects (average age 5 66 years) to a younger group (average age 5 29 years) at a memory test. No audiograms were reported. The items tested were verbal (digits) and nonverbal (musical notes). Digits were presented in the auditory and visual modalities, and notes were presented acoustically. Reaction times and performance accuracy were computed. ERPs to target notes in an auditory target-detection (“oddball”) task were recorded for comparison with the memory tasks. Reaction limes were longer in older subjects than in younger subjects for all stimulus types and set sizes. For the potentials evoked by the probes, the younger group had consistently larger late parietal components (P3b) than the older group, whereas the late frontal potentials (P3a) were larger for the older than younger subjects. Except for visual stimuli, the latencies of the parietal-SPs were not influenced by subject age in contrast to the uniform changes in RT for all stimulus types. Coyle et al. (1991) examined the effects of age on

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ERPs elicited during a two-tone (1 kHz, frequent, probability 5 90%; and 2 kHz, deviant, probability 5 10%) discrimination (“oddball”) task in 97 normal subjects aged from 17 to 80 years. No audiograms were obtained. Strong relationships were found between age and the latencies of the later ERP components N2 and P3. There was no significant difference between the mean RT’s per decade of younger and older subjects. Despite the fact that the mean correlations between RT and P3 and between RT and N2 were significant, the correlation between age and RT was not significant. Iragui et al. (1993) recorded ERPs from 71 healthy individuals between 18 and 82 years of age during performance of a disjunctive RT task in an auditory oddball paradigm. A cursory hearing test was performed. They found no significant slowing of the reaction times of the elderly subjects in relation to the younger ones. However, the peak latencies of both the N1 and P2 components elicited by standard tones were significantly slowed with age. In the ERPs of target tones, the N2, P3, and SW showed a linear increase in latency as a function of age. In general, aging was associated with less negativity (both N2 and SW) and more positivity (P3) over the anterior scalp, together with a smaller P3 and a more pronounced N2 over posterior scalp areas. Iragui et al. (1993) noted that: “The lack of a relationship between P3 latency and RT supports the view that these two measures reflect at least partially different sets of cognitive processes, where RT is sensitive to response selection and organization factors.” Bahramali et al. (1999) investigated the effects of age on late component (N1, P2, N2, and P3) ERPs and RT in 50 adults, 18 70 years of age. No audiograms were measured. A conventional auditory oddball paradigm was used. An equal number of subjects were examined in each age decade. They found no significant associations between ERP components amplitude and age. A significant positive correlation was found between age and N2/P3 latency. There were no significant effects of age on RT in the overall group. However, males had significant correlations between N2 latency and RT, whereas females showed significant correlations between P3 amplitude and RT. Gaa´l et al. (2007) evaluated the patterns of age-dependent changes of P3a and P3b as a function of task difficulty. The participants (age span: 19 68 years, n 5 55, divided into five equal-sized age groups) took part in an easy and a difficult two-tone oddball frequency-discrimination task with instructions to either use speed or accuracy, and in a novelty oddball task. Their hearing level revealed no more than 30 dB mean hearing loss at 0.25, 0.5, 1, and 2 kHz. However, no differentiation by age group was reported. The latency of the P3 components increased with aging. While in the easy task a linear P3b latency increase could be seen, in the difficult tasks (difficult frequency discrimination or distracting novel stimuli) an accelerated latency increase was observed for the

