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Inicio Acta Otorrinolaringológica Española Auditory steady-state response in cochlear implant patients
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Vol. 69. Núm. 5.
Páginas 268-274 (Septiembre - Octubre 2018)
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Vol. 69. Núm. 5.
Páginas 268-274 (Septiembre - Octubre 2018)
Original article
DOI: 10.1016/j.otorri.2017.08.007
Acceso a texto completo
Auditory steady-state response in cochlear implant patients
Potenciales evocados auditivos de estado estable en pacientes con implante coclear
Alejandro Torres-Fortunya, Isabel Arnaiz-Marqueza,
Autor para correspondencia

Corresponding author.
, Heivet Hernández-Pérezb, Eduardo Eimil-Suáreza
a Audiology Department, Cuban Neuroscience Center, Havana, Cuba
b Centre for Language Sciences, Linguistics Department, Macquarie University, Sydney, NSW, Australia
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Figuras (2)
Tablas (4)
Table 1. Description of the study sample according to the etiology of each subject.
Table 2. References free field thresholds for equipment calibration.
Table 3. Physiological and behavioral thresholds.
Table 4. Regression analysis between ASSR amplitude and masking Intensities.
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Introduction and objective

Auditory steady state responses to continuous amplitude modulated tones at rates between 70 and 110Hz, have been proposed as a feasible alternative to objective frequency specific audiometry in cochlear implant subjects. The aim of the present study is to obtain physiological thresholds by means of auditory steady-state response in cochlear implant patients (Clarion HiRes 90K), with acoustic stimulation, on free field conditions and to verify its biological origin.


11 subjects comprised the sample. Four amplitude modulated tones of 500, 1000, 2000 and 4000Hz were used as stimuli, using the multiple frequency technique. The recording of auditory steady-state response was also recorded at 0dB HL of intensity, non-specific stimulus and using a masking technique.


The study enabled the electrophysiological thresholds to be obtained for each subject of the explored sample. There were no auditory steady-state responses at either 0dB or non-specific stimulus recordings. It was possible to obtain the masking thresholds. A difference was identified between behavioral and electrophysiological thresholds of −6±16, −2±13, 0±22 and −8±18dB at frequencies of 500, 1000, 2000 and 4000Hz respectively.


The auditory steady state response seems to be a suitable technique to evaluate the hearing threshold in cochlear implant subjects.

Auditory steady state response
Cochlear implant
Electromagnetic artifact
Free field
Masking technique
Objective measures
Introducción y objetivos

Los potenciales evocados auditivos de estado estable (PEAEE) por estimulación con tonos modulados en amplitud entre 70 y 110Hz han sido propuestos como una alternativa factible para realizar una audiometría objetiva en pacientes con implante coclear. El objetivo del presente estudio es verificar el origen biológico de los umbrales auditivos obtenidos mediante PEAEE por estimulación acústica y en condiciones de campo libre, en pacientes con implante coclear (Clarion HiRes 90K).


La muestra constó de 11 pacientes. Cuatro tonos modulados en amplitud con frecuencias portadoras de 500, 1.000, 2.000 y 4.000Hz y presentados simultáneamente fueron empleados como estímulo. Se registraron series de intensidad hasta alcanzar el umbral auditivo, así como registros a 0dB HL, con estímulos no específicos y empleando técnicas de enmascaramiento.


El estudio permitió obtener los umbrales electrofisiológicos par cada paciente de la muestra explorada. No hubo respuesta de estado estable ni a 0dB ni al emplear estímulos no específicos. Fue posible obtener los umbrales de enmascaramiento. Se identificó una diferencia entre los umbrales conductuales y electrofisiológicos de −6±16dB, −2±13dB, 0±22dB y −8±18dB a las frecuencias de 500, 1.000, 2.000 y 4.000Hz, respectivamente.


Los PEAEE pueden constituir una técnica apropiada para evaluar el umbral auditivo en sujetos con implante coclear.

