International Journal of Pediatric Otorhinolaryngology 76 (2012) 1332–1338

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International Journal of Pediatric Otorhinolaryngology

journal homepage: www.elsevier.com/locate/ijporl

Speech perception and cortical auditory evoked potentials in cochlear implant

users with auditory neuropathy spectrum disorders
Kátia F. Alvarenga a,b,*, Raquel Beltrão Amorim a, Raquel Sampaio Agostinho-Pesse a,
Orozimbo Alves Costa a,b, Leandra Tabanez Nascimento b, Maria Cecilia Bevilacqua a,b
a
Department of Audiology and Speech Pathology at the School of Dentistry, University of São Paulo, Bauru Campus, Brazil
b
Center for Audiological Research at the University of São Paulo, Bauru Campus, Brazil

A R T I C L E I N F O A B S T R A C T

Article history: Objective: To characterize the P1 component of long latency auditory evoked potentials (LLAEPs) in
Received 20 December 2011 cochlear implant users with auditory neuropathy spectrum disorder (ANSD) and determine firstly
Received in revised form 29 May 2012 whether they correlate with speech perception performance and secondly whether they correlate with
Accepted 3 June 2012
other variables related to cochlear implant use.
Available online 15 July 2012
Methods: This study was conducted at the Center for Audiological Research at the University of São Paulo.
The sample included 14 pediatric (4–11 years of age) cochlear implant users with ANSD, of both sexes,
Keywords:
with profound prelingual hearing loss. Patients with hypoplasia or agenesis of the auditory nerve were
Long latency auditory evoked potentials
Cochlear implant
excluded from the study. LLAEPs produced in response to speech stimuli were recorded using a Smart EP
Hearing impaired USB Jr. system. The subjects’ speech perception was evaluated using tests 5 and 6 of the Glendonald
Auditory neuropathy spectrum disorder Auditory Screening Procedure (GASP).
Results: The P1 component was detected in 12/14 (85.7%) children with ANSD. Latency of the P1
component correlated with duration of sensorial hearing deprivation (*p = 0.007, r = 0.7278), but not
with duration of cochlear implant use. An analysis of groups assigned according to GASP performance (k-
means clustering) revealed that aspects of prior central auditory system development reflected in the P1
component are related to behavioral auditory skills.
Conclusions: In children with ANSD using cochlear implants, the P1 component can serve as a marker of
central auditory cortical development and a predictor of the implanted child’s speech perception
performance.
ß 2012 Elsevier Ireland Ltd. All rights reserved.

1. Introduction Brainstem and cortical mechanisms involved in processing

The use of cochlear implants in the treatment of individuals
with severe or profound sensory hearing loss, such as that due to
auditory neuropathy spectrum disorder (ANSD), has been studied
extensively and, therefore, become widely accepted by the
scientific community. When the cochlear implant is switched
on, electrical stimulation from the implant commences, triggering
cortical reorganization in the auditory system following a period of
sensory deprivation. The development of auditory structures in
these patients has often been similar to that which occurs in
hearing people.
* Corresponding author at: Departamento de Fonoaudiologia da Faculdade de
Odontologia da Universidade de São Paulo, Alameda Dr. Octávio Pinheiro Brisola, 9-
75 Bauru, São Paulo, CEP 17.012-901, Brazil. Tel.: +55 14 32358332;
fax: +55 14 32234679.
E-mail address: katialv@fob.usp.br (K.F. Alvarenga).
auditory stimulation can be investigated non-invasively via
recording of auditory evoked potentials (AEPs). Physiological
changes in the auditory system during the development of
peripheral and central systems are reflected in AEP latency and
amplitude, allowing the relationship between these changes and
behavioral development of listening skills to be studied. Many
researchers have chosen to examine long latency auditory evoked
potentials (LLAEPs), which reflect the general electrical activity
generated in the cortico–thalamo–cortical pathway, primary
auditory cortex, and associative cortical areas [1]. More specifical-
ly, the P1 component of the LLAEP has been used as a biomarker to
infer the state of maturation of auditory structures in infants and
children [2]. Numerous studies have described the latency and
amplitude of this component (see Tables 1 and 2) in normally
hearing children under 12 years of age [3–11]. A recent study at our
center that examined children in the age range of 3–12 years
demonstrated that the latency of the P1 component decreases by
1.6 ms per year following installment of a cochlear implant [12].

0165-5876/$ – see front matter ß 2012 Elsevier Ireland Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.ijporl.2012.06.001
 K.F. Alvarenga et al. / International Journal of Pediatric Otorhinolaryngology 76 (2012) 1332–1338 1333

Table 1
Summary of previously published mean P1 component latencies (SD) in normally hearing children 0–12 years.

