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interaural level differences with multiple electrode stimulation in


bilateral cochlear-implant listeners. Ear Hear., 38, e22–e38.
https://doi.org/10.1097/AUD.0000000000000360
van Loon, M. C., Smits, C., Smit, C. F., Hensen, E. F., & Merkus,
P. (2017). Cochlear implantation in adults with asymmetric hearing
loss: Benefits of bimodal stimulation. Otol Neurotol, 38(6), e100–e106.
https://doi.org/10.1097/MAO.0000000000001418
van Wieringen, A., Boudewyns, A., Sangen, A., Wouters, J., &
Desloovere, C. (2018). Unilateral congenital hearing loss in children:
Challenges and potentials. Hear Res.
https://doi.org/10.1016/j.heares.2018.01.010
Wightman, F. L., & Kistler, D. J. (1992). The dominant role of low-
frequency interaural time differences in sound localization. J. Acoust.
Soc. Am., 91(3), 1648–1661. https://doi.org/10.1121/1.402445

CORTICAL AUDITORY EVOKED POTENTIALS INDICATE


SPEECH FEATURE DETECTION AND DISCRIMINATION

By Barbara K. Cone, Ph.D., CCC-A


University of Arizona Department of Speech, Language,
and Hearing Sciences

This paper provides a brief review of how cortical auditory evoked


potentials (CAEP) may be used to estimate speech-feature detection and
discrimination abilities in infants. Work in the Cone Lab has demonstrated
that these methods are reliable and valid for use with the individual, thus
making them clinically applicable. In adults with typical hearing, the
CAEP latency and amplitude measures are sensitive to binaural cues for
spatial release from masking. The aims of present and future research
are to provide an objective means of evaluating speech perception, and
verifying and validating hearing instrument settings.

Introduction
Efforts for early identification and evaluation of hearing loss in
infants has been a major tenet of pediatric audiology and deaf education
since the 1940s. The past three decades, in particular, have been
important to our realization that any degree of hearing loss in an infant

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can cause sensory deprivation, and this can impact brain and perceptual
development. We know that infants with hearing loss may be delayed
in developing the ability to distinguish between phonemes and that, if
untreated, this can lead to receptive and expressive listening and spoken
language delays (Tomblin, 2015).
When families choose amplification and/or cochlear implants for
the infant to facilitate listening and spoken language development, we
know that a critical outcome is the ability to detect and discriminate
speech sounds. Measures of speech perception are critically important
to validating the amplification strategy (American Academy of
Audiology, 2013). Yet, despite the critical importance of speech feature
perception and discrimination abilities for developing listening and
spoken language, there are no clinical methods for assessing this ability
in infants or toddlers who have a receptive language age of less than
2.4 years. Although Eisenberg and colleagues (2007), and more recently
Uhler and colleagues (2017), have developed a visual-reinforcement
infant speech discrimination (VRISD) test method, these methods have
not yet had uptake into the specialty pediatric audiology centers (Uhler
& Gifford, 2014), likely because up to 40% of infants with typical hearing
have difficulty learning the conditioned head-turn task required in these
methods (Cone, 2015; Cowan et al., 2017).
What has motivated my research for the past 15 years is this
challenge: To establish sensitive and specific electrophysiologic methods
for evaluating speech-feature detection and discrimination in infants
and toddlers. I believe that these objective, electrophysiologic methods
would be of tremendous benefit for clinicians who need to measure
auditory abilities of infants and children with hearing loss and to
validate the hearing aid or cochlear implant fitting/mapping. This paper
will review the results from my lab towards this goal.

Summary of Research Findings


Work from Other Labs
During the past two decades, research using auditory evoked
potentials from the cortex has seen a resurgence after taking a back
seat for 25 years to the auditory brainstem response (ABR). This
research shows that cortical-evoked responses for speech sounds have
a correspondence with behavioral measures of speech perception, and
thus show the potential for indicating the therapeutic effects of hearing

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aids and cochlear implants. For example, Sharma and colleagues (2002,
2005) have demonstrated that the cortical auditory evoked potential
(CAEP) component P1 latency indicates cortical plasticity attributed to
the use of cochlear implants, and that changes in P1 latency during the
first months of implant use can be used as a ‘biomarker’ of expected
auditory maturation or plasticity following electrical stimulation of the
auditory nerve.