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P3b and P3a. In the two-tone oddball paradigm age had no effect on P3b amplitude, but in the novelty oddball task the amplitude of P3 potentials decreased with age. P3b latency as well as RT showed a significant increase in the difficult task. Gaa´l et al. (2007) reported that: “while RT is sensitive, P3b latency is relatively insensitive to demands of response selection and execution, and RT—in contrast to P3b latency—showed no age main effect in either condition.” Fjell and Walhovd (2001) administered an auditory oddball task to 72 participants (36 males and 36 females) aged 21.8 94.7 years. No audiometry was performed. In addition, participants were assessed using the Wechsler Abbreviated Scales of Intelligence and digit span from the Wechsler Adult Intelligence Scales—Revised. The activity generated from different brain areas changed at different rates with age. While the posterior area showed a clear reduction of P3 amplitude and an increase of P3 latency with age, the amplitude did not decrease at the same rate in the frontocentral areas, and there was at the same time a marked hemispheric asymmetry in the age-dependent change of activation. The digit span was the single measure that correlated with P3 amplitude, corroborating that P3 amplitude indexes brain actions stemming from maintenance of working memory. Fjell and Walhovd (2001) found that “there were no significant correlations between neuropsychological measures and the right frontal factor, neither for amplitude, nor for latency, but significant correlations with mainly digit span were found for the left frontal factor for both amplitude and latency. This may imply the existence of important topographical differences in the relationship between neuropsychological and electrophysiological measures.” We may conclude that the elderly show an apparent discrepancy between behavioral cognitive tests such as reaction times and electrophysiological outcomes.

9.3.2 The Mismatch Negativity Another event-related potential that traces preattentive brain changes to low-probability sounds is the mismatch negativity, which is often accompanied by the also preattentive, attention-orienting response, P3a. Czigler et al. (1992) recorded ERPs to frequent (standard; 950 Hz, 90%) and infrequent (deviant; 1045 Hz, 10%) auditory stimuli in older (n 5 8; mean age 5 60.8 years) and younger (n 5 8; mean age 5 21.3 years) subjects. Participants had no hearing loss in the frequency range of the stimuli used in the study. In various blocks the ISI was either 800, 2400, or 7200 ms. During the recordings the subjects read books, and ignored the auditory stimuli. The amplitude of the N1 and the amplitude and latency of the P2 increased with increasing ISI.

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The P2 amplitude was larger in the younger group. In the 120 180-ms latency range the deviant stimuli elicited more negative ERPs than the standard stimuli. The amplitude of the MMN—taken as the difference between deviant and standard ERPs—did not change significantly as a function of ISI at electrode positions Fz and Cz (Fig. 9.4). MMN was larger in the younger group, suggesting that the younger subjects were more sensitive to the deviant stimuli. For the two shorter ISIs, the MMN in the younger group was followed by a positive wave (P3a). The emergence of this component is an indication of the increased activity of the orienting system in the younger subjects, in comparison to the older age group. Pekkonen et al. (1996) presented sequences of standard (probability 85%) and deviant (probability 15%) tones to 13 healthy younger (mean age 5 22 years) and 13 older (mean age 5 59 years) adults. Deviant stimuli were, in separate blocks, of either occasional shorter duration or higher frequency. They found that MMNs for both types of deviants with the 0.5-seconds ISI were affected by aging. This finding indicates that automatic stimulus discrimination per se is not impaired with normal aging. When the tones were attended to, deviant tones also elicited an N2b component that partly overlapped with the MMN. However,

Deviant standard difference waves 800 ms ISI

2400 ms ISI

7200 ms ISI

Fz

Cz

Pz S+ 100 200 300 400 ms 2 µV –

S 100 200 300 400 ms

S 100 200 300 400 ms

Younger age group

Older age group

FIGURE 9.4 Group average of deviant minus standard difference potentials in the older and younger age groups at the three ISIs. Source: Reprinted from Czigler, I., Csibra, G., Csontos, A., 1992. Age and inter-stimulus interval effects on event-related potentials to frequent and infrequent auditory stimuli. Biol. Psychol. 33, 195 206. With permission from Elsevier.

