Effects of Contralateral Speech Competition on Auditory Event-Related Potentials Recorded from Elderly Listeners : Brain Map Study

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1 J Am Acad Audiol 9 : (1998) Effects of Contralateral Speech Competition on Auditory Event-Related Potentials Recorded from Elderly Listeners : Brain Map Study Murvin R. Hymel* Jerry L. Cranford* Andrew Stuart* Abstract Topographic brain mapping was used to investigate the ability of young and elderly female listeners to attend to tones at one ear in the presence of speech competition at the opposite ear. An oddball stimulus presentation paradigm was used to record the NJ, P2, and P300 ponents of the late auditory com- evoked potential from 19 scalp locations. With speech competition, elderly listeners exhibited significantly larger reductions in N, amplitude than did young listeners. This suggests that N, may provide an electrophysiologic index of age-related breakdowns in processing sounds in the presence of background competition. An unexpected difference was also found between young and elderly listeners in P300 scalp topography. While the young listeners' P300 response was centered at midline for both left and right ear stimulation, the elderly participants had P300 maxima centered in the parietal area of the hemisphere located contralateral to the test ear. This suggests that some ofthe functional properties (e.g., timing, strength, orientation) of the P300 neural generators may change with age or, alternatively, that different generators may be operative in elderly listeners. Key Words: Auditory event-related potentials, auditory evoked potentials, brain map, elderly listeners, NJ, P3oo, P2, scalp topography, speech competition Abbreviations : CID = Central Institute for the Deaf ; ECI = Electro-Cap International, Inc. ; EEG = electroencephalographic activity ; GFP = global field power ; LAEP = late auditory evoked potential ; PTA = average of pure-tone threshold hearing levels at 500, 1000, and 2000 Hz ; SRT = speech reception threshold ; SSI-CCM = Synthetic Sentence Identification test with contralateral competing message ; WRS = word recognition score frequent complaint of elderly listeners is that, while they have no serious difficulties understanding speech in quiet A environments, they do have significant problems in listening environments containing noise competition (Bergman, 1980 ; Marshall, 1981). Traditional audiometric tests involving puretone threshold and speech recognition measures provide little assistance in understanding the nature of this problem. Behavioral test paradigms that have been "sensitized" by deliberate "Department of Communication Sciences and Disorders, East Carolina University, Greenville, North Carolina Reprint requests : Jerry L. Cranford, Department of Communication Sciences and Disorders, East Carolina University, Greenville, NC distortion of the primary signal or introduction of competing signals (Bocca and Calearo, 1963) can provide useful insights. With behavioral measures, however, it is frequently difficult to identify the stage or level in the nervous system where the apparent breakdown in processing of auditory information is occurring. Breakdowns in performance on specific tasks could be the result of peripheral hearing impairment (input stage), language or cognitive processing dysfunctions (e.g., memory or attention problems), or motor-speech disorders (output stage). Psychological factors such as motivation or conservative response criteria may also contribute to apparent poor performance by some elderly persons (Rees and Botwinick, 1971 ; Potash and Jones, 1977).

