J Am Acad Audiol 20:629–643 (2009) Auditory Steady-State Responses and Speech Feature Discrimination in Infants DOI: 10.3766/jaaa.20.10.5 Barbara Cone* Angela Garinis{ Abstract Purpose: The aim of this study was to determine whether there was a correlation between auditory steady-state responses (ASSRs) for complex toneburst stimuli and speech feature discrimination (SFD) abilities in young infants. Study Sample: Seventeen infants (mean age 5 9.4 months) and 21 adults (mean age 5 27 years) with normal hearing had ASSR and SFD tests. Data Collection: The ASSR test employed an eight-component complex toneburst stimulus; threshold and input–output functions were determined as level was systematically varied. The SFD test utilized an observer-based, visual-reinforcement test procedure to determine the infant’s ability to detect the speech feature change from /ba/ to /da/. Results: The correlation of the group mean /ba/–/da/ discrimination performance (percent correct) with the group mean ASSR score (percent responses present) ranged from r 5 0.64 for the 1500 Hz amplitude-modulated and frequency-modulated tone burst to 0.99 for ASSRs for all stimulus components; however, correlations between ASSRs and SFD scores for individual subjects were modest. Conclusion: The ASSR and SFD results appear to reflect the audibility of the stimuli. Key Words: Auditory evoked potentials, infants, speech audiometry Abbreviations: ABR 5 auditory brain stem response; AM 5 amplitude modulation; ASSR 5 auditory steady-state response; CF 5 carrier frequency; DPOAE 5 distortion product otoacoustic emission; FFR 5 frequency following response; FM 5 frequency modulation; IAFM 5 independently amplitude and frequency modulated; MF 5 modulation frequency; RECD 5 real-ear to coupler difference; SFD 5 speech feature discrimination; SNR 5 signal-to-noise ratio; VRA 5 visual reinforcement audiometry T he ability to discriminate speech sounds relies, in part, upon the temporal- and frequencyresolving power of the auditory system for elements of complex acoustic events. Speech signals are composed of amplitude and frequency variations occurring over time in different frequency bands. Prosodic and speech segmentation information is conveyed by slow (1–50 Hz) amplitude modulation. Many aspects of the fine structure of speech, such as consonant–vowel transitions, voiced–voiceless cues (voice-onset time), and the fundamental frequency of the voice are linked to very rapid (50–500 Hz) amplitude and frequency modulations (AMs and FMs). In the ongoing speech signal, there are multiple AM components and FM components that must be processed concurrently. The discrimination of speech features, such as manner, place, voicing, and vowel type, requires that the ear and brain simultaneously *Speech, Language and Hearing Sciences, University of Arizona, Tucson; {Speech and Hearing Sciences, University of Washington, Seattle Barbara Cone, PhD, Speech, Language and Hearing Sciences, University of Arizona, P.O. Box 210071, Tucson, AZ 85721; Phone: 520-626-3710; Fax: 520-621-9901; E-mail: conewess@u.arizona.edu Portions of this work were presented at the International Evoked Response Audiometry Study Group, June 2005, Havana, and at the American Auditory Society, March 2006, Scottsdale. This work was supported by grants from the National Organization for Hearing Research, the National Institutes of Health–National Institute for Deafness and Other Communication Disorders (R55 DC 05646-01A1) and Intelligent Hearing Systems. 629 Journal of the American Academy of Audiology/Volume 20, Number 10, 2009 process low- and high-frequency spectral components, AMs, and FMs. Thus, one mechanism of speech feature discrimination is the ability to encode rapidly changing temporal (modulation) and spectral (frequency) cues simultaneously across a range of frequencies. Evidence from psychophysical studies of adults suggests that sensitivity for AM and FM is needed for speech perception (Zeng et al, 2005). AUDITORY STEADY-STATE RESPONSES A uditory steady-state responses (ASSRs) from the brain stem can be obtained for amplitude modulation or frequency modulation or combined amplitude and frequency modulation of tones or noise (John et al, 2001). ASSRs obtained for AM tones as carrier frequency is varied provide estimates of pure-tone thresholds (for review, see Picton et al, 2003). ASSRs can be obtained for simultaneous independently amplitudeand frequency-modulated (IAFM) tones (Dimitrijevic et al, 2001; Dimitrijevic et al, 2004), offering insight into how the auditory system encodes simultaneously the temporal and spectral complexities of speech. The interactions between amplitude and frequency modulation (of tones) have been evaluated in adults, using ASSRs. John and colleagues (2001) and Dimitrijevic and colleagues (2001) show that when a tone is both amplitude and frequency modulated, the response amplitude is smaller than that found for the AM response or FM response alone. The phase of the response, however, appears to be unchanged by the presence of another modulated component. Also, the response to FM appeared to be affected by either an additional AM or an additional FM component, while the AM response was affected only by another FM component. These effects offer some insight into how the cochlea and brain stem pathways process AM and FM. Because the decrement in the response to these IAFM tones was small, relative to the AM alone and FM alone condition, it has been suggested that the two types of modulation are processed independently (John et al, 2001). This ‘‘independence’’ may have been largely due to the separation of the cochlear place of excitation patterns for AM versus FM. It is also possible to combine AM and FM to obtain a response that is larger than the response to AM alone. This is referred to as a mixed-modulation stimulus, and the ‘‘improvement’’ in the response amplitude is dependent upon the phase of the FM stimulus component relative to the AM component. ASSRS AND WORD RECOGNITION D imitrijevic and colleagues (2001) demonstrate a correlation between the ASSRs for IAFM tones and word-recognition scores in normal-hearing adults. 