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with a 4.5-seconds ISI the MMN was attenuated significantly more in the older than younger subjects. This suggested to Pekkonen et al. (1996) that the stimulus trace for frequent stimuli decays faster or that involuntary attention switching is less sensitive with aging. Amenedo and Dı´az (1998) elicited the preattentive MMN and the N2b during a selective dichotic-listening task in 16 young females (mean age 5 31 years), 16 middle-aged females (mean age 5 49 years), and 19 elderly females (mean age 5 70 years) to evaluate automatic and effortful memory comparison of auditory stimuli. Participants had no auditory problems. Amenedo and Dı´az (1998) found that MMN latency and amplitude were quite stable regardless of age, while N2b latency was significantly longer in middle-aged and elderly subjects than in young subjects. Cooper et al. (2006) measured MMN responses of an elderly (n 5 21, mean age 5 69 years) and a young (n 5 27, mean age 5 21 years) group. Thresholds were obtained at 500 and 1000 Hz and were on average ,15 dB HL. Standard tones (probability 85%) used were 800 Hz and the deviant (probability 15%) was 550 Hz. They used both a duration- and a frequency-deviant tone at a short (450 ms) and long (3 seconds) stimulus-onset asynchrony (SOA). A smaller and longer latency MMN was observed in the elderly relative to the young group across SOA and deviant conditions. They found the results consistent with an age-related deficit in the encoding of sound properties in auditory sensory memory (ASM). Schiff et al. (2008) recorded ERPs in 72 normal subjects, aged 20 80 years, with 10 12 subjects per age decade. No audiograms were taken. Four blocks of short tones were delivered (20% rare 2000 Hz and 80% frequent 1000 Hz, presented at 110 dB SPL). In the first two blocks, subjects performed a distracting visual search task (distracted condition); in the latter two blocks, they had to attend to the occurrence of the rare tones (active condition). Schiff et al. (2008) found that the rare frequent difference in the N1 amplitude was greater in the active, that is, attention, than in distracted condition. MMN amplitude decreased with age. N2b and P3 latencies increased with age, while their amplitudes decreased. Females had larger-amplitude P3 than males. In the elderly, P3 latency was longer in the second block than in the first. Thus, Schiff et al. (2008) “detected a higher influence of aging on late cognitive processes (P3) than on the perceptual (N1) and preattentive (MNN) ones.” Rimmele et al. (2012) investigated age effects on ASM processing of temporal and frequency aspects of two-tone patterns using a passive listening protocol. All had PTA0.25 2 kHz , 35 dB SPL. The P1 component, the MMN, and the P3a component of event-related brain potentials to tone frequency and temporal pattern deviants were recorded in younger (n 5 13, mean age 5 25.2 years) and older (n 5 13, mean age 5 66.6 years) adults. These components served as measures of auditory event

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detection (P1), ASM processing (MMN), and attention switching (P3a). Compared to the younger group, MMN amplitude was smaller for both frequency and temporal deviants in older adults, indicating that automatic processing of both frequency and temporal aspects of two-tone patterns is impaired in older adults. Furthermore, P3a was elicited only in the younger adults, suggesting a failure to initiate an attention switch, and indicating that impaired ASM processing of patterns may lead to less distractibility in older adults. Rimmele et al. (2012) concluded: “that impaired sensory memory processing may have an impact on attentional orienting (indexed by P3a), which might lead to perceptual deficits in everyday situations.”

9.3.3 Very Long-Latency ERPs; the N450 Passow et al. (2014) investigated electrophysiological correlates of processing conflicts between attentional focus and perceptual saliency in 25 younger (mean age 5 25.8 years) and 26 older (mean age 5 70.0 years) adults, all with hearing thresholds not exceeding 35 dB HL from 250 Hz to 3 kHz. Participants were instructed to attend to the right or left ear, and perceptual saliency was manipulated by varying the intensities of both ears. They found that: “Attentional control demand—as reflected in the N450—was higher in conditions when attentional focus and perceptual saliency favored opposing ears than in conditions without such conflicts. Relative to younger adults, older adults modulated their attention less flexibly and were more influenced by perceptual saliency.” Passow et al. (2014) found that “the magnitude of the N450 modulation effect correlated positively with task performance. In line with lower attentional flexibility, the ERP waveforms of older adults showed absence of the late negativity and the modulation effect.” This suggests that aging compromises the activation of the frontoparietal attentional network when processing competing and conflicting auditory information.