2 Journal of the American Academy of Audiology/Volume 9, Number 5, October 1998 The use of evoked potentials can provide a more objective means of investigating age-related changes in the central auditory processing skills of elderly persons. Most evoked potential studies with elderly listeners have followed the audiologic tradition of using "pure" (i.e., undistorted) signals without any form of auditory competition. These studies also typically required no more than a passive listening response. Using this approach, past studies have shown some indications of age-related changes in all three time domains (auditory brainstem, middle latency, and late latency responses), although the effects were frequently subtle (Kileny, 1985 ; Rosenhall et al, 1985 ; Woods and Clayworth, 1986). In contrast to traditional evoked potentials, test paradigms involving the recording of event-related potentials have been successfully used by some researchers to investigate physiologic brain processes associated with the active processing of stimulus information (Hillyard et al, 1973 ; Ford and Pfefferbaum, 1980 ; Hillyard and Kutas, 1983 ; Kutas and Hillyard, 1984 ; Alho, 1992). In these tests, brain potentials are recorded to specific stimuli that listeners are either actively attending or ignoring. These studies have identified possible neural mechanisms associated with both active and passive auditory attentional processing in the brain. One such line of research, beginning with the pioneering work of Steven Hillyard and colleagues, has uncovered important evidence that the Ni component of the late auditory evoked potential (LAEP) may involve the overlapping summed activity of a number of neural subcomponents that reflect independent exogenous and endogenous processes related to discrimination, selective attention, and memory (Hillyard et al, 1973 ; Parasuraman, 1978 ; Naatanen and Picton, 1987 ; Giard et al, 1988, 1991 ; Woods, 1990). One of the present authors (Martin and Cranford, 1989 ; Cranford and Martin, 1991) performed an electrophysiologic study designed to investigate whether speech competition at one ear might interfere with the listeners' ability to selectively attend to stimuli at the opposite ear. This study investigated possible age-related effects of contralateral speech competition on the N1_P2 component of the LAEP recorded from the opposite ear. While both young and elderly female listeners showed significant decreases in Ni P2 peak-to-peak amplitudes in the presence of speech competition, the magnitude of this effect was significantly greater for the elderly participants. This finding suggests the possibility of some form of decline in the ability of elderly persons to process sounds at one ear when potentially distracting or competing sounds are present at the opposite ear. One limitation of the Cranford and Martin (1991) study was that potentials were recorded from only one recording site, the vertex (C.). This precluded obtaining any information related to possible differences in the scalp distribution of the different components of the LAEP in the presence or absence of contralateral competition. In recent years, topographic brain mapping techniques have been successfully used (Giard et al, 1988, 1991) to document the possible existence of several different attention-related neural processes in the human brain. The present report describes findings from a study that used brain mapping to further investigate possible agerelated effects of speech competition on the LAER This study investigated whether different patterns of topographic brain activity might distinguish persons who have problems attending to sounds in the presence of background competition from those who do not. Participants METHOD Ten adult females were tested in each of two age groups : a "young" group, 20 to 35 years of age, and an "elderly" group, 65 to 80 years of age. The young group (mean = 27 years, 3 months ; range = 22 years, 6 months to 33 years, 6 months) were volunteers from the university student body. The elderly group (mean = 70 years, 0 months ; range = 65 years, 2 months to 78 years, 3 months) were volunteers recruited from church and fitness programs within the community. Women were exclusively selected to preclude possible systematic gender differences in topographic location of LAEP wave components (Baumann et al, 1991). All participants were right handed and had a negative history of neurologic disorders, head trauma and/or surgery, otologic disease (including otitis media), vertigo or persistent tinnitus, ototoxic drug use, speech and language disorders, and significant occupational and recreational noise exposure. All participants from the older group were ambulatory and in good health. Apparatus and Procedures Audiometric Testing A battery of audiometric tests was administered to all participants while they were seated 386