630 First, they measured word recognition as a function of stimulus level and developed a ‘‘performance-intensity’’ function: the percent correct word recognition for each level tested. Then, they determined the number of ASSR components present for an eight-tone complex that consisted of four carrier frequencies (CFs), each of which was amplitude and frequency modulated at different (independent) rates. The ASSR ‘‘score,’’ that is, the percentage of components present (out of a possible eight), for each stimulus level was calculated. They then compared the word-recognition score as a function of level to the ASSR score as a function of level. The percentage of ASSR components detected at each stimulus level had a significant correlation with the word-recognition score at a similar level. Dimitrijevic and colleagues (2004) also tested the correlation between ASSRs and word recognition in adults with hearing loss. They obtained ASSRs in response to IAFM stimuli with CFs, levels, and modulation depths designed to have similar characteristics to speech. Word-recognition abilities were determined using standardized monosyllabic word lists. There were strong correlations between the word-recognition score and the number of ASSR components present for young and elderly adults with normal hearing and also for elderly adults with hearing loss. These investigators suggest that ASSRs for multiple IAFM tones correlate with word-recognition scores because both speech and multiple IAFM tones contain information that varies rapidly in intensity and frequency. The ASSR ‘‘score’’ (i.e., the number of response components present for the eight-component IAFM stimulus) was used as an estimate of how much acoustic information was available to the listener. The more information available in the speech frequency range, for which the auditory system can process rapidly changing intensity and frequency cues, the better the word-recognition capabilities should be. SPEECH FEATURE DISCRIMINATION IN INFANTS I nfants have excellent speech-perception skills (Kuhl, 1992, 2004; Jusczyk et al, 1998; Werker et al, 1981; Werker and Tees, 1999). They are able to discriminate speech features, such as a voiced–voiceless contrast (/ta/ vs /da/), place of articulation (/ba/ vs /da/), or good versus poor exemplars of vowel sounds. Experience listening to speech in the native language during the first year of life appears to exert a strong effect on speech perception and phoneme-discrimination abilities (Werker and Tees, 1984; Kuhl, 2004). Eilers et al (1977) used a visually reinforced operant conditioning method to evaluate the development of speech feature discrimination (SFD) in infants under the age of one year. Yet the methods used for investigating the ASSR and SFD in Infants/Cone and Garinis development of infant speech perception have had little carryover to clinical applications. There are no standardized methods for testing infant speech perception or discrimination procedures that can be used in infants who have receptive language less than 2.5 years. Because decisions about amplification, cochlear implantation, and language-learning methods may be based upon speech-perception abilities, there is a considerable need to develop clinical assessment methods suitable for infants and toddlers. Some methods used to study speech-perception abilities in young infants involve recording nonnutritive sucking behavior in response to sound or rely on a habituation/preferential looking protocol (Werker et al, 1998; Houston et al, 2003). These methods, while useful in the research lab, may not have easy carryover into clinical settings. One method, based upon a visual reinforcement paradigm, has been successfully used in research establishing speech-discrimination abilities in normal-hearing infants (Eilers et al, 1977; Trehub, 1979; Nozza, 1987; Nozza et al, 1991a; Nozza et al, 1991b; Werker et al, 1998; Kuhl, 2004). In this procedure, the infant/toddler is reinforced for detecting when the speech token changes, after having been exposed to a train of identical speech tokens. The technique used—observation of stimulus-contingent behavior, with subsequent reinforcement of ‘‘correct’’ responses—is similar to visual reinforcement audiometry, a readily available clinical protocol (Widen et al, 2000). For instance, the consonant–vowel token /ba/ can be presented repeatedly, and the change token interspersed in this /ba/ train may be /da/. The infant is reinforced for detecting (indicated with a head turn or other stimulus-contingent behavior) when the token changes. The response to the stimulus change indicates that the infant has detected a change in the speech feature, in this example, a place-of-articulation cue for a voiced plosive. Using this technique, Nozza (1987) showed that infants with normal hearing required higher levels than adults to reach their maximum performance on an SFD task. These differences in level were 27 dB for a /ba/–/da/ contrast, 25 dB for a /ba/–/ga/ contrast (Nozza et al, 1991a; Nozza et al, 1991b), and as much as 30 dB for a /da/–/ga/ contrast. These ‘‘performance-intensity’’ functions, that is, the accuracy of speech sound discrimination plotted as a function of level, provide evidence of a developmental process in speech-perception abilities for infants that cannot be accounted for on the basis of a simple elevation in hearing threshold. RATIONALE W e aimed to address the issue of whether and how ASSRs are related to infant speech-discrimination abilities. This knowledge could then be applied to the problem of documenting the effect of intervention strategy (i.e., amplification) on speech-perception abilities for infants with hearing loss. The study was also motivated by the need to develop (clinical) methods for assessing speech-discrimination/perception abilities in young infants (Eisenberg et al, 2005). ASSRs for mixed-modulation tones that model speech characteristics are correlated with speechdiscrimination abilities in adults with normal or impaired hearing (Dimitrijevic et al, 2001; Dimitrijevic et al, 2004). Thus, we aimed to test whether the relationship between ASSRs and speech-discrimination abilities that Dimitrijevic and colleagues (Dimitrijevic et al, 2001; Dimitrijevic et al, 2004) found would hold true for infants. The hypothesis was that infant ASSRs for a tone complex composed of multiple mixed-modulation stimuli (approximating the acoustic complexities of speech) would be correlated with infant speech feature discrimination abilities. The theoretical foundation of this work is based in the realm of speech acoustics and feature detection (Pickett, 1999) as well as in methods to predict speech intelligibility of speech sounds (French and Steinberg, 1947) such as the Articulation Index and the Speech Transmission Index (Humes et al, 1986). As the acoustic features of speech sounds can be analyzed with respect to their frequency components, it is possible to estimate speech-recognition or -discrimination abilities on the basis of audibility for those frequency components. The multiple mixed-modulation stimuli used in this experiment were acoustically similar to speech sounds in terms of mean formant frequencies for consonant–vowel transitions and amount of amplitude and frequency modulation found for individual consonants in the long-term speech spectrum (Dimitrijevic et al, 2004). ASSRs were obtained in response to complex toneburst stimuli and the number of response components present, and their amplitudes were measured as a function of level. Similarly, speech (feature)-discrimination abilities were measured as a function of level, using an observer-based psychophysical method in conjunction with visual reinforcement techniques. METHOD Subjects Seventeen infants aged 4–13 months (mean age 5 9.4 months) and 21 adults aged 22–43 years (mean age 5 27 years) with normal hearing participated in both an ASSR and speech feature