Age (y) P1 (ms)

Ohlrich Barnet [4] Satterfield Satterfield Sharma Albrecht et al. [3] Ponton Ceponiene Gilley
and and et al. [10] et al. [11] et al. [8] et al. [5] et al. [6]
Barnet [7] Braley [9] LH RH

1 (month) 63.0 (10) 65.0 (24) – – – – – – – –

6 (months) 89.0 (39) 99.0 (27) – – – – – – – –
1 66.0 (20) 65.0 (11) – – – – – – – –
2 – 76.0 (19) – – – – – – – –
3 – 67.0 (27) – – – – – – – 107.0 (10)
4 – – – – – – – – 110.0 (14) 107.0 (10)
5 – – – – – 106.0 (9.0) 92.0 (25) 85.0 (16) – 99.0 (21)
6 – – 85.6 (19) 81.33 87.0 (14) 106.0 (9.0) 92.0 (25) 85.0 (16) – 99.0 (21)
7 – – 85.6 (19) 81.33 81.0 (10) 105.0 (10) 94.0 (11) 79.0 (22) – 100.0 (16)
8 – – 89.4 (16) 86.44 79.0 (10) 105.0 (10) 94.0 (11) 66.0 (13) – 100.0 (16)
9 – – 89.4 (16) 86.44 81.0 (5) 99.0 (13) 88.0 (12) 68.0 (16) 111.0 (21) 89 (17)
10 – – 97.8 (6) 95.31 74.0 (18) 99.0 (13) 88.0 (12) 64.0 (6) – 89 (17)
11 – – 97.8 (6) 95.31 78.0 (11) 84.0 (18) 80.0 (26) 61.0 (10) – 82.0 (8)
12 – – 97.8 (6) 95.31 74.0 (15) 84.0 (18) 80.0 (26) 54.0 (16) – 82.0 (8)

LH, left hemisphere; RH, right hemisphere.

In this context, several studies have evaluated auditory function
in cochlear implant users to elucidate how the acoustic signal
processing occurs. Moreover, LLAEPs in implanted individuals with
sensory hearing loss (as opposed to ANSD) have been studied
extensively [13–21], and LLAEP findings have been correlated with
their speech perception performance [22–35]. Thus, the applica-
bility of LLAEP recording to assessment of the auditory system in
cochlear implant users has been well demonstrated.
Previous studies have demonstrated a correlation between
duration of cochlear implant use and the latency of LLAEP
components, which gradually decreases [14,16,18,36,37]. Howev-
er, when the relationship between P1 component latency and
duration of sensory deprivation was examined, it was observed
that later cochlear implant implantation was associated with
reduced variability of the P1 component latency over repeated
recordings, independent of duration of cochlear implant use [37].
Assessment LLAEP recordings, which are thought to be
reflective of acoustic signal processing, in cochlear implant users
with ANSD may provide important information for understanding
the variability of speech perception performance results reported
in this population. Prior studies analyzing the LLAEP in individuals
with ANSD, however, have not included cochlear implant users in
their cohorts. For example, the AEPs and psychophysical abilities
were studied in 14 adults with ANSD with the aim of characterizing
their perceptual capacities [38]. The P2/N2 complex was recorded
in all subjects and the P1/N1 complex was obtained in 10/14
subjects; however, when present, the P1/N1 presented with
latencies and amplitudes within the normal range, and no
correlation was observed between AEP parameters and speech
perception scores.
A study examining juvenile hearing aid users (6 months to 7.6
years of age) showed a correlation between cortical potentials (P1,
N1, and P2) and performance on the phonetically balanced
kindergarten speech perception test [39]. The cortical potentials,
which were evoked by tone burst and speech stimuli, were present
in 17/18 children with sensory hearing loss, but only 11/18
children with auditory neuropathy. The latencies and amplitudes
of the cortical potentials did not correlate with subject age or
hearing loss type. There was, however, a trend towards an increase
in latency for the P1 and N1 components with increased degree of
hearing impairment. Furthermore, there was a strong correlation
between the occurrence of cortical potentials and speech percep-
tion score in subjects using hearing aids, indicating that cortical
potentials can be used as an index of perceptual skills and as a
means of assessing the benefits of amplification.
The relationship between speech identification scores and the
latencies and amplitudes of AEP components (P1, N1 and P2) was
also previously investigated in a quiet setting in 10 individuals
with auditory neuropathy and 10 subjects with normal hearing,
ranging in age from 12 to 39 years [40]. The auditory neuropathy
group had significantly worse speech identification scores than the
normal hearing group. Moreover, the mean N1/P2 range in a
subgroup of the auditory neuropathy subjects who showed poor
speech identification was significantly lower than that of normal
hearing subjects as well as that of the auditory neuropathy subjects
in the good speech identification subgroup. Performance in the

Table 2
Summary of previously published mean P1 component amplitudes (SD) in normally hearing children 0–12 years.

Age (y) P1 (mV)

Sharma et al. [11] Satterfield et al. [10] Albrecht et al. [3] Ponton et al. [8] Ceponiene et al. [5] Gilley et al. [6]

LH RH

3 – – – – – – 2.3 (0.9)
4 – – – – – 3.64 (1.16) 2.3 (0.9)
5 – – 2.3 (0.9) 1.3 (0.8) 1.86 (0.56) – 3.2 (1.6)
6 2.6 (0.9) 5.14 2.3 (0.9) 1.3 (0.8) 1.86 (0.56) – 3.2 (1.6)
7 2.4 (0.7) 5.14 2.8 (1.5) 1.4 (0.7) 1.51 (0.60) – 3.6 (1.4)
8 1.8 (1.1) 3.88 2.8 (1.5) 1.4 (0.7) 1.36 (0.61) – 3.6 (1.4)
9 2.6 (1.6) 3.88 2.6 (1.1) 1.8 (0.9) 1.80 (0.82) 4.58 (2.3) 1.6 (0.7)
10 2.0 (1.1) 4.22 2.6 (1.1) 1.8 (0.9) 1.45 (0.57) – 1.6 (0.7)
11 2.0 (0.9) 4.22 0.9 (0.8) 0.8 (0.7) 0.86 (0.56) – 1.9 (1.0)
12 1.6 (1.2) 4.22 0.9 (0.8) 0.8 (0.7) 0.66 (0.56) – 1.9 (1.0)

LH, left hemisphere; RH, right hemisphere.