3 Auditory Event-Related Potentials in Elderly Listeners/Hymel et al Table 1 Mean Audiometric Test Results Young Group Elderly Group (n = 10) (n = 10) Mean SD Mean SD Pure-Tone Average (db HL) Left ear Right ear Speech Reception Threshold (db HL) Left ear Right ear Word Recognition Score (%) Left ear Right ear SSI-CCM Score (%) Left ear Right ear in a sound-treated test booth, the mean results of which are shown in Table 1. Pure-tone average (PTA) thresholds at 500, 1000, and 2000 Hz were better than 20 and 30 db HL for all young and elderly participants, respectively. Interaural differences in PTA thresholds were 10 db HL or less for all participants. Speech recognition thresholds (SRTs) were obtained using Central Institute for the Deaf (CID) W-1 word lists. Word recognition scores (WRSs) were obtained at 40 db SL re the SRT using CID W-22 word lists, and were better than 92 percent for all participants. In addition to these speech tests, the Synthetic Sentence Identification test (Speaks and Jerger, 1965) with contralateral competing message (SSI-CCM) was presented to assess the possibility of central auditory processing problems in both young and elderly participants. This test was presented at 40 db SL (re the SRT) with a 0 message-to-competition ratio. The SSI-CCM scores of all participants were no lower than 8 percent below their respective WRSs. According to the criterion of Stach et al (1990), SSI scores must be 15 percent or more below the WRS to indicate the possibility of central auditory processing dysfunction. All speech material, including the SSI, was presented by the Department of Veterans Affairs Speech Recognition and Identification Materials Disc 1.1 compact disc. Finally, tympanometry screening revealed normal middle ear function (ASHA, 1990). Electrophysiologic Testing An "oddball" stimulus paradigm (Squires and Hecox, 1983) was used to evoke the LAEP. The frequent stimulus event consisted of Hz tone bursts with an 80 percent probability of occurrence, while 2000-Hz tones served as the rare event (20% probability). Each tone was 50 msec in duration, with a 10-msec rise-fall time. Three hundred presentations (240 frequent and 60 rare) were made during each test run with a 1.3 ±.l sec interstimulus interval. Generation and randomization of the tones were performed using a PC-based computer stimulus package (NeuroScan STIM). Competition was provided using the Auditec Multitalker tape played on a professional tape deck (Marantz PMD-40). Test and competing stimuli were presented at 55 db SL re the PTA of the ear receiving the respective signal. All stimuli were presented via insert receivers (Etymotic ER-3A). Electrophysiologic recordings were conducted in a sound-treated and electrically shielded test booth with the participants seated in a reclining chair. Participants were asked to maintain visual fixation on a target placed at eye level on the wall in front of them and to blink normally in order to minimize contamination by ocular movement. Two recording runs were obtained per ear per participant : one run with the tones presented to one ear with no contralateral competition and one run with speech competition presented to the contralateral nontest ear. The presentation order of the initial test ear was counterbalanced across participants. Participants were instructed to ignore the speech competition and keep a mental count of the total number of rare tones they heard. None of the participants exhibited counts of the rare tones that varied by more than ±4 of the actual number presented (60). Neuroelectrical activity was recorded from 19 electrodes (FPJ, FP 21 F7, F3) Fz, F4, F8, T3, C3, CZ, C4> T4, T5, P3, PZ, P4, T6101,02) fixed to the scalp with an appropriately sized commercial electrode cap (ECI Electro-Cap) according to the International system and referenced to linked earlobes. Ocular movement was monitored by electrodes placed vertically above and below the left eye. Electrode impedances were maintained below 5000 ohms. Individual sweeps of time-locked electroencephalographic (EEG) activity extended from -100 to msec relative to stimulus onset. EEG activity was amplified 1000 times, analog filtered (1-70 Hz, 24 db/ octave slope), and digitized at an analog-to-digital rate of 500/sec with a PC-based NeuroScan system and SynAmps 16-bit amplifiers. The digitized epochs were then sent to a microcomputer for off-line averaging, digital filtering (1-40 Hz, 24 db/octave slope), and

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5 Auditory Event-Related Potentials in Elderly Listeners/Hymel et al Mung Group F C Z Elderly Group Right Ear Figure 2 Grand-averaged N1 and P2 waveforms recorded at scalp locations F and C from the young and elderly subjects. Waveforms were recorded in the left and right ears with and without speech babble present in the contralateral nontest ear. Dashed vertical lines indicate onset of frequent stimulus tones. LATENCY IN MSEC group exhibiting a greater reduction. Figure 2 shows grand-averaged N7 and P2 waveforms recorded from Fz and Cz in the young and elderly subjects. To focus on possible topographic differences in the general region of maximum activity, nine electrode locations centered around the vertex were selected for statistical analysis (i.e., F3, F2, F4, C3, Cz, C4, P3, P., and P4). Each participant's N7 amplitudes from the nine electrode locations were selected from averaged frequent stimulus waveforms. N7 amplitude was defined as the lowest absolute voltage value (from baseline) between 75- and 125-msec post-stimulus onset (Alexander et al, 1996). A mixed four-factor analysis of variance (ANOVA) was performed Table 2 Summary Table for the Four-Factor ANOVA Investigating N7 Amplitude as a Function of Participant Group, Listening Condition, Test Ear, and Electrode Location Source of F P Group 1, Condition 1, * 50 Ear 1, Location 8, * 76 Group x condition 1, * 16 Group x ear 1, Group x location 8, Condition x ear 1, Condition x location 8, Ear x location 8, Group x condition x ear 1, Group x condition x location 8, Group x ear x location 8, Condition x -ear x location 8, Group x condition x ear x location 8, *Considered significant at p <.01.