discrimination test. Nine of the 21 adults participated in a second ASSR test, described below. To demonstrate normal hearing, adult subjects had a pure-tone threshold test prior to participation in the study, and thresholds were # 20 dB HL at 500–8000 Hz. 631 Journal of the American Academy of Audiology/Volume 20, Number 10, 2009 For infant subjects, distortion product otoacoustic emission (DPOAE) and click-evoked auditory brain stem response (ABR) tests were used to establish normal hearing. To be considered normal, DPOAEs were present at 3 dB over the noise floor in the 1000– 4000 Hz frequency range, and ABRs were present with normal latencies for click stimuli presented at 30 dB nHL. ASSR Test Stimuli A complex toneburst stimulus, consisting of four carrier tones each presented at two different modulation rates, with amplitude modulation alone or combined with frequency modulation, was used for the ASSR test. Stimuli were generated using the Intelligent Hearing Systems software package for the SmartEP-ASSR system. The carrier frequencies were 500, 1500, 2500, and 4000 Hz. The modulation frequencies were 78 and 85 Hz for the 500 Hz carrier, 83 and 90 Hz for the 1500 Hz carrier, 88 and 95 Hz for 2500 Hz, and 93 and 100 Hz for 4000 Hz. At 78, 83, 88, and 93 Hz (i.e., the lower modulation frequency for each CF pair) the tones were amplitude modulated with a cosine ramp. This created an AM stimulus. At 85, 90, 95, and 100 Hz (the higher modulation frequency for each CF pair) the tones were frequency modulated at 35, 30, 20, and 35 percent, respectively, with a phase of 90 degrees, and also shaped with a cosine ramp, creating an AM+FM stimulus. The CFs and modulation rates and depths were chosen to approximate the stimuli used by Dimitrijevic and colleagues (2004); however, a cosine ramp was used for all carriers in the present study, resulting in the creation of a complex, eight-component toneburst stimulus. This complex toneburst stimulus was presented monaurally through insert earphones at levels of 20 to 80 dB SPL in 10 dB steps. A fourcomponent toneburst stimulus was also created, composed of the AM+FM components described above, that is, 500, 1500, 2500, and 4000 Hz tone bursts with additional frequency modulation presented at rates of 85, 90, 95, and 100 Hz, respectively. The four-component stimulus was used to test a small sample (N 5 9) of adults for comparison to the larger group tested with the eight-component stimulus. Stimulus calibration was carried out using a 2 cc coupler with an H1a adapter in conjunction with a Larson Davis Model 824 sound pressure level meter. Speech Feature Discrimination Test Stimuli Consonant–vowel tokens /ba/ and /da/ were used for the SFD test. The /ba/ versus /da/ contrast has been used in past research employing psychophysical or electrophysiologic measures and so was chosen for this 632 investigation. The /ba/ versus /da/ contrast consists of a place-of-articulation cue (bilabial vs lingual-alveolar voiced plosive) signaled by the change in second format frequency in the transition from the consonant to the vowel. A /ba/ versus /sa/ contrast was used for training. This contrast consists of changes in place, manner (plosive vs sibilant), and voicing (voiced vs unvoiced). This contrast was used in order to provide multiple cues for speech feature change. Digital recordings were made of a female speaker saying the syllables /ba/, /da/, and /sa/. Using Praat Speech Analysis Software, exemplar tokens were truncated at 150 msec following the consonant onset, using a 20 msec tapering function. Each token was then copied four times, with a 500 msec interval between the offset of one token and the onset of the next. The test stimuli were, therefore, 2100 msec in duration, with four 150 msec speech samples presented at a rate of 2 Hz. These digitized samples were then presented through the Intelligent Hearing Systems software package for visually reinforced infant speech discrimination tests. Stimuli were presented through a loudspeaker and were calibrated using a sound pressure level meter placed in the position of the test subject. Stimulus presentation levels during the SFD test were 30–70 dB SPL. While it has been shown that infants need higher sensation levels than adults for optimum performance (Nozza, 1987; Nozza et al, 1991b), the aim of the present study was to establish speech feature–discrimination scores as a function of level, using levels that ranged from close to threshold to those typical of conversational speech. These scores as a function of level were then compared to the ASSR test results obtained at the same presentation levels. ASSR Test Method ASSRs were obtained using the Intelligent Hearing Systems Smart ASSR System. Infants were tested during natural sleep, and adults were tested while resting in a reclining position with their eyes closed. Many of the adults slept during the test; however, sleep stage was not formally monitored. EEG electrodes were placed at the vertex and at the ipsilateral mastoid as the noninverting and inverting electrodes, respectively, with the contralateral mastoid serving as ground. The EEG was sampled over a 1024 msec epoch, with a gain of 80 dB, filtered at 30–300 Hz, and averaged for spectral analysis. A response at a particular modulation frequency was deemed to be statistically significant using an F-statistic to evaluate the signal (power at the MF)-to-noise (power in spectral bands adjacent to the MF) ratio. Responses were significant when p , .05 was achieved. Averaging was continued until the averaged background noise level in five frequency bins above and below the ASSR and SFD in Infants/Cone and Garinis modulation frequency reached a level of 0.011 mV or until all components reached significance, whichever occurred first. The percentage of significant responses (out of eight possible) was calculated as a function of stimulus level. SFD Test Method Infants were tested using visually reinforced operant procedures with observer-based psychophysics. Infants were brought into the test booth while the ‘‘control’’ or background stimulus was presented continuously, that is, the four-token sample, such as /ba/-/ba/-/ba/-/ba/, at 70 dB SPL. A test assistant in the booth manipulated toys to keep the infant quiet and alert. The parent and test assistant listened to music presented through earphones to keep them masked as to the nature of the stimuli being presented. Infants and observers were first trained to detect a change in the speech stimulus. The training consisted of pairing the presentation of the contrast sound, /sa/ (repeated four times), with the visual reinforcer: an animated toy obscured in a smoked Plexiglas box. When activated as a reinforcer, the box was illuminated and the toy was animated. The pairing of the reinforcer with the change trial was used to teach the infant to emit a behavior used during the testing phase. The behavior could be a head turn, an eye movement toward the reinforcer, a change in facial expression, or cessation of or increase in body