Palabras clave:
Potenciales evocados auditivos de estado estable
Implante coclear
Dispositivos electromagnéticos
Campo libre
Medidas objetivas
Texto completo

Audiology specialists often use cochlear implants as a treatment for patients with severe to profound hearing loss. Common techniques used to set map parameters for individual electrodes are Neural Response Telemetry (NRT)1–3 and electrical auditory brainstem response.4–6 Once the cochlear implant is set, behavioral audiometry in free-field conditions reveals information about how the device is working at conversational speech levels. The success of cochlear implantation in very young children (less than 2 years7–10) highlights the need of objective measures to assess hearing sensitivity.

Auditory steady state responses (ASSR) to continuous tones modulated in amplitude may be an approach that allowing for automated objective evaluation of audition. To evoke the ASSR stimulation can be trough by air conduction (headphones or insert earphones or loudspeaker), bone conduction (bone vibrator), or electrical (in cochlear implant subjects). ASSRs generated using headphones have extensively studied and it provides reasonably reliable estimates of hearing thresholds, e.g. in hearing impaired subjects to within 12–15dB HL of the behavioral thresholds.11–17 ASSRs to multiple continuous amplitude modulated (AM)-tones have previously been recorded in sound-field conditions in subjects with hearing aids18–20 and young candidates for cochlear implant.21,22 ASSR to multiple frequencies tones under free-sound-field conditions can provide valid hearing thresholds information and an objective indication of a patient's response to sound similar to speech. These measurements allow demonstrating the utility of the cochlear implant as part of the rehabilitation/information giving process and an outcome measure for discussion with parents of cochlear implant children.

A major barrier to using any auditory evoked potentials to evaluate cochlear implant subjects with electrical stimulation is the frequent occurrence of electromagnetic artifacts. Researchers have reported frequent electromagnetic contamination during ASSR recordings.23–25 Several techniques are available to remove the cochlear implant artifact,26–29 but they have not proven to be entirely satisfactory.30 That is why any methods used to evaluate cochlear implants must consider these kinds of artifact.

The aim at recording ASSRs in cochlear implant patients using acoustic stimulation in sound-field conditions it is to determine if such artifacts are capable of contaminating the recordings. Validating the use of ASSRs in these conditions, also provide more data that will highlight the significance of introducing ASSR into routine clinical examinations and practice. Moreover, ASSR recordings in sound-field conditions can help to demonstrate that any available commercial device might assess the auditory sensitivity in cochlear implant patients.


Eleven subjects (4 of which were females), took part in this study with chronological ages ranging between 10 and 19 years (14±3). Their auditory ages (time since the cochlear implants were activated) were between 3 and 8 years. All subjects used Clarion HiRes 90K (Advanced Bionics Corp) cochlear implants, unilaterally. In all cases, behavioral thresholds to warble tones on free field conditions were obtained using a Madsen Orbiter 922 audiometer while the subject was lying comfortably in a bed. For this purpose, the psycho-acoustic technique of ascending and descending limits 10dB up and 5dB down31 was used. An informed consent was obtained from the subjects’ parents. The sample was heterogenic according to the etiology of the hearing loss (see Table 1).

Table 1.

Description of the study sample according to the etiology of each subject.

Code  Etiology 
DMS  Ototoxicity 
NMM  Genetics 
APS  Etiology not specified 
GSM  Bacterial meningoencephalitis 
SMS  Bacterial meningoencephalitis 
JSMO  Etiology non-specified 
AGS  Ototoxicity 
LGC  Bacterial meningoencephalitis 
YRV  Ototoxicity 
GCH  Ototoxicity 
YJP  Genetics 
Auditory stimuli

The stimuli were delivered by the AUDIX system (NEURONIC S.A., Havana). The output of the system was directly connected to the loudspeaker (B&W Loudspeakers, Ltd; DM 601 S3): output of 100w/8Ω, frequency response of 60Hz–22kHz (−3dB) on reference axis. The stimuli consisted of a combination of four sinusoidal carrier tones of 500, 1000, 2000 and 4000Hz modulated in amplitude (95% depth) at the following rates: 104.2, 107.8, 111.4 and 115Hz, respectively. They were presented binaurally with the subject facing a single loudspeaker. The tones were summed to create the multiple frequency stimuli.