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7 1w" alip (42r4se : r<' 7B Auditory Event-Related Potentials in Elderly Listeners/Hymel et al Table 3 Summary Table for the Four-Factor ANOVA Investigating Pz Amplitude as a Function of Participant Group, Listening Condition, Test Ear, and Electrode Location Source df F P w2 Group 1, Condition 1, Ear 1, Location 8, * 60 Group x condition 1, Group x ear 1, Group x location 8, Condition x ear 1, Condition x location 8, * 26 Ear x location 8, Group x condition x ear 1, Group x condition x location 8, Group x ear x location 8, Condition x ear x location 8, Group x condition x ear x location 8, *Considered significant at p <.01 differences in P2 activity. Each participants' P2 amplitudes from the nine electrode locations were selected from averaged frequent stimulus waveforms. P2 amplitudes were defined as the absolute voltage (relative to baseline) at the highest peak following Nl. A mixed four-factor ANOVA was performed to investigate P2 amplitude differences as a function of group, listening condition, test ear, and electrode location. A summary of the ANOVA test findings is presented in Table 3. Statistically significant main effects were found for listening condition and electrode location. These main effects reflect the fact that the amplitude of P2 was reduced in the presence of competition and had a more anterior scalp distribution. The only significant interaction involved listening condition by electrode location. This finding reflects the fact that greater competition-related decreases in P2 amplitudes were found at the anterior electrode sites. N,-P2 Peak-to-Peak Amplitude Topographic mapping methods do not allow direct portrayal of N1_P2 peak-to-peak amplitude. In order to allow comparison of these data to the findings of Cranford and Martin (1991), a third analysis was performed. N1_P2 amplitude was computed as the voltage difference between the Ni and P2 peaks (as defined above) from listeners' averaged frequent stimulus waveforms for the nine electrode locations. The mixed fourfactoranovainvestigated N1_P2 amplitude differences as a function of group, listening condition, test ear, and electrode location. The summary of the analysis is found in Table 4. This analysis revealed a significant main effect for listening condition and electrode location! These main effects reflect the finding that the Ni and P2 components of the LAEP were reduced in the presence of competition and had a more anterior scalp distribution. The only significant interaction involved listening condition by electrode location. This again reflects the finding that greater competition-related amplitude decreases were found in the forward electrode sites. P300 Component of the LAEP Figure 5 displays the topographic maps of the P300 component of the LAEP as a function of group, listening condition, and test ear. In constructing the maps, it was necessary to use different color scale values for the two subject groups in order to reveal topographic features of the P300 response (i.e., a ± 7 VLV scale for the young group as opposed to a ± 3 RV scale for the elderly group). Examination of the topographic maps revealed two obvious trends. First, the P300 component of the LAEP was larger in amplitude for the young group relative to the elderly group (as evidenced by the difference in map scales). Second, the region of maximum P300 activity appears to be symmetric and centered at the vertex in the younger participants regardless of listening condition. In contrast, elderly participants exhibit the greatest P300 amplitude in the parietal area contralateral to the test ear

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9 Auditory Event-Related Potentials in Elderly Listeners/Hymel et al Young Group z Left Ear Elderl Grou Figure 6 Grand-averaged P301 waveforms recorded at C,, P3, and P4 from the young and elderly subjects. P3 P4 P4 u LATENCY IN MSEC of the LAEP, as well as the scalp distribution of the activity. Each of these findings is discussed. Effects of Contralateral Speech Competition The present study confirmed the Cranford and Martin (1991) finding that contralateral speech competition does not differentially affect the P300 amplitudes of young and elderly listeners. With respect to the earlier components of the LAEP, while Cranford and Martin found reductions in N1-P2 peak-to-peak amplitudes in the presence of the speech competition that were significantly greater for elderly participants than for young participants, the present study found nonsignificant aging effects involving N1_P2 peak-to-peak amplitudes. Unlike the earlier study, the present investigation also examined possible age effects