1334 K.F. Alvarenga et al. / International Journal of Pediatric Otorhinolaryngology 76 (2012) 1332–1338

Table 3
Demographic and clinical characteristics of the present study sample.

Subject Sex Age at testing Age at surgery Cochlear implant device

Internal component Processor Signal processing

model strategy

1 F 8y3m 2y9m Nucleus 24 K Sprint ACE

2 F 6y1m 4y HiRes 90 K Platinum HR-P
Sound Fidelity 120
3 F 6y5m 1y10m Nucleus 24 K Sprint ACE
4 F 8y3m 3y Nucleus 24 K Sprint ACE
5 F 10y3m 3y10m Nucleus 24 K Sprint ACE
6 M 11y 6y2m Nucleus 24 K Sprint ACE
7 M 6y6m 1y10m Nucleus 24 K Sprint ACE
8 F 6y 1y9m Nucleus 24 K Sprint ACE
9 M 5y8m 2y2m Pulsar CI 100 Opus 1 FSP
10 M 4y10m 3y HiRes 90 K Harmony HR-P
Fidelity 120
11 F 8y11m 3y5m Nucleus 24 K Sprint ACE
12 F 11y1m 4y3m Nucleus 24 K Sprint ACE
13 M 9y4m 4y9m Nucleus 24 K Sprint ACE
14 M 9y2m 4y4m Pulsar CI 100 Opus 1 FSP

F, female; M, male; ages are given in condensed combination of years and months (y, m).