The stimuli was calibrated in free field conditions following the ISO 389-7 (1998) standard provides reference sound field hearing thresholds for calibrations purposes where the sound source is at frontal position (0° azimuth; see Table 2). All measurements were made using the Brüel & Kjaer sound level meter (Investigator 2250). The microphone type 4189 was located at the same position as the subject's head should be positioned during the recording. Each carrier frequency was adjusted in intensity according to the audibility differences among the individual tones. The stimuli were calibrated in dB HL and loudspeaker reproduced it accurately.

Table 2.

References free field thresholds for equipment calibration.

Frequency (Hz)  Free-field 
  (dB ref. 20μPA) 
125  22 
160  18 
200  14.5 
250  11 
315  8.5 
630  2.5 
1250  1.5 
1500  0.5 
2000  −1.5 
2500  −4.0 
3000  −6 
3150  −6.5 
4000  −6.5 
5000  −3 
6000  2.5 
8000  11.5 

Electrode discs of Ag/AgCl were fixed with electrolytic paste at Cz (positive), 2.5cm below inion (negative), and at Fpz (ground). Impedance values were kept below 5kΩ at 10Hz. The bioelectric activity was amplified with a resolution of 16bit (0.012μV) and 48dB/octave analog-filtered between 10 and 300Hz. The responses were averaged between 7 and 24 epochs of 8192 samples (digitized with a sampling period of 1.08ms and a sampling rate of 920Hz). Epochs containing electrophysiological activity exceeding ±25μV were rejected. From further analysis taking in consideration the number of averaged epochs and the artifact rejection the final recording times were between of 5 and 15min. Subjects reposed comfortably on a bed in a sound treated room (3m×3m). The test booth interior was dimly lit, and the subjects were encouraged not to move, to relax and to fall asleep in order to reduce the residual noise level (RNL). The subjects were watched during recordings through the room's window. If subjects moved their head on falling asleep, the recordings were stopped and the head was repositioned.

The measurements were made using a 1/3 octave bands in dB SPL (LAeq). The level per cycle of the ambient noise measured on the vicinity of the test frequencies 500, 1000, 2000, and 4000Hz was approximately 31, 30, 30 and 31dB SPL respectively and the global environment noise was 35dB SPL.

Experimental design

Physiological thresholds were determined by the presence or absence of recognizable ASSR recorded in all subjects. For suprathresholds intensities the ASSR were always averaged with a minimum of 7 epochs. Our stopping criteria were a residual noise level lower than 0.002μV through a maximum number of 24 sweeps. The multiple-frequencies stimulus was presented in a series of decreasing intensities (steps of −10dB HL; from 70dB HL until reaching the individuals’ physiological thresholds). Subjects were lying comfortably on a bed (same behavioral thresholds conditions) to avoid any ear level differences.

In order to explore whether ASSR recordings contain electromagnetic artifacts, it was measured the effects of masking noise on ASSR at increased intensities, similar to the procedure described by Dimitrijevic and his colleagues32 during recording of ASSR with bone stimulation.

The masking stimulus was a white noise generated by a clinical audiometer (Madsen Orbiter 922) and delivered by a second loudspeaker (F-GM240, TOA Corporation): output of 150w/8Ω, frequency response of 65Hz–20kHz (−10dB) on reference axis. The loudspeakers were situated in front of the subjects at one meters of distance. This corresponds to more than three wavelengths at 500Hz and above, at 0° azimuth at all times. The two loudspeakers were one above the other and aligned with subject's head, making the sound incidence angle of both loudspeakers similar.

The first step in this experimental condition was to record a reference ASSR amplitude. For this purpose, the ASSR was recorded at a supra-threshold intensity of 50dB HL in absence of masking noise (clinical audiometer turned off).

The second step was to fix the multiple frequencies stimuli at 50dB HL and record the ASSR in presence of the masking noise. The idea to use masking technique to discriminate between physiological and artifactual responses remains on the fact that, if the obtained data contain physiological elements, the ASSR amplitude might decrease with the same rate at which the masking intensity increase. On the contrary, if the obtained data only contain artifactual elements, an independent relation between the ASSR amplitude and masking intensity should be expected. Fig. 1 illustrates this idea considering ASSR at 2000Hz of stimulation frequency.