for N1 and P2 separately. These analyses revealed a statistically signifi- cant age effect for the N1 component but not for P2. In the presence of contralateral speech competition, elderly listeners exhibited significantly larger reductions in N1 amplitude than did the younger listeners. These findings reinforce earlier evoked potential and magnetoencephalography findings (Roth et al, 1976 ; Knight et al, 1980 ; Makela and Hari, 1990; Rif et al, 1991) that suggest that, while N1 and P2 may covary in many dimensions, the N1 response is independent of P2 and reflects different underlying central auditory processes. The present findings with N1 are interesting in light of previous research that implicates N1 as reflecting underlying neural processes related to selective attention. Earlier studies (Picton et al, 1971 ; Hillyard et al, 1973 ; Picton and Hillyard, 1974 ; Parasuraman, 1978) found evidence that the N1 component of the LAEP showed a significant increase in amplitude when participants were selectively attending to the

10 Journal of the American Academy of Audiology/Volume 9, Number 5, October 1998 Table 5 Summary Table for the Four-Factor ANOVA Investigating P300 Amplitude as a Function of Participant Group, Listening Condition, Test Ear, and Electrode Location Source df F P Group 1, * 06 Condition 1, Ear 1, Location 8, Group x condition 1, Group x ear 1, 18 < Group x location 8, Condition x ear 1, Condition x location 8, Ear x location 8, Group x condition x ear 1, Group x condition x location 8, Group x ear x location 8, Condition x ear x location 8, Ear x condition x location x Group 8, *Considered significant at p <.01. evoking stimuli and ignoring stimuli being presented to the contralateral ear. At first, this effect was believed to be a manifestation of a gating mechanism that augmented the neurophysiologic response (i.e., the exogenous component) to information in the attended channel while attenuating information in the unattended channel (Picton and Hillyard, 1974). However, later studies by Schwent and Hillyard (1975) and Hansen and Hillyard (1980) supported an alternate interpretation of this effect. These studies suggest that the observed Ni amplitude increase is not the result of a simple gating of attended versus unattended information but instead represents a separate endogenous neurologic process, referred to as the "processing negativity," invoked by the listener's selective attention to the target stimulus Who et al, 1987). The Ni response is now believed (Naatanen and Picton, 1987 ; Giard et al, 1988 ; Woods, 1995) to be the summation of several overlapping components, all of which occur in the same general time frame and which may have different patterns of scalp topography. Thus, the Ni is believed to reflect the occurrence of both exogenous neural processes relating to transmission and reception of information at the level of the primary and association auditory cortices (Scherg and von Cramon, 1985), as well as endogenous components evidenced with selective attention to the evoking stimulus. To the best of our knowledge, the only experiments that have investigated age-related changes in Nl using a selective attention paradigm are those of Ford and Pfefferbaum (1980) and Woods (1992). Both of these studies required participants to selectively attend to rare tones randomly interspersed among more frequently occurring tones in one ear while ignoring discriminably different rare and frequent tones at the opposite ear. These investigators found that, while all participants exhibited significantly larger Ni responses to tones in the attended ear than they did to tones in the nonattended ear, the size of this amplitude increase did not differ between young and elderly groups. The present study obtained results opposite that of an Ni enhancement effect. The present participants were requested to ignore speech competition in one ear and attend to tones presented to the opposite ear. The finding that Nl amplitudes were significantly decreased in the presence of contralateral speech competition may be interpreted as reflecting some form of breakdown in the listener's ability to "ignore" irrelevant competing stimuli. The absence of significant age effects in the Ford and Pfefferbaum (1980) and Woods (1992) studies, combined with the fording of such effects in the present investigation, tentatively suggest that the neural processes underlying selective attention may be less vulnerable to age-related deterioration than those involved with ignoring specific stimuli. In this regard, it is interesting that a frequent complaint expressed by elderly listeners is not that they have difficulty attending to speech in ideal quiet listening environments, but that environments containing noise or other forms of distractions produce the greatest communication problems. 394