speech identification test correlated with the amplitude of cortical
potentials (N1/P2 complex) but not with the latency of cortical
potentials. The authors concluded that measuring cortical poten-
tial can provide a means of predicting perceptual skills in
individuals with auditory neuropathy.
The morphology, latency, and amplitude of the P1 component
were used to evaluate physiological maturity in 21 juvenile
hearing aid users with ANSD, aged 9 months to 11.5 years. And
those data were analyzed relative to the children’s auditory
behavioral development as reflected by their infant-toddler
meaningful auditory integration scale (IT-MAIS) scores [41]. The
authors used the speech stimulus /ba/, presented in at a free-field
intensity of 75 dB hearing level (HL). The P1 records were classified
into three types: normal latency and morphology; normal
morphology with increased latency; and absent or abnormal
response. The group with normal P1 morphology and latency
showed the expected decrease in P1 latency with age, and also
showed greater development of listening skills as reflected by their
IT-MAIS scores. Thus, the authors concluded that P1 appears to be a
good predictor of behavioral outcomes in juveniles with ANSD and
suggested that this component could be used as a clinical tool to
guide decisions related to intervention and to evaluate the
effectiveness of this response in this population.
In light of the aforementioned findings, the primary aim of this
study was to characterize the P1 component of the LLAEP in
implanted individuals with ANSD and correlate parameters of the
P1 component with speech perception performance. Our secondary
aim was to correlate parameters of the P1 component with other
variables related to the use of cochlear implants.
2. Materials and methods
2.1. Setting and subjects
This study was conducted at the Center for Audiological
Research (Centro de Pesquisas Audiológicas, CPA) at the University of
São Paulo, and approved by the Ethics Committee of the National
Survey on Case No. 181/2004. The parents of the enrolled subjects
were informed of the purpose of the study and provided informed
consent at the time of testing.
A total of 14 boys and girls, 4–11 years of age were enrolled in
the study. All 14 subjects had profound prelingual hearing loss
attributable to ANSD, received treatment at the CPA and were
cochlear implant users. The characteristics of the sample, in terms
of gender ratio, age at testing, age at surgery, internal component
model, processor model, and signal processing strategy are
summarized in Table 3. In all cases, the diagnosis of ANSD was
made by an interdisciplinary team based on the results of pre-
surgical tests. The individuals enrolled in this study did not have
any other neurological impairments beyond ANSD, nor did they
exhibit other changes that could compromise auditory and
language development. Patients with hypoplasia or agenesis of
the auditory nerve detected by magnetic resonance imaging in pre-
operative testing were excluded from the study.
Each subject’s skin was cleaned with NuPrep abrasive gel before
the experiment. Disposable MeditraceTM 200 electrodes were
used with TEM 20TM conductive gel for the recording of LLAEPs
and eye-evoked potentials. The impedance of the electrodes was
maintained between 1 and 3 kV. LLAEPs were recording using the
two-channel Smart EP USB Jr. system produced by Intelligent
Hearing Systems. The P1 component of LLAEP research was
conducted following previous study [12]. The electrodes were
placed so that the recording of evoked potentials occurred through
channel A and the recording of eye movements and blinking was
made through channel B.
For channel A, the active electrode was positioned at Cz and
connected to the (+) input of the pre-amplifier and the reference
electrode was placed on the earlobe on the side with the cochlear
implant (A1/A2) and connected to the ( ) input. The ground
electrode was placed at Fpz, connected to the ground position. For
channel B, the active electrode was placed in the supra-orbital
position contralateral to the implant and plugged into the (+) input
of the pre-amplifier and the reference electrode was placed in the
infra-orbital position on the same side and connected to the ( )
input. This arrangement of electrodes was used to allow us to
establish the extent of eye movement and blinking before
recording AEPS so that we could define the appropriate level of
rejection within each test, and thereby minimize artifacts related
to eye movement.
The speech sample was constructed in an acoustically treated
room of the Laboratory of Phonetics and Psycholinguistics
(Laboratorio de Fonetica e Psicolinguistica, LAFAPE) of the Institute
of Language Studies (Instituto de Estudos da Linguagem, IEL), at the
Universidade Estadual de Campinas (UNICAMP) [42]. The emis-
sions were recorded via a unidirectional microphone, placed
directly into the PC card, through the open source program Praat
(www.praat.org), in a 22-kHz sample. The voice of a young adult
male, 22 years of age, with fluid voice quality was used for the
standard speech signal. The syllable /ba/ was extracted from the
second syllable of the utterance of the word /ba’ba/. F1, F2, and F3
 K.F. Alvarenga et al. / International Journal of Pediatric Otorhinolaryngology 76 (2012) 1332–1338
Table 4
Inter-observer comparison of parameters of the P1 component by paired t-test and Dahlberg’s method (1940) of evaluating systematic error and random error.
P1 1st
parameter observer
Mean SD
Latency (ms) 110.00 29.506
Amplitude (mV) 2.80 1.358
p  0.05, statistically significant.
values for the initial and stable portions of the isolated syllable
were verified. Bandwidths were taken from the stable frequency
forming region. With these values, we compiled a script in Praat
(version 2.4.31) and a re-synthesized syllable. The duration of the