Figure 1.

Expected behavioral rate among ASSR amplitude (at 2000Hz) and masking levels according to the presence of physiological elements.


The masking noise was not synchronized with the ASSR recording. Rather it was always delivered before the presentation of the multiple frequency stimuli. The masking noise was presented in 5 and 10dB HL steps over the individual physiological thresholds until the ASSR could not be recorded. The masking threshold was defined as the intensity of masking noise at which the four carrier frequencies were recorded for the last time. However, due to the time expenses, data was only recorded for two participants.

Statistical analysis

It was considered a variant of the multivariate Hotelling T2 statistic33,34 for assessing the presence of a significant steady state response at each explored frequency; and thus, to determinate the physiological thresholds data set.

Subsequent statistical analyses were carried out using Statistic 8.0 desktop application.

Mean and standard deviations for physiological and behavioral thresholds were computed as well as the differences between (among) them. Due to the absent of normality on the sample, a Wilcoxon Matched Pairs Test (p<0.01) was considered for estimating statistical differences among physiological and behavioral thresholds at each frequency.

It was also computed a Nonparametric Spearman Rank Order Correlations for each frequency considering as null hypothesis a non-correlation between curves (p<0.05).

In order to discriminate among physiological and artifactual elements, a linear model between ASSR amplitude and masking noise intensity was fitting for each carrier frequency explored, under the null hypothesis of β=0 (p<0.05).

ResultsBehavioral and physiological thresholds

Table 3 shows the physiological thresholds obtained for a sample of 11 subjects with cochlear implants. Non-parametric statistical comparisons did not reveal significant differences between physiological and behavioral thresholds for 500Hz (Z=0.25, p=0.80); 1000Hz (Z=0.53, p=0.59); 2000Hz (Z=0.00, p=1.00) and 4000Hz (Z=1.69, p=0.09). Consequently, previous exposed data did not reveal a well-established result of lower behavioral thresholds in compared to physiological thresholds. The linear correlation between thresholds for all frequencies in cochlear implant participants was not significant: 500Hz (r=0.47; p-level=0.15); 1000Hz (r=0.42; p-level=0.19); 2000Hz (r=0.1; p-level=0.77); 4000Hz (r=0.68; p-level=0.001) and overall correlation (r=−0.31; p-level=0.35).

Table 3.

Physiological and behavioral thresholds.

Thresholds  Frequencies (Hz)
  500  1000  2000  4000 
Behavioral  48±44±13  42±14  43±12 
Physiological  42±16  42±13  42±15  35±10 
Mean±SD (dB HL) 
−6±16  −2±13  0±22  −8±18 
Masking experiment

Data recorded during the masking experiment confirmed the idea of an inverse relation between the intensity level of masking noise and the amplitude of the ASSR, which totally disappears when the masking noise intensity is higher enough than the intensity level of the steady-sate stimulus.

Fig. 2 shows the behavior of ASSR amplitudes at masking noise presentation for the masking experiment. Note that no ASSRs were obtained at masking noise intensities of 65dB HL (masking threshold).

Figure 2.

ASSR amplitude versus masking noise intensity. Data from two subjects are given. The multiple frequency stimuli were set in 50dB HL (suprathreshold intensity for the two subjects recorded). The ASSR amplitude (Y axis) is expressed in (uV). Masking noise intensity (X axis) is expressed in dB HL. Note that the ASSR amplitude for the four modulation frequencies decreases when masking noise increases, reaching an intensity value where no ASSR was recorded (masking thresholds).


The linear model between ASSR amplitude and masking noise intensity was a necessity in order to discriminate between physiological and artifactual elements in our data. A slope hypothesis test was performed under the null hypothesis of β=0, which corresponds to no relationship between ASSR amplitude and masking intensities. The majority of the carrier frequencies explored rejected this null hypothesis for a significant level of 0.05. The linear regression for both subjects, at each carrier frequencies explored is shown in Table 4. Three parameters are presented: the regression slope (β) with the corresponding standard error (St. Err. β) and p-value. An asterisk denotes statistical significance for an alpha level of 0.05.

Table 4.

Regression analysis between ASSR amplitude and masking Intensities.