movement. Training consisted of five pairings of the change trial with the reinforcer. Background and change trials were presented at the same level, 70 dB SPL. (Between change trials, the background control stimulus [/ba//ba/-/ba/-/ba/] was being played continuously.) After five pairings, a probe trial was used in which the stimulus change was presented but the reinforcer was withheld until the infant emitted a response. The response window was 5 sec in duration. If the observer detected the infant’s response, the reinforcer was introduced. The observer had to correctly detect the presence of stimulus change based upon the infant’s behavior for two consecutive probe trials before testing was begun. Infants who did not emit behaviors that could be correctly detected by the observer during the probe trials underwent further training trials. Up to five training trials were undertaken for each session. If the observer could not meet criterion for that infant after multiple training trials, the infant was dismissed for the day. The infants were allowed to participate in up to three training sessions. If observer criteria were not met after the third training session, the infant was dismissed from further participation. When observer criteria were met, infants were allowed to participate in as many as five sessions in order to obtain data for as many levels as possible. Data from 17 infants are reported; an additional 12 infants were tested who did not meet the observer’s training criteria. After training, a test block was initiated using the /ba/ versus /da/ contrast. Test blocks were initiated at a level of 60 dB SPL. The next level tested was 40 dB SPL. Trials at 50 and 30 dB SPL were undertaken after data were obtained at 60 and 40 dB SPL. An attempt was made to test at two levels per stimulus contrast. The test block consisted of 10 trials, with at least 40 percent of the trials being controls. The percentage of correct responses for both change and control trials was determined. During testing, the observer controlled when a trial was initiated but was masked as to the nature of these trials, that is, whether they contained a speech feature contrast (change trial) or no stimulus change (control trial). The order of trials was automatically randomized by the computer software. The observer voted on each trial by pressing a response button. The observer had to determine whether the trial contained a speech feature change based solely on observation of the infant’s behavior. When the observer made a correct detection, the infant was given the visual reinforcer. When the observer made a correct rejection (no response on a control trial) there was no reinforcer. Likewise, there was no reinforcer for a miss (failure to detect a change trial) or a false alarm (voting that a change occurred when there was a control trial). Adults were tested using similar procedures. Adult subjects were told to ‘‘raise your hand when you hear the sound that makes the toy light up.’’ Only three pairings of the stimulus change with the reinforcer were used for adult subjects, and only one probe was used prior to initiating testing. After training, stimulus trials were conducted at 50 dB SPL and at 10 dB decrements until the score for change trials was ,40 percent. Adults were tested with both contrasts. RESULTS ASSR Tests Effects of Level, CF, and Modulation Envelope The percent of ASSRs present for the eight stimulus components was calculated as a function of level and collapsed across CF and MF. ‘‘Percent present’’ was calculated as ([NS 3 NP] 4 [NS 3 8]) 3 100, where NS 5 number of subjects tested at a given level and NP 5 number of ASSR components present. This was calculated for data from infant and adult groups. For the data shown in Figure 1, NS decreased with level because testing was terminated if there were no ASSRs present for any stimulus component. There were some remarkable similarities between the percentages of significant ASSRs as a function of stimulus level for 633 Journal of the American Academy of Audiology/Volume 20, Number 10, 2009 Figure 1. Percent present auditory steady-state response (ASSR) components plotted as a function of stimulus level for adult and infant groups. ‘‘Percent present’’ was first calculated as ([NS 3 NP] 4 [NS 3 8]) 3 100, where NS 5 number of subjects tested at a given level and NP 5 number of ASSR components present. Error bars indicate the standard error of the mean. A second calculation of percent present (filled and open circles for adults and infants, respectively) uses a fixed NS in the denominator: 17 for the infant group and 21 for the adult group. infants and adults. Fewer than five out of eight response components were present, on average, even at the highest level tested. The difference in adult versus infant percent present scores never exceeded 9 percent and was observed only at 80 and 50 dB SPL. When a fixed NS in the denominator was used (17 for infants and 21 for adults), in order to take into account differences in threshold across CF and subject group, there were larger differences in the percent present scores for adults and infants. These differences were 14 and 15 percent at 50 and 60 dB SPL, respectively. Otherwise, the differences in percent present scores were, on average, 6 percent. There was considerable variability in both infant and adult groups, and the adult–infant differences in percent of responses present were not statistically significant. Effect of CF and Envelope The percentage of responses present was calculated for each stimulus component. The formula used was (NP/NS) 3 100, where NS is the number of subjects tested with that stimulus and NP is the number of ASSRs present. The percent of responses present is shown for each stimulus component as a function of level for adults (Figure 2A–B) and infants (Figure 2C– D), with stimulus component as the parameter. For both adults and infants, the response to the 1500 Hz AM+FM tone burst at a MF of 90 Hz was most often present. In general, more responses were present for the AM+FM tone bursts than for the tone bursts containing only AM. The only significant differences 634 between the distributions of responses present for adults and infants were at 500 Hz, for which infants were less likely to have responses (x2 5 8.091, p 5 .004). A chi-square test detected a trend for infants to have more responses present for 2500 Hz tone bursts than did adults (x2 5 3.497, p 5 .06). Interaction of AM+FM and AM The finding that there were differences in the number of responses present as a function of CF and modulation envelope raised the question of how the presence of multiple stimulus components affected the response. The effects of the presence of the AM stimulus components upon the AM+FM responses were evaluated in two ways. First, the difference in the percentage of responses present was calculated for the AM+FM stimulus minus the AM stimulus. The differences were largest for the 500 and 1500 CFs and averaged 35 percent (collapsed across level), while at 2500 and 