synthesized syllable /ba/ was 180 ms. The linguistic stimuli
produced, manipulated, and saved on CD at LAFAPE/UNICAMP,
were scanned and saved on the hard drive of a computer running
USB Smart EP Jr. software. The potentials evoked by acoustic
stimuli presented to the individuals were recorded by the USB
Smart EP Jr. system.
The speech stimulus was presented with a 526-ms inter-
stimulus interval, at an intensity of 70 dB HL and a presentation
rate of 1.9 stimuli/s. The stimuli were applied with a band-pass
filter of 10–30 Hz, and a gain of 100 dB in both channels. On
average, 512 stimuli were applied within each test session. The
response analysis window extended from 100 ms prestimulus to
500 ms poststimulus. The procedure was performed in an open
field, with the speaker positioned at a 908 azimuth, 40 cm away
from the implanted ear.
The system was calibrated in free field hearing level (dB HL)
before the start of the study, with the following characteristics:
power amplifier with 30 W of RMS output, together with a 50-W
RMS speaker with tripod. In the (passive) signal input of the
amplifier, we installed an isolating transformer with an input
impedance of 440 V (impedance equal to the insertion headphone
used in audiometry brainstem response (ABR)) and a 5-kV output
amplifier.
The tests were conducted in a quiet environment. Each subject
was seated comfortably in a reclining chair and instructed to watch
a silent video. Once the presence of AEPs was identified in the
registry through visual observation, the P1 component was
identified and its latency and amplitude were analyzed. The
component’s amplitude was determined as the difference between
the point corresponding to 0.0 mV (baseline record) and the
maximum positive value. The P1 component’s latency was
considered to end at the point of maximum amplitude. The
records were analyzed separately by two audiologists experienced
in auditory electrophysiology to verify the concordance of the
analysis.
Tests 5 and 6 of the GASP [43,44] were applied and analyzed,
enabling us to classify speech perception ability into two levels:
word recognition and comprehension of sentences. The tests were
conducted in a soundproof booth and applied through the MD622
Madsen audiometer at the intensity of 60 dB HL with presentation
in free field at a 08 azimuth. To remove variability in how the tests
were applied, stimuli recorded on CD [45] were utilized, and at the
beginning of each test a calibration of the audiometer volume unit
meter was performed. The test 5 results (range, 0–100%) were
analyzed and test 6 was applied when the subject had a score 50%
on test 5.
The analysis of inter-observer variations was analyzed by Kappa
statistic, which assesses the concordance between the observers
through the paired analysis and shows the percentage of
concordance, which is interpreted by the value of Kappa. The
paired t-error calculation and the error calculation were used to
check the systematic and random error in inter-observer analysis.
1335
2nd Difference t p Random
observer error
Mean SD
107.45 28.133 2.545 0.955 0.362 6.22
2.83 1.372 0.029 0.335 0.744 0.20
The systematic error is significant and its interpretation indicates
that an observer tends to identify larger values of p  0.05. The
random error is an ‘‘average’’ value of the error on the marking of
components presented in the same unit that was measured, in this
study the latency in ms and amplitude in mV.
The Kolmogorov–Smirnov normality test was used to confirm
normal distributions of the datasets, and then parametric tests
were applied. Pearson’s test was used to test for P1 component
correlations with duration of cochlear implant use and duration of
sensorial hearing deprivation.
The k-means clustering procedure was used to divide the
subjects into two groups based on their GASP test results. Student’s
t-tests were used to compare the LLAEP parameters between the
groups. In all analyses p  0.05 was adopted as the significance
level.
3. Results
The two audiologists were found to have good inter-observer
concordance (92.86%, Kappa 0.76). LLAEPs were not recorded in 2/
14 children (14.3%). Systematic error and random error analyses
were carried out on data from subjects in whom the component
had been identified by both observers. The mean latency (SD) and
amplitude (SD) for the P1 components recorded in our subjects are
reported in Table 4 together with the systematic error and random
error data. Notably, as shown in Fig. 1, our Pearson’s correlational
analysis indicated that duration of sensorial hearing deprivation
correlated with the LLAEP P1 latency (p = 0.007, r = 0.7278), but not
the LLAEP P1 amplitude (Pearson’s test: p = 0.171, r = 0.4224).
Duration of cochlear implant use did not correlate with P1 latency
(p = 0.181, r = 0.4142) or P1 amplitude (p = 0.921, r = 0.0323).
A descriptive statistical analysis of sensory deprivation dura-
tion, cochlear implant use duration, P1 latency, and P1 amplitude
for subjects whose performance placed them in the lower
performing cluster (Group 1) and the higher performing cluster
(Group 2) on the GASP test are reported in Table 5. After the
subjects were divided into the two GASP performance groups
(Group 1: subjects 5, 6, 9, 10, and 11; Group 2: subjects 1, 2, 3, 4, 7,
8, 12, 13, and 14) by the k-means clustering procedure (Fig. 2),
Fig. 1. Statistically significant (*p  0.05) relationship between P1 latency and
duration of sensory deprivation. *p  0.05, statistically significant.
1336 K.F. Alvarenga et al. / International Journal of Pediatric Otorhinolaryngology 76 (2012) 1332–1338
Table 5
Descriptive statistical analysis of the P1 component parameters and clinical characteristics of subjects separated by speech perception performance.
Feature Group 1 (lower performers)
Mean SD
Duration of sensorial deprivation 47.80 15.658