Work Completed in My Lab: Findings in Infants and Children


Rance and colleagues (2002) in Australia measured CAEPs in a
group of infants and young children diagnosed with auditory neuropathy
spectrum disorder. The research showed a strong, statistically significant,
positive correlation between the presence of CAEP and the child’s speech
perception abilities. These findings were the first to suggest that CAEP
could be used as a prognostic measure of speech perception in infants
and young children with auditory neuropathy (Cone, 2008). This is
especially important as a hallmark of auditory neuropathy type hearing
loss is that the ABRs are absent for clicks, tones, or speech sounds and
so cannot be used to estimate hearing abilities. These findings have now
been independently replicated and extended by the work of Golding et
al. (2007), Sharma et al. (2011), and He et al. (2015).
In 2006, the Cone Lab published findings from new techniques for
measuring CAEPs in infants and toddlers who were awake (Wunderlich
et al., 2006). We used tones and speech tokens to evoke CAEPs from
newborns, infants, toddlers, and pre-schoolers. One of the novel aspects
of this work is that we presented the low and high frequency tones, and
words “bad” and “dad”, at a very slow rate, effectively about one word
every three seconds. Most other researchers use rates of one word per
second, or even slightly faster. Figure 1 shows examples of CAEP results
from newborns. What was found is that an early negative trough could
be discerned. It was previously thought that this part of the cortical
response, the N1, did not emerge until after age 8 or 10 years. By
using a very slow stimulus rate, a new developmental perspective for
interpreting CAEP in infants and children was found. We hypothesized
that the presence of this biomarker may estimate neurodevelopment in
infants and young children with hearing loss.
Cone and Whitaker (2013) employed the slow rate method to test
the hypothesis that CAEP could be used to estimate tone and speech

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detection abilities in infants. We tested 36 infants with typical hearing


and typical neurodevelopment. The infants were between the ages of 5
and 12 months (mean age of 8 months) and they were tested while awake.
We used tones at 500, 1000, 2000, and 4000 Hz, and Ling speech sounds
(Ling, 1988) to evoke CAEPs. Tones were used to estimate hearing
across the range of hearing typically tested in a clinical evaluation. The
Ling sounds had ecological validity as they are commonly used in simple,
functional, trouble-shooting tests of hearing aids and cochlear implants.
Figure 2 shows examples of CAEP wave forms from infants for different
vowel tokens. The amplitude of the CAEP was measured as a function
of stimulus level. These amplitude input-output functions (Figure 3) in
infants were quantitatively similar to those found in adults. These results
from the cortex reflect the maturity of cochlear mechanisms that have
been found using otoacoustic emission and ABR techniques. Perceptual
estimates of threshold were also measured using visually reinforced
behavioral methods similar to those used in visual reinforcement
audiometry. Infant perceptual thresholds were 20 dB higher than those
of adults, as has been found in many other studies of infant perceptual

Figure 1. Newborn CAEPs to Speech and Tones. CAEP were obtained from
newborns. Word tokens (“dad” or “bad”), low frequency tones (400 Hz), and high
frequency tones (3000 Hz) were used to evoke the CAEP. Newborns were tested
as they slept. Note that the newborn CAEP in response to words is much larger
than the response to a low frequency tone, and the response to the low frequency
tone is larger than the response to a high frequency tone. These results illustrate
the sensitivity of the newborn CAEP to spectral complexity (word stimuli) and also
to stimulus frequency.

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thresholds. Yet CAEP thresholds were found at 10–15 dB lower levels on


average, compared to perceptual thresholds. This discrepancy between
perceptual and electrophysiologic threshold is also found for the ABR.
The advantage of CAEPs is that the response at threshold has a larger
amplitude relative to the background EEG, when compared to ABR.
Another way in which CAEPs can be used to help us evaluate infant
hearing is to record a response to changes in speech sounds. This can
be done for vowel sounds, consonant-vowel sounds, and fricatives.
This evoked response from the cortex is called the Acoustic Change
Complex (ACC). A vowel token such as /a/ can be played in a quasi-
steady state or continuous fashion, and then a change to /i/, /o/, or

Figure 2. Infant CAEP for Vowel Stimuli. CAEPs for tones and Ling sounds were
obtained from a group of infants less than 12 months of age who were tested while
awake. The examples shown are from individual infants. The CAEP waveforms are
shown as a function of dBA SPL. Note the replicability of the waveforms shown
in response to vowel token /a/, and also that a response is present at 40 dBA. The
response for token /u/ was present down to a level of 50 dBA in this example. The
mean CAEP minimum response level was 10–15 dB better (lower) than the mean
behavioral detection thresholds.

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Figure 3. CAEP Input-Output Functions. The amplitude of CAEP components P1-


N1-P2 were measured as a function of stimulus level in young adults and infants
(mean age = 7 months). The slope of the input-output function for infants is
equivalent to those of adults indicating the maturity of cochlear mechanisms, in
particular the compressive non-linearity of the outer hair cells.