4000 Hz the differences averaged only 9 percent. Second, nine adults were additionally tested using a four-CF tone complex consisting of the AM+FM components at 500, 1500, 2500, and 4000 Hz. The results for the four-CF/MF toneburst complex were compared to the previous results obtained with the eight-component stimulus. The percent of responses present at each CF for the four- minus eight-component stimulus was calculated. Overall, the presence of the AM component produced a 23 percent decrement in the percent present score. The largest effect was seen at 2500 Hz, for which a 38 percent difference was ASSR and SFD in Infants/Cone and Garinis Figure 2. Infant and adult auditory steady-state response percent present for each carrier frequency/modulation frequency (CF/MF) component. The percentage of responses present was calculated for each stimulus as (NP/NS) 3 100, where NS is the number of subjects tested with that stimulus and NP is the number of ASSRs present. The stimulus component type (CF/MF) is the parameter: filled symbols indicate the amplitude modulation and frequency modulation (AM+FM) stimulus components, and open symbols indicate the AM stimulus components. The components have been grouped by type, with A and C showing adult and infant responses for AM+FM, respectively, and B and D showing adult and infant responses for AM. The number of subjects tested at each level is indicated in parenthesis on the x-axis. observed, and the smallest effect was seen at 500 Hz, with only a 7 percent difference. ASSR Threshold and Amplitude Threshold as a function of CF was estimated at the 50 percent point on the functions for the AM+FM stimuli (Figure 2A–B), shown in Table 1. In general, thresholds were somewhat elevated with respect to previously published data, using either single or simultaneous presentation of CFs (Cone-Wesson et al, 2002; Luts et al, 2004). Thresholds could not be estimated at 2500 Hz in adults because the percentage of significant responses remained under 50 percent at every level tested. The threshold elevations for individual CF/MF components are easily explained by the fact that the CFs used in the present study were selected to represent speech, and so one spectral component could very well mask another. This effect is evident in the threshold differences estimated for the four-component stimulus compared to the thresholds for the same components presented in the context of an eight-component stimulus (Table 1). Infant thresholds were 20 dB higher than those of adults at 500 Hz. Response amplitudes for each carrier frequency were measured for the AM+FM tone burst when it was used in combination with seven other carriers and in combination with three other carriers. The values shown are those for responses that met the a priori statistical criterion for ‘‘response present.’’ These amplitudes are plotted in Figure 3 (adult subjects only). At 500 and 1500 Hz the amplitudes were larger in response to the four-component stimulus compared to the eight-component stimulus, but this was statistically significant only 635 Journal of the American Academy of Audiology/Volume 20, Number 10, 2009 Table 1. Threshold Estimates for Auditory Steady-State Response Percent Present as a Function of Stimulus Level Carrier Frequency/Modulation Frequency (Hz) Subject Group Infant Adult Adult (four-component stimulus) 500/85 1500/90 2500/95 4000/100 65 dB SPL 45 dB SPL 35 dB SPL 28 dB SPL 35 dB SPL 28 dB SPL 68 dB SPL CNE 28 dB SPL 65 dB SPL 60 dB SPL 45 dB SPL Note: The percentage of subjects with responses present for each carrier frequency/modulation frequency (CF/MF) component was calculated as a function of stimulus level (see Figure 2A–B). The 50% point on each CF/MF function was used to calculate threshold. CNE 5 could not evaluate. for the 500 Hz carrier (F[1, 119] 5 6.24, p 5 .01). The amplitudes appeared smaller for the four-component compared to the eight-component stimulus condition for 2500 and 4000 Hz carriers, but this was not significant. Analyses of variance were used to determine if response amplitudes, side-bin noise amplitudes, and signal-to-noise ratios (SNRs) varied with respect to stimulus type, that is, the four-CF AM+FM stimulus versus the same components embedded in an eightcomponent stimulus. The means and standard deviations for these response parameters are presented in Table 2. The differences in side-bin noise and SNR were significant (p , .001), with the responses to the four-component stimulus having larger SNRs, owing to significantly lower noise levels in this condition. Adult versus infant differences for response amplitude, side-bin noise, and SNR (amplitude/sideband noise ratios) were evaluated for ASSRs in response to the AM+FM signal components. These are summarized in Table 2. The values shown are those for responses that met the a priori statistical criterion for ‘‘response present,’’ collapsed across stimulus level. Analyses of variance were completed to determine if there were differences attributable to age group. Those values marked with an asterisk were significant at the p , .05 level. Response amplitudes obtained from adults were significantly larger than those obtained from infants at 500 and 1500 Hz (Figure 4). Although adults had a greater percentage of responses present for 500 Hz, infants and adults had the same percentage of Figure 3. Auditory steady-state response amplitude in adults in nanovolts plotted as a function of stimulus level for carrier frequencies at 500, 1500, 2500, and 4000 Hz, presented at modulation frequencies of 85, 90, 95, and 100 Hz, respectively. Filled symbols indicate response amplitude when the component was presented as part of the eight-component mixed-modulation stimulus. Open symbols indicate the response amplitude when the component was present as part of the four-component mixed-modulation stimulus. Bars indicate standard errors. 636 Note: The amplitude of the auditory steady-state response (ASSR), background noise, and the ASSR/noise amplitude ratios are shown for infants and adults. The asterisks indicate values for which infant and adult differences are statistically significant (p , .05). The number of carrier frequencies (four or eight) is indicated in parentheses. 