Duration of cochlear implant use 49.00 23.569
Latency 134.25 26.132
Amplitude 2.12 0.471
Min, minimum; Max, maximum.
Student’s t-tests revealed that Group 2 had significantly shorter P1
component latencies than Group 1 (p = 0.022).
4. Discussion
The development and neural organization of cortical struc-
tures are influenced by sensory experiences, that is, by
stimulation from the environment [12]. Hearing loss during
the period of greatest plasticity (i.e., the first years of life) results
in sensory deprivation, which prevents normal growth and
proper formation of the connections necessary to form a
functional sensory system. Thus, children with a history of
early sensorial deprivation present anatomical and functional
changes in their auditory system, which in turn affects the
results they can achieve using hearing devices, such as hearing
aids or cochlear implants, since the nervous system is rendered
unable to adequately process afferent activity [17,28,36].
Importantly, if the development of central auditory structures
does not occur normally, it can be assumed that the perceptual
skills that are the basis for speech perception and production
will not develop normally either. On the other hand, with early
diagnosis and intervention, while the central auditory system is
highly plastic and degeneration has not been extensive,
restoration of function may be possible with a prosthesis such
as the cochlear implant [46].
The present findings complement prior research indicating that
the P1 component correlates with speech perception ability and
that a shorter time of deprivation is associated with a P1
component that more closely resembles that found in hearing
children [22–39,47]. ANSD is characterized by compromised
neural synchrony, which is the basis for the compound action
Fig. 2. Speech perception performance of Group 1 (lower performers) and Group 2
(higher performers), divided by application of k-means clustering technique to
GASP tests 5 and 6.
Group 2 (higher performers)
Min Max Mean SD Min Max
37 75 40.55 15.597 23 63
20 75 52.88 13.977 24 70
102 166 97.00 20.709 67 132
1.5 2.49 3.00 1.551 0.8 5.45
potential of the auditory nerve that relays encoding signals from
the cochlea through the midbrain up to the auditory cortex. In
children with congenital ANSD, it has been speculated that sensory
deprivation may alter the maturation process of central auditory
system structures. Some hearing aid users with ANSD have been
reported to show an increase in the latency of the P1 component,
suggesting that the central auditory system is hyporesponsive and
that this hyporesponsivity correlates with compromised speech
perception [39,41].
Since this is the first study, to the best of our knowledge, to
examine the P1 component of the LLAEP in cochlear implant users
with ANSD, it is difficult to compare our findings directly to those
of previous studies, remembering that stimulation of the auditory
system in individuals with ANSD will differ from that in individuals
with sensory hearing loss. The strong inter-observer concordance
observed in our study (Kappa = 0.76, substantial), with no
significant systematic errors for latency and amplitude
(p = 0.362, p = 0.744) and a random error of 6.22 ms for latency
and 0.2 mV for amplitude, provide confidence in our inter-observer
reliability, which is important given the subjectivity that can be
involved in AEP analysis.
Our finding that it was possible to register the P1 component in
85.7% of our subjects shows that electrical stimulation from the
cochlear implant supplied the initial neural dyssynchrony and
generated a P1 component with typical morphology, similar to that
observed in implanted individuals who suffer from sensory
hearing loss [26,31,34], in hearing children [40,48], and in children
with ANSD who are using hearing aids [39,41].
In children diagnosed with ANSD, indicating the use of a
cochlear implant requires the assurance that the hearing aid does
not bring benefits to speech perception, a result observed in a small
percentage of children, but likely to occur. This reflects directly on
the age to indicate the cochlear implant, usually around two years
old according to international recommendations of the NHS
Confederation (2008), and consequently the time of sensory
deprivation.
In this study, we observed a significant, positive correlation
between duration of sensorial hearing deprivation and P1
component latency. A longer duration of sensory deprivation
was associated with a greater P1 component latency. This result
confirms that dyssynchrony observed in these children can also
lead to an abnormal pattern of maturation of the auditory system
[16,34,37]. Such findings have important ramifications for clinical
decisions for children with ANSD and the optimal time for
provision of cochlear implants. One must question whether
carrying out testing with hearing aids in this population for an
extended period of time may be preventing stimulation of the
auditory system that could be achieved with a cochlear implant in
a period crucial to the development of cortical structures and
acquisition of listening skills and language.
Our negative finding of no correlation between P1 component
parameters and duration of cochlear implant use differs from
previously reported findings in cochlear implant users with
sensory hearing loss [14,16–18,37]. This unexpected finding
should be researched further with controls for more variables,
 K.F. Alvarenga et al. / International Journal of Pediatric Otorhinolaryngology 76 (2012) 1332–1338
such as the stimulation the child receives, family collaboration and
involvement, and participation in speech therapy, among other
variables, which can affect the results achieved with a cochlear
implant.
The dissociation of P1 component latency that we observed
between subjects with better versus worse performance in the