/u/ can be introduced. The start of the first vowel evokes a CAEP and
then the change to another vowel evokes a second CAEP, and that is
called the ACC. As in a previous study (Cone & Whitaker, 2013), infants
with typical hearing under the age of 12 months were tested using this
vowel change test while they were awake and sitting in a high chair
(Cone, 2015). They were kept engaged and quiet by a test assistant
who interacted with them with quiet toys. Figure 4 shows examples of
ACC waveforms obtained in a control condition when there is no vowel
change, compared to the responses when there is a contrasting vowel.
The amplitudes in the contrast conditions are two to six times greater
than those obtained in the control (no-change condition). These ACCs
were obtained in over 90% of the infants tested.
The ability of infants to detect a change in vowel sound was also
tested behaviorally. We used an operant conditioning paradigm and

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video cartoon samples as a reinforcer. On average, infants with typical


hearing could only get 68% of the contrasts correct, despite using up
to 15 training trials. There were many infants who had clear ACCs
but could not learn the behavioral “game” (test method) in order to
determine their discrimination abilities. Even so, for infants who could
learn the behavioral test, there were moderate to strong correlations (r =
0.5–0.81) between the perceptual and electrophysiologic results.

Figure 4. Acoustic Change Complex for Vowels. CAEPs were obtained in a group
of infants under the age of 12 months, tested while awake. Vowel stimuli were
presented in a quasi-steady fashion: Each token had a duration of 500 ms, and these
were presented at a rate of 2/s, creating a modulated stimulus with modulation rate
of 2 Hz. The probability of the /a/ token was 75% and the probability of a contrasting
token (either /i/ or /o/) was 25%. A control condition in which the token did not
change was also obtained. The response to the standard /a/ (75% probability) does
not exhibit a clear response because at this rate, the CAEP has undergone neural
adaptation. The response to the “control” condition, /a/, has an onset response,
P1, at around 150 ms. When there is a test condition and the token changes to /i/
or /o/, the evoked response exhibits P1, N1, and P2 components. This onset-like
response to a stimulus change is known as the acoustic change complex (ACC). The
amplitude of the ACC is two to six times larger than the response in the control
condition, and is present in 90% of the infants tested.

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Findings in Adults
The feasibility of the methods in those with hearing loss was
demonstrated in a pilot project with adults, who were tested with
and without hearing aids. Ten adults with mild to moderately severe
sensorineural hearing loss were tested using the vowel-contrast paradigm,
or ACC (Cone, 2015). The contrasts /a/ versus /i/ and /o/ versus /u/ were
presented at two levels, 60 and 30 dBA sound pressure level (SPL). For
the aided conditions, listeners wore Phonak Naida IX BTE hearing aids
programmed according to the NAL-NL2 formula for their hearing loss
and verified in situ. The presence, latency, and amplitude of the ACCs
were measured as a function of vowel contrast type, level, and listening
condition (aided versus unaided) and audiogram configuration. Only
40% of subjects had responses present at 30 dBA in the aided condition.
When present, the ACC obtained in the aided condition demonstrated
significantly larger amplitudes than those in the unaided condition.
These increased ACC amplitudes exhibited the improved audibility and
access to frequency and timing information necessary to discriminate
vowel contrasts.
The hearing aid, although fit to a prescriptive target and verified
in situ, was not providing adequate audibility for the brain to register
the vowel differences at 30 dBA for 60% of the subjects. This finding
suggests a role for having cortical-evoked potential validation of hearing
aid fitting in infants, providing information that goes beyond verification
of audibility to validation of speech-feature discrimination by the cortex.
The ACCs can also be obtained in children who use cochlear implants.
Figure 5 shows the waveforms from a 10-year-old who is deaf and uses
a cochlear implant to hear. When the cochlear implant is not turned on,
there is no response. When it is turned on, there is a clear response for
vowel changes /u/–/i/ and /a/–/i/.
We have recently completed an experiment in young adults with
typical hearing that is dependent on binaural hearing to extract speech
in a noise background. When speech and a noise masker are co-located,
that is, coming from the same direction, the masker has a maximum
effect. When the speech signal and noise are spatially separated, there
can be an improvement in speech detection threshold. This is known as
spatial release from masking. Spatial release from masking is due to brain
mechanisms for detecting time and level differences that occur between
the ears due to the sound location. Previous research on perceptual