4.19 (1.3) 3.24 (1.2)* 4.91 (2.4)* 3.42 (1.49)* 5.24 (3.6)* 3.85 (1.29) 2.64 (0.54) Amplitude/Noise (SD) Adult (4) Adult (8) Infant (8) 9.43 (6.3) 5.41 (2.8) 4.38 (1.8) 3.12 (1.04) 3.09 (1.0) 7.74 (4.5) 5.18 (3.06) 4.77 (1.9) 2.81 (.80) 3.31 (1.4) 4.15 (1.7) 3.8 (3.4) 4.82 (3.7) 0.008 (0.004) 0.010 (0.003)* 0.007 (0.003)* 0.011 (0.004)* 0.007 (0.002)* 0.011 (0.003) 0.011 (0.005) Noise Amplitude, mV (SD) Adult (4) Adult (8) Infant 0.009 (0.004) 0.011 (0.015)* 0.007 (0.007)* 0.012 (0.005)* 0.007 (0.003)* 0.008 (0.004) 0.011 (0.003)* 0.007 (0.003)* 0.010 (0.004)* 0.007 (0.003)* 0.008 (0.004) 0.011 (0.015) 0.007 (0.003) 0.033 (0.033) 0.034 (0.016) 0.031 (0.016) 0.036 (0.020) 0.038 (0.027) 0.039 (0.013) 0.027 (0.011) 0.074 (0.048) 0.056 (0.030)* 0.029 (0.009)* 0.035 (0.014)* 0.021 (0.006)* 0.059 (0.025) 0.053 (0.039)* 0.033 (0.012)* 0.029 (0.012)* 0.022 (0.010)* 0.030 (0.012) 0.034 (0.024) 0.033 (0.027) 4000/100 4000/93 2500/95 2500/88 1500/90 1500/83 500/85 500/78 ASSR Parameters Response Amplitude, mV (SD) Adult (4) Adult (8) Infant (8) Carrier Frequency/Modulation Frequency (Hz) Table 2. Auditory Steady-State Response Amplitude, Noise, and Amplitude-to-Noise Ratios ASSR and SFD in Infants/Cone and Garinis responses present at 1500 Hz. Infant and adult ASSR thresholds were not significantly different, so the differences in ASSR amplitude cannot be accounted for on the basis of threshold differences. It is interesting to note that response amplitudes decrease with increasing CF for adults but are unchanging for infants. These observations were confirmed statistically using analyses of variance as a function of frequency for the adult (F[3, 282] 5 7.67, p , .001) and infant (F[3, 156] 5 0.43, p 5 .07) groups. Infants had significantly lower noise in the averaged EEG than did adults. Response-to-noise ratios were larger for infants at 4000 Hz only. Speech Feature Discrimination Tests The percentages of contrasts detected by the infant subjects are plotted as a function of level in Figure 5. Each gray circle represents the trial score for an individual infant. The percentage of contrasts correctly detected decreased with stimulus level. The mean score was 74 percent at 60 dB SPL, 63 percent at 50 dB SPL, and 57 percent at 40 dB SPL. Performance at levels below 40 dB SPL showed less than 40 percent correct detection of contrasts. These performance differences as a function of level were significant (F 5 4.18, p , .01). The mean score for correct rejections during control trials was 87 percent. Total correct scores (correct contrast + correct control trials) are shown for individuals in Figure 5. The data were examined to determine if there were differences in performance as a function of age of the infant. Although infant age at the time of testing ranged from 4.7 months to 13.9 months, the mean age at time of test was 9.4 months. There was no apparent effect of age on performance, with the correlation between percent correct detection of contrasts and age (in months) at r 5 0.04, when tests at all levels were considered. When considering the effect of age on performance at 60 dB SPL only, 30 percent of infants aged four–six months had 100 percent correct detection, while this increased to 44.4 percent of infants aged seven–nine months and 56.2 percent of infants aged 10 months or older. While these appeared to be steady gains in performance with age, they were not statistically significant. SFD performance as a function of level is shown for 12 infants for whom data were obtained for at least two levels (Figure 5). Testing at two or more levels was possible for the infants who needed fewer training trials and who had high performance levels early in the test session. There was considerable variability in performance, especially at levels below 60 dB SPL. Performance increased with level, in a monotonic fashion. For these subjects, the mean score (% correct contrast trials detected) was 90.7 percent at 60 dB SPL. 637 Journal of the American Academy of Audiology/Volume 20, Number 10, 2009 Figure 4. Auditory steady-state response amplitude in infants and adults in nanovolts plotted as a function of stimulus level for carrier frequencies at 500, 1500, 2500, and 4000 Hz, presented at modulation frequencies of 85, 90, 95, and 100 Hz, respectively. Filled symbols indicate infant response amplitudes, and open symbols indicate adult response amplitudes. Bars indicate standard error. Adults were tested using the same methods as infants, as described above. Mean percent correct discrimination scores (correct detection of the contrast stimulus) were 8.3, 63.1, 91.8, and 99.0 percent for stimulus levels of 0, 10, 20, and 30 dB SPL, respectively. Comparison of ASSR and SFD Comparisons were made between the infant ASSR and SFD data. For SFD, the percent correct contrasts detected as a function of level for all infants and for the select group tested at two or more levels were examined. The mean detection scores as a function of level for ‘‘all’’ infants and for the ‘‘select’’ group tested at two more levels are presented in Figure 6. Also shown in Figure 6 are the infant ASSR ‘‘percent present’’ data for all eight stimulus components, collapsed across CF and MF. The ASSR percent present scores (collapsed across CF and MF) were calculated for the four AM+FM tone bursts at 500, 1500, 2500, and 4000 Hz at modulation rates of 85, 90, 95, and 100 Hz, respectively (Figure 6). Finally, as the responses to the 1500 Hz AM+FM tone burst at a MF of 90 Hz were most often present in infant subjects, these are highlighted in Figure 6. Speech feature discrimination performance and the percentage of ASSRs present are monotonically increasing functions. 638 Correlation of the mean scores for SFD and ASSR are shown in Table 3. The correlations of the /ba/–/da/ discrimination data with ASSR data range from r 5 0.64 for the 1500 Hz component (most often present) to 0.99 for all ASSR components. It is obvious that increasing level is important for obtaining ASSRs to one or more stimulus components when they are presented in the context of seven other tone bursts. Similarly, the infants’ ability to discriminate the placeof-articulation /ba/–/da/ speech feature change is related to stimulus level. Owing to the variability in infants, correlation between ASSR and SFD scores for individuals was low (r 5 .50) but statistically significant (F 5 9.276, p , .01). DISCUSSION T he hypothesis that ASSRs for complex toneburst stimuli would be correlated to infant speech feature discrimination performance was partly supported by the results. In previous work, Dimitrijevic and colleagues (2004) have shown that the results of ASSR tests using mixed-modulation stimuli designed to approximate speech characteristics were strongly correlated with conventional word-recognition scores in adults with normal hearing and hearing loss. This ASSR and SFD in Infants/Cone and Garinis Figure 5. Speech feature discrimination in infants, with individual scores for the /ba/ vs /da/ contrasts shown for infant subjects as a function of stimulus level. ‘‘Correct contrast’’ is the percent correct for stimulus change trials. ‘‘Total correct’’ is the percent correct for both stimulus change trials and for (correct) no responses for the no-change trials. The group means are shown for all subjects (mean correct contrast) and for a select group of 12 subjects with tests completed for at least two stimulus levels (select correct contrast). The errors bars indicate standard error of the mean. study aimed to test this concept in young infants, in an age group for which there are no standardized methods for evaluating SFD. The novel ASSR test stimuli were composed of two different toneburst (modulation) envelopes used for each of four CFs, and ASSRs for each modulated component were measured as all CFs were presented simultaneously. This