Stimulus level effects on speech-evoked obligatory cortical auditory evoked potentials in infants with normal hearing

https://doi.org/10.1016/j.clinph.2012.09.011Get rights and content

Abstract

Objective

To determine stimulus level effects on speech-evoked cortical auditory evoked potentials (CAEPs) in infants for a low (/m/) and high (/t/) frequency speech sound.

Methods

CAEPs were recorded for two natural speech tokens, /m/ and /t/. Participants were 16 infants aged 3–8 months with no risk factors for hearing impairment, no parental concern regarding hearing or development, and normal tympanograms and otoacoustic emissions. Infants were either tested at levels of 30, 50, and 70 dB SPL or at 40, 60, and 80 dB SPL, in counterbalanced order.

Results

Input–output functions show different effects of increasing sound level between stimuli. There were minimal changes in latency with increase in level for /t/. For /m/, there were approximately 50–60 ms latency increases at soft compared to loud levels. Amplitudes saturated at moderate–high levels (60–80 dB SPL) for both stimuli.

Conclusions

Infants’ CAEP input–output functions differ for /t/ versus /m/ and differ from those previously reported for adults for other stimuli. Effects of stimulus and level on CAEPs should be considered when using CAEPs for hearing aid or cochlear implant evaluation in infants.

Significance

Speech-evoked CAEPs provide an objective measure of central auditory processing. Possible differences in CAEP growth between infants and adults suggest developmental effects on intensity coding by the auditory cortex.

Highlights

► This study shows robust cortical auditory evoked potential (CAEP) amplitudes at low stimulus levels in infants. ► The effect of stimulus level on CAEP latencies differs between speech stimuli. ► CAEP input–output functions for infants differ from published findings for adults.

Introduction

Obligatory cortical auditory evoked potentials (CAEPs) can provide source and timing information regarding neural processes that underlie speech perception (Alain and Tremblay, 2007, Oates et al., 2002, Martin et al., 2008). In addition, CAEPs can be used clinically to assess auditory system maturation, auditory processing ability, and speech audibility in infants with hearing loss (Rapin and Graziani, 1967, Gravel et al., 1989, Sharma et al., 2002, Golding et al., 2007, Martin et al., 2008). CAEPs are robust responses that can been evoked by clicks, tones, and speech sounds across the life span, in infants (Kurtzberg et al., 1984, Ponton et al., 2002, Purdy et al., 2004), young children (Ponton et al., 1996, Cunningham et al., 2000, Ceponiene et al., 2002, Sharma et al., 2007), adolescents (Ponton et al., 1996, Cunningham et al., 2000), young adults (Ponton et al., 1996, Cunningham et al., 2000, Wunderlich and Cone-Wesson, 2001, Sharma et al., 2002), and the elderly (Cunningham et al., 2000). Although CAEP peaks, especially P2, are influenced by attention (Coch et al., 2005), obligatory CAEPs are typically recorded using a passive listening paradigm, with the listener watching a silent subtitled video or reading. Infants can be tested while they are awake and distracted by a visually engaging toy or book (Purdy et al., 2004) or during “active” sleep (Kurtzberg et al., 1984, Novak et al., 1989, Kushnerenko et al., 2001).

Stimulus parameters that influence CAEP characteristics include presentation rate (Budd et al., 1998, Sharma et al., 2007), stimulus duration (Onishi and Davis, 1968, Agung et al., 2006, Beukes et al., 2009), stimulus level (Madell and Goldstein, 1972; Garinis and Cone-Wesson, 2007), and type of speech sound (Kurtzberg, 1989, Sharma and Dorman, 1999, Agung et al., 2006) or tonal stimulus frequency (Jacobson et al., 1992). Golding et al. (2006) recorded speech-evoked CAEPs in infants and reported significantly smaller and later P1 latencies for /m/ compared to /t/, across a range of stimulus durations and inter-stimulus intervals. This is consistent with a magnetoencephalography study of adult listeners by Gage et al. (1998), that showed larger cortical amplitudes and shorter latencies for words with initial stop consonants (/b/, /p/, /d/, /t/, /g/, /k/) versus non-stops (/f/, /l/, /m/, /r/, /s/). Gage et al. (1998) suggested that these differences are due to stops having greater energy at onset than other sounds. The auditory cortex is dominated by neurons with discharge spikes time-locked to the onset of auditory stimuli (Heil, 1997) and the /t/ stimulus has a much faster onset-to-peak time than /m/ (Golding et al., 2006). Prasher (1980) investigated whether onset effects on CAEP latencies and amplitudes are affected by spectral splatter effects by comparing effects of rise time for tones and noise, and found that latencies reduced with stimulus rise time for noise and tonal stimuli, but amplitude increases for short rise times only occurred for tonal stimuli. Thus, both spectral and temporal differences are likely to account for the latency and amplitude differences between /m/ and /t/ CAEPs reported by Golding et al. (2006).