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Figure 5. ACC: Child with a Cochlear Implant. A 10-year-old who uses a cochlear
implant to hear was tested using an ACC paradigm. Vowel sounds /a/ and /i/ were
used to evoke the ACC, presented through a loudspeaker. The left panels illustrate
that no responses are evident when the implant is not activated. The right panels
illustrate that ACCs are present for the /i/–/a/ and /a/–/i/ stimulus contrasts. The
ACC paradigm employs a standard stimulus (75% probability), a control stimulus
(no change in token), and a contrast stimulus (25% probability). ACCs are present
only for the contrast and not for the control condition. Also, the /i/–/a/ ACC has a
different morphology than the /a/–/i/ ACC because the direction of vowel formant
frequency change is high-to-low for /i/–/a/, and low-to-high for the /a/–/i/ contrast.

measures of spatial release from masking indicate a 3–6 dB advantage


for the spatially-separated condition, and that can translate into a 30%
improvement in speech perception scores. Yet, past research has also
shown that people with hearing loss may have a reduced spatial release
from masking benefit or none at all, even with directional hearing aids.
Also, there is some uncertainty about when this ability reaches maturity
in children with hearing loss, and very little data about how and if this
develops in infants and children with hearing loss.
We aimed to demonstrate that evidence of spatial release from
masking would be evident in cortical evoked responses. We used

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speech sounds /ta/ and /da/ to evoke CAEPs in quiet and in noise. We
systematically varied the speech sound levels, the signal-to-noise ratios
(SNR), and the noise location. First, we established the CAEP latencies
in quiet. Then, co-located noise was introduced at SNRs of 10, 0, and -5
dB. CAEPs were obtained for each combination of stimulus and SNR.
Then, the noise masking was spatially separated from the speech sound
and CAEPs were obtained in that condition.
The first result is that the latency or timing of the CAEP brainwave
is shorter for /da/ compared to /ta/. That is, the CAEP is sensitive to the
voiced versus voiceless consonant differences (Figure 6). These latency
differences were seen in both quiet and noise conditions.
The second result was that there were significant differences in CAEP
latency and amplitude when the co-located versus spatially-separated
noise conditions were compared (Figure 7). The decrease in latency and
the increase in amplitude in the spatially-separated conditions were
interpreted as release from masking. This was consistent with results
from speech perception tests conducted in co-located and spatially-
separated noise that demonstrated the typical 3 dB SNR speech-in-
noise benefit.
It is possible that the spatial release from noise benefit was due to the
head shadow effect. When the 20-talker speech-babble masking noise
was moved 90˚ from the source of the speech token (a speaker at 0˚
azimuth, facing the listener), there was a 12–16 dB difference in high
frequency (2000–6000 Hz) energy at the right versus left ear. Interaural
level differences such as this are used by the brain to separate the speaker
from back-ground noise. The results from the CAEP electrophysiology
test were sensitive to these interaural level differences, suggesting that
these methods could be used to determine the amount of directionality
and noise reduction benefit that an infant or child receives from their
hearing device.

Summary and Conclusion


Behavioral test results are often touted as the gold standard for
pediatric audiology. Yet, there are many instances in which the infant
or toddler behavioral repertoire is limited or simply not reliable. This
is why we rely on electrophysiologic methods, such as the ABR, to
estimate audiometric thresholds when we know that we cannot obtain
valid behavioral estimates. It is now possible to estimate speech-feature

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Figure 6. CAEP Latencies for /ta/ and /da/ Speech Tokens. CAEPs were obtained
from a group of college-aged students, all with typical hearing, in response to
speech tokens /ta/ and /da/. The stimuli were presented via loudspeaker at 0°
azimuth (in front of listener), at a distance of 1.5 meters. The mean latencies for
CAEP components P1, N1, and P2 are shown, with the error bars indicating the
standard deviation. The CAEP latencies in response to /da/ are 35–50 ms shorter
than those to /da/. The CAEP accurately encodes the voice onset time. For /da/,
the voice onset time is essentially 0 ms, whereas for /ta/ the voice onset time is
approximately 40 ms.

detection and discrimination abilities in infants using the CAEP with


metrics that are valid for individuals, and thus clinically applicable.
In adults with typical hearing, the CAEP latency distinguishes the
difference between voiced versus voiceless speech features, and latency
and amplitude measures are sensitive to the binaural cues for spatial
release from masking. The aims of present and future research are
to provide an objective means of evaluating speech perception, and
verifying and validating hearing instrument settings.

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Figure 7. CAEPs: Spatial Release from Masking. Grand mean waveforms in response
to speech tokens /ta/ and /da/ are shown for CAEPs obtained when masking noise
(20-talker babble) was co-located (Co), and also when it was spa-tially separated
(R) at 90°. The latencies decreased and the amplitudes increased when the masking
noise was spatially separated from the speech token. This was interpreted as
electrophysiologic evidence of spatial release from masking.