GASP test suggests that prior development of central auditory
structures, reflected in the P1 component, is related to real
differences in behavioral auditory skills [30,38–40]. That is, our
findings indicate that a lesser P1 latency is predictive of better
GASP test performance.
The two children (14.3%) for which LLAEPs could not be
detected had vastly different speech perception performance on
the GASP test. One scored 0% on the sentence comprehension
part of the GASP test, and the other scored 100%. The unexpected
finding of an absence of the P1 component in the child with good
speech proficiency, in principle, could be explained by the way
the LLAEPs were evoked: through a passive paradigm, in which
the child was not asked to pay attention to the stimuli
presented. Attending to the stimulus can have a major effect
on the recording of cortical potentials in individuals with
auditory neuropathy; attending has been reported to shift
latency or even produce a shift from the absence to the presence
of a response [48].
Correlation between a P1 component parameter and speech
perception is extremely important since in children with ANSD,
determining the functional gain with a hearing aid (i.e., the
threshold for behavioral audiometric frequencies of speech) has
no predictive value for speech perception performance. Thus, as
found in children with sensory hearing loss, in children with
ANSD, the P1 component has the potential to serve as a predictor of
performance in those who use cochlear implants for speech
perception [39,48–50].
In conclusion, it was possible to register the P1 component in
implanted children diagnosed with ANSD, and P1 component
latency correlated with speech perception performance and
with duration of sensory deprivation. These findings indicate
that, in children with ANSD, the P1 component has the potential
to serve as a marker of the development of auditory cortical
structures and a predictor of the child’s potential for speech
perception.
References
[1] C. Ponton, J.J. Eggermont, D. Khosla, B. Kwong, M. Don, Maturation of human
central auditory system activity: separating auditory evoked potentials by dipole
source modeling, Clin. Neurophysiol. 113 (3) (2002) 407–420.
[2] M.F. Dorman, A. Sharma, P. Gilley, K. Martin, P. Roland, Central auditory develop-
ment: evidence from CAEP measurements in children fit with cochlear implants, J.
Commun. Disord. 40 (4) (2007) 284–294.
[3] R. Albrecht, W.V. Suchodoletz, R. Uwer, The development of auditory evoked
dipole source activity from childhood to adulthood, Clin. Neurophysiol. 111 (12)
(2000) 2268–2276.
[4] A.B. Barnet, Auditory evoked potentials during sleep in normal children from ten
days to three years of age, Electroencephalogr. Clin. Neurophysiol. 39 (1) (1975)
29–41.
[5] R. Ceponiene, T. Rinne, R. Näätänen, Maturation of cortical sound processing as
indexed by event-related potentials, Clin. Neurophysiol. 113 (6) (2002) 870–882.
[6] P.M. Gilley, A. Sharma, M. Dorman, K. Martin, Developmental changes in refrac-
toriness of the cortical auditory evoked potential, Clin. Neurophysiol. 116 (2005)
648–657.
[7] E.S. Ohlrich, A.B. Barnet, Auditory evoked responses during the first year of life,
Electroencephalogr. Clin. Neurophysiol. 32 (2) (1972) 161–169.
[8] C.W. Ponton, J.J. Eggermont, B. Kwong, M. Don, Maturation of human central
auditory system activity: evidence from multi-channel evoked potentials, Clin.
Neurophysiol. 111 (2) (2000) 220–236.
[9] J.H. Satterfield, B.W. Braley, Evoked potentials and brain maturation in hyperac-
tive and normal children, Electroencephalogr. Clin. Neurophysiol. 43 (1) (1977)
43–51.
[10] J.H. Satterfield, A.M. Schell, R.W. Backs, K.C. Hidaka, A cross-sectional and longi-
tudinal study of age effects of electrophysiological measures in hyperactive and
normal children, Biol. Psychiatry 19 (7) (1984) 973–990.
1337
[11] A. Sharma, N. Kraus, T.J. McGee, T.G. Nicol, Developmental changes in P1 and N1
central auditory responses elicited by consonant–vowel syllables, Electroence-
phalogr. Clin. Neurophysiol. 104 (November (6)) (1997) 540–545.
[12] L.M. Ventura, O.A. Costa, K.F. Alvarenga, Central hearing system maturation in
normally hearing children, Pró-Fono Revista de Atualização Cientı́fica 21 (abr–jun
(2)) (2009).
[13] M. Pelizzone, A. Kasper, R. Hari, J. Karhu, P. Montandon, Bilateral electrical
stimulation of a congenitally-deaf ear and of an acquired-deaf ear, Acta Otolar-
yngol. 111 (2) (1991) 263–268.
[14] C.W. Ponton, M. Don, J.J. Eggermont, M.D. Waring, B. Kwong, A. Masuda, Auditory
system plasticity in children after long periods of complete deafness, Neuroreport
8 (1) (1996) 61–65.
[15] C.W. Ponton, M. Don, J.J. Eggermont, M.D. Waring, A. Masuda, Maturation of
human cortical auditory function: differences between normal-hearing children
and children with cochlear implants, Ear Hear. 17 (5) (1996) 430–437.
[16] J.J. Eggermont, C.W. Ponton, M. Don, M.D. Waring, B. Kwong, Maturational delays
in cortical evoked potentials in cochlear implant users, Acta Otolaryngol. 117 (2)
(1997) 161–397.
[17] A. Sharma, M.F. Dorman, A.J. Spahr, Rapid development of cortical auditory
evoked potentials after early cochlear implantation, Neuroreport 13 (10)
(2002) 1365–1368.
[18] P.W. Bauer, A. Sharma, K. Martin, M. Dorman, Central auditory development in
children with bilateral cochlear implants, Arch. Otolaryngol. Head Neck Surg. 132
(10) (2006) 1133–1136.
[19] S. Burdo, S. Razza, F. Di Berardino, G. Tognola, Auditory cortical responses in
patients with cochlear implants, Acta Otorhinolaryngol. Ital. 26 (2) (2006) 69–77.
[20] L. Friesen, K. Tremblay, Acoustic change complexes recorded in adult cochlear
implant listeners, Ear Hear. 27 (6) (2006) 678–685.
[21] J. Guiraud, S. Gallego, L. Arnold, P. Boyle, E. Truy, L. Collet, Effects of auditory