9.4 AGING MUSICIANS Zendel and Alain (2014) investigated the effects of lifelong musicianship on auditory ERPs in younger (n 5 14; mean age 5 28.1 years) and older musicians (n 5 15; mean age 5 69 years), and young (n 5 15; mean age 29.9 years) and older nonmusicians (n 5 13; mean age 5 69.2 years), while they either attended to auditory stimuli or watched a muted subtitled movie of their choice. All younger adults had clinically normal hearing. Older nonmusicians with mild hearing loss were recruited so

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that pure-tone thresholds in older nonmusicians did not differ from those in older musicians (who often suffer noise-induced hearing loss). Both age and musical training-related differences were observed in the obligatory P1 N1 P2 components; however, the differences between musicians and nonmusicians were similar across the lifespan. That is, P1 N1 P2 were enhanced in musicians, but decline with age at the same rate. On the other hand, attention-related long-latency ERPs were selectively enhanced in older musicians, suggesting that they use a compensatory strategy to overcome age-related decline in obligatory processing of acoustic information. O’Brien et al. (2015) used harmonic tone complexes to evoke CAEPs, including P1 N1 P2, MMN, and P3a. Data from older adult musicians (n 5 8, mean age 5 62.5 years) and nonmusicians (n 5 8, mean age 5 61.4 years) were compared to previous data from young adult musicians (n 5 40; mean age 5 22 years) and nonmusicians (n 5 20; mean age 5 23 years). All participants had clinically normal pure-tone thresholds for the frequencies of interest in the present study (#3000 Hz). They found that P1 N1 P2 amplitudes and latencies did not differ between older adult musicians and nonmusicians; however, MMN and P3a latencies for harmonic tone deviances were earlier for older musicians than older nonmusicians. Comparisons of P1 N1 P2, MMN, and P3a components between older and young adult musicians and nonmusicians suggest that P1 and P2 latencies are significantly affected by age, but not musicianship, while MMN and P3a appear to be more sensitive to effects of musicianship than aging. O’Brien et al. (2015) concluded that: “Findings support beneficial influences of musicianship on central auditory function and suggest a positive interaction between aging and musicianship on the auditory neural system.”

9.5 THE OCCASIONAL DISCREPANCY BETWEEN BEHAVIOR AND ELECTROPHYSIOLOGY I want to emphasize here the apparent discrepancy between behavioral cognitive tests and electrophysiological outcomes. The behavioral tests have been sorted into reaction times, and neuropsychology tests. It should be noted again that changes in the P3 latency are putatively sensitive to high-frequency hearing loss.

9.5.1 Reaction Time Older subjects had lower single-trial P3 RT correlations and longer P3 peak latency compared with the young subjects (Pfefferbaum et al., 1980a). Mean RT did not differ between the two groups, although P3 III. COMPENSATORY CHANGES IN THE AGING BRAIN

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latencies were significantly longer for the elderly group (Ford et al., 1982; Picton et al., 1984). Strong relationships were found between age and the latencies of the N2 and P3 components. The mean correlations between RT and P3 and between RT and N2 were significant, whereas the correlation between age and RT was not (Coyle et al., 1991; Bahramali et al., 1999). RT in contrast to P3b latency showed no main age effect in either condition (Gaa´l et al., 2007).

9.5.2 Neuropsychology Tests There were no significant correlations between neuropsychological measures and the right frontal factor, neither for amplitude, nor for latency, but significant correlations with mainly digit span were found for the left frontal factor for both amplitude and latency of P3 (Fjell and Walhovd, 2001). “A smaller and longer latency MMN was observed in the elderly relative to the young group across SOA and deviant conditions, which was consistent with an age-related deficit in the encoding of sound properties in ASM" (Cooper et al., 2006). There was a higher effect of aging on late cognitive processes (P3) than on the perceptual (N1) and preattentive (MNN) ones (Schiff et al., 2008). Although perception and neural representation concurrently declined with age they were not significantly correlated (Clinard et al., 2010). Age-related differences in the neurophysiological pattern were observed but not in the behavioral task accuracy (Rufener et al., 2014).