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References
American Academy of Audiology. (June 2013). Pediatric amplification
clinical practice guidelines. Retrieved from https://www.audiology.org/
sites/default/files/publications/ PediatricAmplificationGuidelines.pdf
Cone, B. (2008). The electrophysiology of auditory neurop-athy
spectrum disorder. In J. Northern (Ed.), Guidelines for identification
and management of infants and young children with auditory neuropathy
spectrum disorder (pp. 20–27). Denver, CO: The Bill Daniel’s Center for
Children’s Hearing.
Cone, B.K. (2015). Infant cortical electrophysiology and perception
of vowel contrasts. International Journal of Psychophysiology, 95, 65–
76. https://doi.org/10.1016/j.ijpsy-cho.2014.06.002
Cone, B., & Whitaker, R. (2013). Dynamics of infant cortical auditory
evoked responses for tones and speech. International Journal of Pediatric
Otorhinolaryngology, 77(7), 1162–1173.
https://doi.org/10.1016/j.ijporl.2013.04.030
Cowan, R., Ching, T., Van Dun, B., Zhang, V., Wong, C., Bardy, F., …
Dillon, H. (2017). Evaluating auditory discrimination in infants using
visual reinforcement infant speech discrimination (VRISD) and the
acoustic change complex (ACC). Journal of Hearing Science, 7(2), 56.
Eisenberg, L.S., Martinez, A.S., & Boothroyd, A. (2007). Assessing
auditory capabilities in young children. International Journal of
Pediatric Otorhinolaryngology, 71, 1339–1350.
https://doi.org/10.1016/j.ijporl.2007.05.017
Golding, M., Pearce, W., Seymour, J., Cooper, A., Ching, T., & Dillon,
H. (2007). The relationship between obligatory cortical auditory evoked
potentials (CAEPs) and functional measures in young infants. Journal
of the American Academy of Audiology, 18(2), 117–125.
https://doi.org/10.3766/jaaa.18.2.4
He, S., Grose, J. H., Teagle, H. F., Woodard, J., Park, L. R., Hatch,
D. R.,…Buchman, C. A. (2015). Acoustically evoked auditory change
complex in children with auditory neuropathy spectrum disorder: A
potential objective tool for identifying cochlear implant candidates. Ear
and Hearing, 36(3), 289–301.
https://doi.org/10.1097/AUD.0000000000000119
Ling, D. (1988). Foundations of spoken language for the hearing-
impaired. Washington, DC: Alexander Graham Bell Association for the
Deaf.

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Rance, G., Cone-Wesson, B., Wunderlich, J., & Dowell, R. C. (2002).


Speech perception and cortical event related potentials in children with
auditory neuropathy. Ear and Hearing, 23(3), 239–253.
https://doi.org/10.1097/00003446-200206000-00008
Sharma, A., Cardon, G., Henion, K., & Roland, P. (2011). Cortical
maturation and behavioral outcomes in children with auditory
neuropathy spectrum disorder. International Journal of Audiology,
50(2), 98–106. https://doi.org/10.3109/14992027.201 0.542492
Sharma, A., Dorman, M. F., & Kral, A. (2005). The influence of
a sensitive period on central auditory development in children with
unilateral and bilateral cochlear implants. Hear. Res., 203, 134–143.
https://doi.org/10.1016/j.heares.2004.12.010
Sharma, A., Dorman, M. F., & Spahr, A. J. (2002). A sensitive period
for the development of the central auditory system in children with
cochlear implants: implications for age of implantation. Ear. Hear., 23,
532–539. https://doi. org/10.1097/00003446-200212000-00004
Tomblin, B. (2015). Language outcomes in young children with mild-
to-severe hearing loss. Ear. Hear., 36, Suppl. 1, 76S–91S.
https://doi.org/10.1097/AUD.0000000000000219
Uhler, K., & Gifford, R. H. (2014). Current trends in pediatric cochlear
implant candidate selection and postoperative follow-up. American
Journal of Audiology, 23, 309–325.
https://doi.org/10.1044/2014_AJA-13-0067
Uhler, K., Warner-Cysz, A., Gifford, R. H., & PMSTB Working Group.
(2017). Pediatric minimum speech test battery. Journal of the American
Academy of Audiology, 28, 232–247. https://doi.org/10.3766/jaaa.15123
Wunderlich, J. L., Cone-Wesson, B. K., & Shepherd, R. (2006).
Maturation of the cortical auditory evoked potential in infants and
young children. Hearing Research, 212(1-2), 185–202.
https://doi.org/10.1016/j.heares.2005.11.010

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