The effects of stimulus parameters on infant CAEPs have not been investigated as extensively as they have in adults (Hyde, 1997). A number of studies have shown that, for stimulus rates of about 1 per second, CAEPs in infants are dominated by the P1 peak occurring at about 100–300 ms after stimulus onset, followed by a late negativity at about 350 ms (Kurtzberg et al., 1984, Ponton et al., 1996, Kushnerenko et al., 2001, Sharma et al., 2002, King et al., 2008).

The adult CAEP waveform consists of distinct P1, N1, and P2 peaks. Up to about 7 years of age the vertex-recorded cortical potential often primarily consists of a single positive wave rather than a P1–N1–P2 complex. P1 latency shows considerable maturational change in the preschool period, reducing from several hundred milliseconds in very young infants (e.g. Sharma and Dorman, 2006) to approximately 100 ms at 5 years (see review by Wunderlich and Cone-Wesson, 2006). CAEPs recorded in adults using similar stimulus presentation rates have earlier P1, N1, and P2 peaks occurring at about 50, 100, and 200 ms, respectively. The time range of the adult N1–P2 overlaps with the infant P1 occuring between 100 and 300 ms. Ponton et al. identified tangential and radial N1 sources, with differing maturational time courses, and proposed that P1 is reduced in adults due to phase cancellation of the later parts of the P1 peak by the increasing magnitude of N1. Hence, when adult and infant studies are compared it is difficult to separate stimulus influences on P1 and N1 since these peaks in the CAEP waveform are likely to have overlapping sources.

Studies reporting effects of stimulus and recording parameters on CAEPs in adults generally focus on N1. Adult findings cannot be readily extrapolated to infants, however, since P1, N1, and P2 have different sources and maturation patterns (Ponton et al., 2002) and thus the effects of stimulus parameters may differ across these peaks. In adults P1 is small; reduced P1 amplitudes are associated with the emergence of a large N1 in late childhood (Ponton et al., 2002). Thus, intensity effects on P1 in adults may be difficult to observe and have not been widely reported. In general, adult N1 and P2 latencies reduce and amplitudes increase as stimulus level increases from near-threshold to loud levels, but there are variations across studies in the shape of the input–output function for CAEP latencies and amplitudes (Beagley and Knight, 1967, Picton et al., 1974, Morita et al., 2006, Kaskey et al., 1980, Garinis and Cone-Wesson, 2007, Lütkenhöner and Klein, 2007). Differences in stimulus type, duration and inter-stimulus interval, and the range of presentation levels investigated are likely to account for the variation in findings.

To our knowledge CAEP input–output characteristics have not been reported for infants. CAEP input–output characteristics are of interest because of the use of CAEPs to evaluate the audibility of amplified speech in children with hearing impairment (Purdy et al., 2004, Martin et al., 2008). The aim of the current study was to assess the effects of stimulus level on latencies and amplitudes of speech-evoked CAEPs in infants, using two speech sounds (/m/ and /t/) with different spectral and temporal characteristics that are known to produce differences in CAEP morphology.

Section snippets

Participants

Participants were 16 infants (5 girls and 11 boys) aged 2.5–10 months (mean 5.3 months, SD 2.6), with no risk factors for hearing impairment and no parental concerns about hearing. Prior approval for the study was obtained from Ethics Review Board of University of Auckland. All participants had normal 1000-Hz tympanograms (Baldwin, 2006) on the day of testing and passed transient evoked otoacoustic emission testing. Infants were randomly divided into two groups to be tested using levels of either

Results

Grand average CAEP waveforms recorded in response to /m/ and /t/ are shown in Fig. 2. All infants had a P1 response at approximately 150–200 ms, followed by a negativity at about 250–300 ms. There is an additional earlier biphasic response (positivity followed by a negativity) evident in the /t/ grand average waveforms for the higher stimulus levels. This biphasic peak evident in the responses to /t/ at higher stimulus levels is the post auricular response (PAMR), occurring at approximately 20–50 

Discussion

The current study was undertaken to determine the effects of stimulus level on cortical responses to a high and a low frequency speech sound in babies. CAEPs were recorded across the range of stimulus levels for both stimuli. CAEPs show a trend of increasing amplitudes up to 50 dB SPL for /m/ and up to 60 dB SPL for /t/. The differences in amplitude across stimulus level were not significant for /t/. This may be due to a lack of statistical power as a result of the small sample size and amplitude

Conclusions

CAEP input–output functions for /m/ and /t/ behave differently. Increasing audibility influences speech-evoked CAEP amplitudes and latencies, but only over a limited range of stimulus levels. If the results obtained here are applicable to children with hearing loss, CAEP amplitudes may be robust, even when stimuli are at low sensation levels, particularly for the high frequency speech sound /t/. Thus, loudness is unlikely to correlate with CAEP amplitudes. The presence of CAEPs indicates

Acknowledgment

This research was supported in part by a Churchill Fellowship awarded to the fourth author.

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