9.6 SUMMARY Age-related declines in neural synchrony in the human auditory system have been inferred through the use of cortical auditory evoked potentials. One frequently used auditory cortical evoked response is the P1 N1 P2 complex, and age-related differences affecting its latency and amplitude have been reported. Although the presence of a CAEP response indicates that a stimulus was physiologically discriminated, its presence neither quantifies the quality of stimulus encoding nor indicates if subcortical age-related changes, such as reduced neural synchrony, contribute to elevated cortical thresholds in older adults. Inconsistencies between behavioral and CAEP data, in particular, age-related differences in the neurophysiological pattern without corresponding effects in the behavioral task accuracy were found. Typically, a higher influence of aging on late cognitive processes than on the perceptual (N1) and preattentive (MNN) ones is found. In particular, a reduced MMN response to duration and frequency deviants is a robust feature among aged adults, which is due to a decline in frontal-based control mechanisms, with alterations in connectivity between temporal and frontal regions. III. COMPENSATORY CHANGES IN THE AGING BRAIN

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References Amenedo, E., Dı´az, F., 1998. Automatic and effortful processes in auditory memory reflected by event-related potentials. Age-related findings. Electroencephalogr. Clin. Neurophysiol. 108, 361 369. Anderson, S., Parbery-Clark, A., White-Schwoch, T., Kraus, N., 2012. Aging affects neural precision of speech encoding. J. Neurosci. 32, 14156 14164. Bahramali, H., Gordon, E., Lagopoulos, J., Lim, C.L., Li, W., Leslie, J., et al., 1999. The effects of age on late components of the ERP and reaction time. Exp. Aging Res. 25 (1), 69 80. Bertoli, S., Probst, R., 2005. Lack of standard N2 in elderly participants indicates inhibitory processing deficit. Neuroreport 16, 1933 1937. Bertoli, S., Probst, R., Bodmer, D., 2011. Late auditory evoked potentials in elderly longterm hearing-aid users with unilateral or bilateral fittings. Hear. Res. 280, 58 69. Ceponiene, R., Westerfield, M., Torki, M., Townsend, J., 2008. Modality-specificity of sensory aging in vision and audition: evidence from event-related potentials. Brain Res. 1215, 53 68. Clinard, C.G., Tremblay, K.L., Krishnan, A.R., 2010. Aging alters the perception and physiological representation of frequency: evidence from human frequency-following response recordings. Hear. Res. 264, 48 55. Cooper, R.J., Todd, J., McGill, K., Michie, P.T., 2006. Auditory sensory memory and the aging brain: a mismatch negativity study. Neurobiol. Aging 27, 752 762. Coyle, S., Gordon, E., Howson, A., Meares, R., 1991. The effects of age on auditory eventrelated potentials. Exp. Aging Res. 17 (2), 103 111. Czigler, I., Csibra, G., Csontos, A., 1992. Age and inter-stimulus interval effects on eventrelated potentials to frequent and infrequent auditory stimuli. Biol. Psychol. 33, 195 206. Fjell, A.M., Walhovd, K.B., 2001. P300 and neuropsychological tests as measures of aging: scalp topography and cognitive changes. Brain Topogr. 14 (1), 25 40. Ford, J.M., Hink, R.F., Hopkins, W.F., Roth, W.T., Pfefferbaum, A., Kopell, B.S., 1979. Age effects on event-related potentials in a selective attention task. J. Gerontol. 34 (3), 388 395. Ford, J.M., Duncan-Johnson, C.C., Pfefferbaum, A., Kopell, B.S., 1982. Expectancy for events in old age: stimulus sequence effects on P300 and reaction time. J. Gerontol. 37 (6), 696 704. Gaa´l, Z.A., Csuhaj, R., Molna´r, M., 2007. Age-dependent changes of auditory evoked potentials—effect of task difficulty. Biol. Psychol. 76, 196 208. Gmehlin, D., Kreisel, S.H., Bachmann, S., Weisbrod, M., Thomas, C., 2011. Age effects on preattentive and early attentive auditory processing of redundant stimuli: is sensory gating affected by physiological aging? J. Gerontol. A. Biol. Sci. Med. Sci. 66A (10), 1043 1053. Hansen, J.C., Hillyard, S.A., 1980. Endogenous brain potentials associated with selective auditory attention. Electroencephalogr. Clin. Neurophysiol. 49, 277 290. Harris, K.C., Wilson, S., Eckert, M.A., Dubno, J.R., 2012. Human evoked cortical activity to silent gaps in noise: effects of age, attention, and cortical processing speed. Ear Hear. 33 (3), 330 339. Iragui, V.J., Kutas, M., Mitchiner, M.R., Hlllyard, S.A., 1993. Effects of aging on eventrelated brain potentials and reaction times in an auditory oddball task. Psychophysiology 30, 10 22. Kim, J.-R., Ahn, S.-Y., Jeong, S.-W., Kim, L.-S., Park, J.-S., Chung, S.-H., et al., 2012. Cortical auditory evoked potential in aging: effects of stimulus intensity and noise. Otol. Neurotol. 33, 1105 1112.