was a complex stimulus, with frequency components that were chosen to approximate speech characteristics, particularly the formant frequencies, and amplitude and frequency modulation depths and rates that would be present in consonant– vowel transitions (Dimitrijevic et al, 2004).The number of ASSRs present for each stimulus component (as a function of level) was used as a gross estimate of the amount (and frequency range) of acoustic information available to the listener, an approach based on principles similar to the Articulation Index (Humes, 1991). We did not replicate all of the stimulus parameters used by Dimitrijevic and colleagues (2004). Their stimuli were composed of four carrier frequencies that were independently amplitude or frequency modulated. The stimuli used in the present study were trains of tone bursts, using tone bursts at the same frequencies and modulation rates as Dimitrijevic and colleagues. The linear and brief onset ramps of the toneburst stimuli used in this study produced larger amplitude responses than those evoked by IAFM tones (Dimitrijevic et al, 2001). The overall percentage of ASSRs present as a function of level was similar for adults and infants. The mean age of the infants tested was 8.4 months, an age when cochlear tuning and eighth nerve response characteristics are thought to be mature (Werner and Gray, 1998). This maturation may have contributed to the similarities. There were, however, some significant differences as a function of carrier frequency. Infants had fewer responses present at 500 Hz than did adults. The maturation of perceptual thresholds for 500 Hz stimuli is known to be delayed until later childhood (Werner and Marean, 1996), likely due to differences in middle ear function. It is also the case that tone burst–evoked ABR thresholds for 500 Hz are elevated in infants and young children, compared to adults (Stapells, 2000). There was also a trend for infants to have a greater number of responses than adults at 2500 Hz. All ASSR tests were conducted with insert phones, and perhaps the differences in ear canal sound pressure level in the infant ear, compared to the adult ear, contributed to this disparity. In newborns, there may be as much as a 15–20 dB ‘‘gain’’ 639 Journal of the American Academy of Audiology/Volume 20, Number 10, 2009 Figure 6. Infant group mean data for three auditory steady-state response (ASSR) and two speech feature discrimination (SFD) scores shown as a function of stimulus level. The three ASSR scores are (1) % present for all eight carrier frequency/modulation frequency (CF/ MF) components; (2) % present calculated for the four CF/MF components that had amplitude modulation and frequency modulation (AM+FM); and (3) % present for the 1500 Hz CF/90 Hz MF component. The two SFD scores are (1) % correct contrast discrimination for infant subjects and (2) % correct contrast discrimination for 12 infant subjects for whom data were obtained for at least two stimulus levels. Error bars indicate standard error of the mean. in SPL; however, ABR thresholds for clicks or a 4000 Hz tone burst are elevated with respect to adults, when the ear canal SPL differences are considered (Sininger et al, 1997). Rance and Tomlin (2006) measured ASSR thresholds for 500 and 4000 Hz AM+FM tones together with ear canal sound pressure levels. They show that by six weeks of age real-ear versus coupler differences (RECDs) in SPL were only 1.5 dB at 500 Hz but were 11 dB at 4000 Hz. Yet, even when accounting for the RECDs, the neonatal ASSR thresholds were elevated with respect to adults. In the current data set, it may be that stimulus levels were effectively higher in the infants compared to adults, owing to differences in ear Table 3. Correlation of Mean Values for Auditory Steady-State Response (ASSR) and Speech Feature Discrimination (SFD) ASSR Test Conditions SFD All (Eight Components) AM+FM (Four Components) CF 1500 Hz/MF 90 Hz 1.00 0.99 0.86 1.00 0.89 1.00 0.99 0.99 0.99 0.97 0.64 0.53 /ba/–/da/ All /ba/–/da/ Select 1.00 0.98 1.00 ASSR All AM+FM (Hi-MF) CF 1500 Hz/MF 90 Hz SFD /ba/–/da/ All /ba/–/da/ Select Note: The mean values for three ASSR responses and two SFD scores were calculated as a function of stimulus level. The three ASSR scores are (1) % present for all eight CF/MF components; (2) % present calculated for the four CF/MF components that had AM+FM (Hi-MF); (3) % present for the CF 1500 Hz/MF 90 Hz component. The two SFD scores were (1) % correct contrast discrimination for all subjects and (2) percent correct contrast discrimination for 12 select subjects for whom data were obtained for at least two stimulus levels. CF 5 carrier frequency; MF 5 modulation frequency; AM+FM 5 amplitude modulation and frequency modulation. 640 ASSR and SFD in Infants/Cone and Garinis canal and middle ear properties, thus leading to ‘‘better’’ responses for infants at 2500 Hz. Thresholds estimated from the data relating number of responses present to stimulus level (Figure 2) were elevated with respect to previously published results (Cone-Wesson et al, 2002; Rance et al, 2005). This is to be expected, because the stimulus used was a complex toneburst stimulus with four CFs and eight MFs. These may be ‘‘masked’’ threshold estimates, as there could be considerable interaction of one CF/MF component upon the other (John et al, 2002). Herdman and colleagues (2002) show that AM+FM tones produce a place-specific cochlear response; however, the place specificity is just over an octave band wide. Thus, cochlear activation areas produced by the AM+FM carriers at 1500, 2500, and 4000 Hz would be expected to overlap and affect the responses to one another, because they were spaced less than one octave apart. These CFs were used because they approximate the formant frequencies for some vowels. In previous studies of ASSR threshold, single CFs were used or the CFs were spaced at octave intervals so as to avoid interaction. In contrast, we were particularly interested in how the ear and brain responded when presented with a complex stimulus with (spectrally) overlapping stimuli, as this could give a clue into how speech sounds are encoded. Studies employing behavioral methods similar to those used in this study have established that infants under the age of one year are able to discriminate place-of-articulation cues. Studies of particular relevance to the current results are those completed by Nozza and associates (Nozza and Wilson, 1984; Nozza, 1987, Nozza et al, 1991a; Nozza et al, 1991b). They show that infants with normal hearing required higher levels than adults to reach their maximum performance on a speech feature discrimination task. We do not know if we reached the levels needed for maximum performance in the current study because we did not test above 70 dB SPL. Compared to the performance of adults, who achieved close to 100 percent discrimination scores at 30 dB SPL, it is evident that the infants need at least 25–30 dB greater levels to perform this discrimination of the place of articulation speech feature. The adult SFD performance scores suggest that the task required only detection of an acoustic difference between tokens, not discrimination or recognition. This is evident from the performance/level functions, which were very steep, with greater than 50 percent performance at 10 dB SPL and 99 percent at 30 dB SPL. The correspondence between the (infant) group mean SFD performance intensity function (% correct 3 level) and the group mean ASSR performance intensity function (% components present 3 level) was high (r . 