11 Auditory Event-Related Potentials in Elderly Listeners/Hymel et al Age-Related Differences in Scalp Topography The findings of the present study with respect to the scalp topographies of both Nl and P2 are in close agreement with findings from earlier studies (Kooi et al, 1971 ; Picton et al, 1974 ; Marvel et al, 1992 ; Friedman et al, 1993). With both young and elderly participants (and with both the competition and noncompetition conditions), the location of maximal activity for both components remained centered at midline slightly forward of C.. In contrast to these earlier components, the present study found scalp distributions of P 30o activity that were distinctively different from those reported in earlier studies. The present young group exhibited P3oo maxima that remained centered at CZ despite changes in stimulus ear or competition condition. With the elderly group, the region of maximum Psoo activity was centered in the parietal region of the hemisphere located contralateral to the test ear. Earlier investigations (Pfefferbaum et al, 1980, 1984 ; Friedman et al, 1993) reported evidence that P3oo maxima are centered in the parietal region (P.) in young participants as contrasted to the frontal region (F.) in elderly participants. Other investigators (Goodin et al, 1978 ; Smith et al, 1980 ; Picton et al, 1984 ; Kugler et al, 1993) have described a somewhat similar forward shift of P300 activity in elderly participants but with the additional finding that the response becomes more equipotential over the scalp. It is important to note, however, that the conclusions of the present investigation related to P300 topography were based on trends observed in the group brain maps (see Method section). The maps of individual participants did not, in every case, show the same pattern of scalp activity as seen in the group maps. Two participants in each group, in fact, showed scalp distributions that were more similar to those reported in the above referenced studies (i.e., more posterior scalp location in young listeners in contrast to more frontal in the elderly). The discrepancy between the present study and earlier investigations with respect to P300 topography is not easily explained in terms of differences in testing or EEG recording methods. While different electronic test systems were involved, the studies used similar filtering and recording techniques, reference electrode placements (linked ears or mastoids), stimulus presentation, and patient task requirements. One critical difference may, however, relate to the use of monaural stimulation in the present study. The vast majority of previous P300 research, including those cited above, used binaural stimulation. There is now research that suggests that the source of the P300 recorded from the scalp may involve separate neural generators at multiple levels of the nervous system. A number of intracranial recording studies and tests following cortical and subcortical lesions in humans (Halgren et al, 1980 ; Knight, 1984 ; Yingling and Hosobuchi, 1984 ; Smith et al, 1990) as well as animals (Harrison et al, 1988), have reported P3oo like waves in several different cortical and subcortical areas including frontal and temporoparietal cortex, the hippocampus and amygdala, and in the pons and midbrain regions. If multiple generators are the source of the P3oo, then monaural versus binaural stimulation might be expected to produce different patterns of scalp activity, especially if some of the generators are specific to binaural input. The results of the present study suggest that monaural stimulation, in conjunction with topographic mapping, may reveal distributions of cortical and subcortical activity that differ from those found when binaural paradigms are used. Further studies that use brain mapping in combination with different forms of monotic and dichotic (or diotic) discrimination tasks may provide evidence of unique patterns of scalp activity that distinguish persons with impaired binaural processing from those with normal processing. These data would not only provide new insights into the nature of the underlying brain processes involved but might also be developed as a clinical tool to identify persons with impaired binaural function (Jerger et al, 1995). Acknowledgment. This paper was presented at the Student Research Forum, American Academy of Audiology Annual Convention, April 19,1997, Ft. Lauderdale, FL. REFERENCES American Speech-Language-Hearing Association. (1990). 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