Carrier (Hz)  Subject 1Subject 2
  β  St. Err. β  p-value  β  St. Err. β  p-value 
500  −0.59  0.47  0.29  −0.98  0.13  0.01* 
1000  −0.88  0.27  0.048*  −0.99  0.05  0.002* 
2000  −0.8  0.34  0.1  −0.99  0.11  0.012* 
4000  −0.98  0.1  0.004*  −0.99  0.07  0.004* 

Representa la significación estadsitica.

The results show that ASSR amplitude decreases significantly as the intensity of masking noise increases, suggesting that the responses recorded in cochlear implants participants were not merely artifacts but true biological components.

DiscussionBehavioral and physiological thresholds

The main criterion used to evaluate the accuracy of an electroaudiometric method for assessing audition in patients with cochlear implants is the correlation between physiological and behavioral hearing thresholds. Past research on ASSR has reported differences of 6–14dB HL for audiometric frequencies between 500 and 4000Hz in hearing impaired subjects.11–17,35–37 These differences are similar to other commonly used methods such as ABR (12–15dB HL).38 Typically, reports of physiological thresholds are always higher than behavioral thresholds. However, the results reported here showed an opposite pattern which probably translates into an inaccurate estimation of the behavioral thresholds. Importantly, Attias et al.22 reported similar unreliable audiograms under free-field stimulation in cochlear implants candidates and subjects with auditory neuropathy. Similar results were found by Yang et al.24 in children with cochlear implants. The inherent imprecision in the behavioral testing of subjects who have suffered of profound hearing disabilities for a long time may explain the lacks of correlations between the two measures. Under this condition, sound detection is difficult, especially at threshold levels. This may translate into an increase in the inherent variability of the tonal audiometric test (accepted between ±10dB HL).39 Unreliable behavioral threshold estimations may explain the differences between physiological and behavioral thresholds in our experiment.

Masking experiment

Cochlear implant artifacts are probably a consequence of the capacitive coupling between the transmission radio-frequency cable and the voltage differences produced by the derive-current through body tissue. Electrical pulses generated by the electrodes of the implant can also contribute to the artifact contamination. In contrast to the electrical stimulation, acoustical stimulation allows the use of amplitude modulated tones and thereby the evaluation of the speech processor based upon its regular parameters. Note, however, that studies of ASSR using acoustical stimulation40–42 also described artifacts induced by the closeness between the stimulus transducers (headphone and bone vibrator) and the recording electrodes.

Previous studies have employed masking techniques to check for the presence of electromagnetic artifacts during recording of ASSR with bone stimulation.32 The authors showed that the effect of masking noise relies on a significantly reduction of the physiological thresholds as masking level increases. In addition, Menard and collaborators,23 assume that the signal component resulting from the artifact must grow linearly as a function of stimulation levels. Our hypothesis in using masking technique relies on masking levels might not affect electrical artifacts, which might grow linearly as stimulus levels increase. On the other hand, the presence of masking noise certainly affects ASSR amplitude unless it reached masking thresholds, suggesting that the responses recorded in subjects with cochlear implants were not merely artifacts but real/typical physiological responses.

We are confident that our recordings contain real biological responses, because free-sounds-field stimulation can suppress or eliminates the artifact induced by stimulus transducer. Moreover, Gilley et al.28 described that artifact components are distributed over the scalp with maximum amplitude next to the implant, with an isopotential contour typically extending to Cz and across the forehead. Consequently, the middle-line electrode array used here may contribute to avoid and/or minimize the cochlear implant artifact.


It was possible to estimate Physiological thresholds in cochlear implant subjects by means of using ASSR to Multiple Amplitude-Modulated tones under sound-field conditions. However, obtained results did not demonstrate the predictive value of ASSR under free-sound-field conditions. Results of the masking experiment showed that ASSR recordings were not merely electromagnetic artifacts. An important perspective is to replicate these findings on a large number of participants with different etiologies, as well as to test cochlear implant patients with different cochlear implant models. In addition, it is necessary to explore different ASSR intrinsic parameters, such as amplitude, phase and their variations as a function of stimulation intensities.

Conflict of interest

Authors declare no conflict of interest.

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