pathway anatomy and deafness characteristics? Part 2: On electrically evoked
late auditory responses, Hear. Res. 228 (1–2) (2007) 44–57.
[22] P.A. Groenen, M. Makhdoum, J.L. van den Brink, M.H. Stollman, A.F. Snik, P. van
den Broek, The relation between electric auditory brain stem and cognitive
responses and speech perception in cochlear implant users, Acta Otolaryngol.
116 (6) (1996) 785–790.
[23] P.R. Kileny, A. Boerst, T. Zwolan, Cognitive evoked potentials to speech and tonal
stimuli in children with implants, Otolaryngol. Head Neck Surg. 117 (3) (1997)
161–169.
[24] M. Okusa, T. Shiraishi, T. Kubo, Y. Nageishi, Effects of discrimination difficulty on
cognitive event-related brain potentials in patients with cochlear implants,
Otolaryngol. Head Neck Surg. 121 (5) (1999) 610–615.
[25] A.J. Beynon, A.F. Snik, P. Van den Broek, Evaluation of cochlear implant
benefit with auditory cortical evoked potentials, Int. J. Audiol. 41 (7)
(2002) 429–435.
[26] J. Maurer, L. Collet, H. Pelster, E. Truy, S. Gallégo, Auditory late cortical response
and speech recognition in Digisonic cochlear implant users, Laryngoscope 112
(12) (2002) 2220–2224.
[27] C. Pantev, B. Ross, A. Wollbrink, M. Riebandt, K.W. Delank, E. Seifert, et al.,
Acoustically and electrically evoked responses of the human cortex before and
after cochlear implantation, Hear. Res. 171 (1–2) (2002) 191–195.
[28] A. Sharma, E. Tobey, M. Dorman, S. Bharadwaj, K. Martin, P. Gilley, et al., Central
auditory maturation and babbling development in infants with cochlear
implants, Arch. Otolaryngol. Head Neck Surg. 130 (5) (2004) 511–516.
[29] S. Singh, A. Liasis, K. Rajput, A. Towell, L. Luxon, Event-related potentials in
pediatric cochlear implant patients, Ear Hear. 25 (6) (2004) 598–610.
[30] K.A. Gordon, S. Tanaka, B.C. Papsin, Atypical cortical responses underlie poor
speech perception in children using cochlear implants, Neuroreport 16 (18)
(2005) 2041–2045.
[31] A.S. Kelly, S.C. Purdy, P.R. Thorne, Electrophysiological and speech perception
measures of auditory processing in experienced adult cochlear implant users,
Clin. Neurophysiol. 116 (6) (2005) 1235–1246.
[32] S. Roman, G. Canévet, P. Marquis, J.M. Triglia, C. Liégeois-Chauvel, Relationship
between auditory perception skills and mismatch negativity recorded in free field
in cochlear-implant users, Hear. Res. 201 (1–2) (2005) 10–20.
[33] C. McNeill, M. Sharma, S.C. Purdy, Are cortical auditory evoked potentials useful in
the clinical assessment of adults with cochlear implants? Cochlear Implants Int.
10 (Suppl. 1) (2009) 78–84.
[34] K.A. Gordon, S. Tanaka, D.D. Wong, B.C. Papsin, Characterizing responses from
auditory cortex in young people with several years of cochlear implant experi-
ence, Clin. Neurophysiol. 119 (10) (2008) 2347–2362.
[35] C. McNeill, M. Sharma, S.C. Purdy, K. Agung, Cortical auditory evoked responses
from an implanted ear after 50 years of profound unilateral deafness, Cochlear
Implants Int. 8 (4) (2007) 189–997.
[36] A. Sharma, M.F. Dorman, A.J. Spahr, A sensitive period for the development of the
central auditory system in children with cochlear implants: implications for age
of implantation, Ear Hear. 23 (6) (2002) 532–539.
[37] A. Sharma, M.F. Dorman, A. Kral, The influence of a sensitive period on central
auditory development in children with unilateral and bilateral cochlear implants,
Hear. Res. 203 (1–2) (2005) 134–143.
[38] A.U. Kumar, M. Jayaram, Auditory processing in individuals with auditory neu-
ropathy, Behav. Brain Funct. 1 (2005) 21.
[39] G. Rance, B. Cone-Wesson, J. Wunderlich, R. Dowell, Speech perception and
cortical event related potentials in children with auditory neuropathy, Ear Hear.
23 (3) (2002) 239–253.
[40] V.K. Narne, C. Vanaja, Speech identification and cortical potentials in individuals
with auditory neuropathy, Behav. Brain Funct. 4 (2008) 15.
1338 K.F. Alvarenga et al. / International Journal of Pediatric Otorhinolaryngology 76 (2012) 1332–1338
[41] A. Sharma, G. Cardon, K. Henion, P. Roland, Cortical maturation and behavioral
outcomes in children with auditory neuropathy spectrum disorder, Int. J. Audiol.
50 (2) (2011) 98–106.
[42] M. Banhara, Potenciais auditivos de longa latência: N1, P2, N2 e P300 evocados
por estı́mulo de fala em usuários de implante coclear, Dissertação (Mestrado),
Universidade de São Paulo, São Paulo, 2007.
[43] M.C. Bevilacqua, E.A. Tech, Elaboração de um procedimento de avaliação de
percepção de fala em crianças deficientes auditivas profundas a partir de cinco
anos de idade, in: I.Q. Marchesan, J.M. Zorzi, I.C.D. Gomes (Org.), Tópicos em
Fonoaudiologia, Lovise, São Paulo, 1996, pp. 411–433.
[44] N.P. Erber, Auditory Training, Alexander Graham Bell Association for the Deaf,
Washington, 1982.
[45] C.A. Quintino, Desenvolvimento de um software para avaliação da percepção de
fala em crianças deficientes auditivas, Dissertação (Mestrado), Universidade de
São Paulo, São Paulo, 2007.
[46] P.M. Gilley, A. Sharma, M.F. Dorman, Cortical reorganization in children with
cochlear implants, Brain Res. 1239 (2008) 56–65.
[47] K. Kurnaz, B. Satar, S. Yetiser, Evaluation of cochlear implant users’ performance
using middle and late latency responses, Eur. Arch. Otorhinolaryngol. 266 (3)
(2009) 343–350.
[48] H.J. Michalewski, A. Starr, T.T. Nguyen, Y.Y. Kong, F.G. Zeng, Auditory temporal
processes in normal-hearing individuals and in patients with auditory neuropa-
thy, Clin. Neurophysiol. 116 (3) (2005) 669–680.
[49] W. Pearce, M. Golding, H. Dillon, Cortical auditory evoked potentials in the
assessment of auditory neuropathy: two case studies, J. Am. Acad. Audiol. 18
(5) (2007) 380–390.
[50] B. Cone, The electrophysiology of auditory neuropathy spectrum disorder, in:
Guidelines for Identification and Management of Infants and Young Children with
Auditory Neuropathy Spectrum Disorder, NHS Confederation, Aurora, 2008, pp.
20–27.