0.95), although the correlation for individuals was modest (r 5 0.50). There was considerable variability in both the ASSR and SFD scores. The variability in ASSR, particularly among normalhearing infants, has recently been demonstrated by Rance and Tomlin (2006). They found variability in ASSR threshold, even when using single tones, rather than simultaneous presentation of modulated tones. ASSR is known to be of smaller amplitude than its ABR cousin and so, more easily obscured by myogenic and electrophysiologic noise. Using a stimulus paradigm with spectral overlap among the components, as in the present study, would increase the likelihood of masking and further variability. Another source of variability between the ASSR and SFD data was the difference in stimulus transducer used for each test. Insert earphones were used for ASSR, with one ear tested, whereas soundfield testing was used for the SFD test, and so both ears could contribute to the response. There were likely calibration differences between the two test conditions, especially considering the RECDs for the insert phone condition, as discussed previously. Admittedly, presentation of stimuli via insert phone for the SFD test would preferable. Earspecific testing with insert phones is the clinical standard for visual reinforcement audiometry (Widen et al, 2000). One application for SFD tests given in the sound field, as was done in this study, would be to test the performance of an infant with hearing loss as amplification or cochlear implant parameters were adjusted. The method used for testing infant speech feature discrimination incorporated familiar elements of visual reinforcement audiometry (VRA), including a number of training trials during which the contrast stimulus (speech feature change) was paired with a visual reinforcer. Unlike conventional VRA, the observertester did not know whether the trial contained a contrast or control stimulus. The percentage of correct detections is therefore based upon observer’s response, which in turn is contingent upon the infants emitting a behavior (head turn, eye widening, vocalization) that indicates that they have detected the stimulus change. This observer-based technique (Werner, 1995) controls for observer bias, unlike conventional VRA. When observer-based techniques are used to study infant psychophysical abilities, a lengthy training period is the norm for both observer and infant (Werner, 1995), so that the observer can learn to detect the infant’s responses. The training period used in this study may not have been long enough; or perhaps the training criterion was not of sufficient stringency to ensure optimal results. Another possibility may be that infants need training for each stimulus used in the discrimination task. The infants were trained to detect a /ba/ versus /sa/ speech feature change but were tested on the stimulus contrast /ba/ versus /da/. Although 641 Journal of the American Academy of Audiology/Volume 20, Number 10, 2009 infants were required to meet a performance criterion for the /ba/–/sa/ contrast, this may not have generalized to /ba/ versus /da/. Eisenberg and colleagues (Eisenberg et al, 2004, 2005, 2007) have reported their experiences with infant speech feature discrimination tests, and they are similar to the results in the present study. They used consonant voicing, manner and place contrasts, and a visually reinforced operant procedure to test normally hearing infants aged 7–11 months. Confidence level scores, their measure of test performance, ranged between 65 and 77 percent for these consonant contrasts. This is the same level of test performance achieved by infants in the present study, when tested using stimuli presented at levels of 50– 70 dB SPL. Overall, infant SFD performance increased with level, and variability decreased, an expected stimulus-response relationship. Certainly, there will always be a strong relationship between audibility and speech perception performance, as shown in adults with hearing loss (Yellin et al, 1989; Jerger et al, 1991), and various Articulation Index methods for estimating performance (Humes et al, 1986; Humes, 1991). It may be that the ASSR and SFD results of this study simply reflect the audibility of the stimuli, as both improve with increased SPL. And yet, the perceptual task was not merely to detect the presence of the stimulus, which would obviously improve with level, but, rather, to discriminate the difference between two stimuli based primarily upon a formant transition. There was a reasonably high correlation between the ASSR for the 1500 Hz AM+FM tone and SFD results. The acoustic cue for place of articulation is signaled by the change in the second formant transition, and for these sounds, the formant transition is in the range of 1500 Hz. It is not clear why the response to the 1500 Hz AM+FM tone was remarkably robust as a function of level, even in the presence of all the other ‘‘competing’’ stimulus components. There are other electrophysiologic methods that can be used to indicate brain stem mechanisms underlying speech perception. The frequency following response (FFR) is an evoked response that reflects the activity of phase-locking neurons of the auditory brain stem (Moushegian et al, 1973). When vowel sounds are used to evoke FFR, phase locking to the fundamental frequency of the vowel sound and its formants, at least up to 1500 Hz or so, can be detected (Krishnan, 2002). Reduced amplitudes or prolonged latencies of FFR in response to vowel tokens are evident in children with language-based learning disorders (King et al, 2002; Banai et al, 2005). The FFR is also influenced by language experience (Krishnan et al, 2005), which is further evidence that phase locking to vowel formants is a speech-encoding mechanism. There are, however, 642 no studies that have directly linked vowel perception or discrimination to FFR presence, amplitude, or latency. This is the first report of infant ASSRs evoked by a complex toneburst stimulus designed to represent the rapid amplitude and spectral modulations found for certain consonant–vowel transitions. This is the first report of infant speech feature–discrimination abilities as a function of level, using a methodology that could be developed for routine clinical use. This is the first report of the correlation between infant ASSR and SFD abilities. Although the correlations for individual subjects were modest, the grand mean results are encouraging. 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