III. COMPENSATORY CHANGES IN THE AGING BRAIN

REFERENCES

225

Mamo, S.K., Grose, J.H., Buss, E., 2016. Speech-evoked ABR: effects of age and simulated neural temporal jitter. Hear. Res. 333, 201 209. Martini, A., Comacchio, F., Magnavita, V., 1991. Auditory evoked responses (ABR, MLR, SVR) and brain mapping in the elderly. Acta Otolar. 111 (sup476), 97 104. O’Brien, J.L., Nikjeh, D.A., Lister, J.J., 2015. Interaction of musicianship and aging: a comparison of cortical auditory evoked potentials. Behav. Neurol. Available from: https:// doi.org/10.1155/2015/545917. Article ID 545917. Ottaviani, F., Maurizi, M., D’alatri, L., Almadori, G., 1991. Auditory brainstem responses in the aged. Acta Otolar. 111 (sup476), 110 113. Otto, W.C., McCandless, G.A., 1982. Aging and auditory site of lesion. Ear Hear. 3 (3), 110 117. Passow, S., Westerhausen, R., Hugdahl, K., Wartenburger, I., Heekeren, H.R., Lindenberger, U., et al., 2014. Electrophysiological correlates of adult age differences in attentional control of auditory processing. Cereb. Cortex 24, 249 260. Pekkonen, E., Rinne, T., Reinikainen, K., Kujala, T., Alho, K., Na¨a¨ta¨nen, R., 1996. Aging effects on auditory processing: an event-related potential study. Exp. Aging Res. 22 (2), 171 184. Pfefferbaum, A., Ford, J.M., Roth, W.T., Hopkins, W.F., Kopell, B.S., 1979. Event-related potential changes in healthy aged females. Electroencephalogr. Clin. Neurophysiol. 46, 81 86. Pfefferbaum, A., Ford, J.M., Roth, W.T., Kopell, B.S., 1980a. Age differences in P3-reaction time associations. Electroencephalogr. Clin. Neurophysiol. 49, 257 265. Pfefferbaum, A., Ford, J.M., Roth, W.T., Kopell, B.S., 1980b. Age-related changes in auditory event-related potentials. Electroencephalogr. Clin. Neurophysiol. 49, 266 276. Pichora-Fuller, M.K., Schneider, B.A., Macdonald, E., Pass, H.E., Brown, S., 2007. Temporal jitter disrupts speech intelligibility: a simulation of auditory aging. Hear. Res. 223, 114 121. Picton, T.W., Stuss, D.T., Champagne, S.C., Nelson, R.F., 1984. The effects of age on human event-related potentials. Psychophysiology 21 (3), 312 325. Pollock, V.E., Schneider, L.S., 1992. P3 from auditory stimuli in healthy elderly subjects: hearing threshold and tone stimulus frequency. Int. J. Psychophysiol. 12, 237 241. Ponton, C.W., Eggermont, J.J., Kwong, B., Don, M., 2000. Maturation of human central auditory system activity: evidence from multi-channel evoked potentials. Clin. Neurophysiol. 111, 220 236. Porto, F.H.G., Tusch, E.S., Fox, A.M., Alperin, B.A., Holcomb, P.J., Daffner, K.R., 2016. One of the most well-established age-related changes in neural activity disappears after controlling for visual acuity. NeuroImage 130, 115 122. Pratt, H., Michalewski, H.J., Patterson, J.V., Starr, A., 1989. Brain potentials in a memoryscanning task. II. Effects of aging on potentials to the probes. Electroencephalogr. Clin. Neurophysiol. 72, 507 517. Presacco, A., Jenkins, K., Lieberman, R., Anderson, S., 2015. Effects of aging on the encoding of dynamic and static components of speech. Ear Hear. 36, e352 e363. Rimmele, J., Sussman, E., Keitel, C., Jacobsen, T., Schro¨ger, E., 2012. Electrophysiological evidence for age effects on sensory memory processing of tonal patterns. Psychol. Aging 27 (2), 384 398. Rosenhall, U., Pedersen, K., Dotevall, M., 1986. Effects of presbycusis and other types of hearing loss on auditory brainstem responses. Scand. Audiol. 15 (4), 179 185. Ross, B., Tremblay, K., 2009. Stimulus experience modifies auditory neuromagnetic responses in young and older listeners. Hear. Res. 248, 48 59. Ross, B., Fujioka, T., Tremblay, K.L., Picton, T.W., 2007. Aging in binaural hearing begins in mid-life: evidence from cortical auditory-evoked responses to changes in interaural phase. J. Neurosci. 27, 11172 11178.

III. COMPENSATORY CHANGES IN THE AGING BRAIN

226

9. AGE-RELATED ELECTROPHYSIOLOGICAL CHANGES IN THE AUDITORY BRAIN

Rufener, K.S., Liem, F., Meyer, M., 2014. Age-related differences in auditory evoked potentials as a function of task modulation during speech nonspeech processing. Brain Behav. 4 (1), 21 28. Schiff, S., Valenti, P., Andrea, P., Lot, M., Bisiacchi, P., Gatta, A., et al., 2008. The effect of aging on auditory components of event-related brain potentials. Clin. Neurophysiol. 119, 1795 1802. Schroeder, M.M., Lipton, R.B., Ritter, W., Giesser, B.S., Vaughan, H.G., 1995. Event-related potential correlates of early processing in normal aging. Int. J. Neurosci. 80 (1 4), 371 382. Shahin, A., Bosnyak, D.J., Trainor, L.J., Roberts, L.E., 2003. Enhancement of neuroplastic P2 and N1c auditory evoked potentials in musicians. J. Neurosci. 23, 5545 5552. Smith, D.B.D., Michalewski, H.J., Brent, G.A., Thompson, L.W., 1980. Auditory averaged evoked potentials and aging: factors of stimulus, task and topography. Biol. Psychol. 11, 135 151. Spink, U., Johannsen, H.S., Pirsig, W., 1979. Acoustically evoked potential: dependence upon age. Scand. Audiol. 8 (1), 11 14. Tong, Y., Melara, R.D., Rao, A., 2009. P2 enhancement from auditory discrimination training is associated with improved reaction times. Brain Res. 1297, 80 88. Tremblay, K.L., Piskosz, M., Souza, P., 2003. Effects of age and age-related hearing loss on the neural representation of speech cues. Clin. Neurophysiol. 114, 1332 1343. Woldorff, M.G., Hillyard, S.A., 1991. Modulation of early auditory processing during selective listening to rapidly presented tones. Electroencephalogr. Clin. Neurophysiol. 79, 170 191. Woldorff, M.G., Gallen, C.C., Hampson, S.A., Hillyard, S.A., Pantev, C., Sobel, D., et al., 1993. Modulation of early sensory processing in human auditory cortex during auditory selective attention. Proc. Natl. Acad. Sci. U.S.A. 90, 8722 8726. Zendel, B.R., Alain, C., 2014. Enhanced attention-dependent activity in the auditory cortex of older musicians. Neurobiol. Aging 35, 55 63.

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